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Green Algae and the Origins of Multicellularity in the Plant Kingdom

James G. Umen

Donald Danforth Plant Science Center, St. Louis, Missouri 63132 Correspondence: [email protected]

The green lineage of chlorophyte algae and streptophytes form a large and diverse clade with multiple independent transitions to produce multicellular and/or macroscopically complex organization. In this review, I focus on two of the best-studied multicellular groups of green algae: charophytes and volvocines. Charophyte algae are the closest relatives of land plants and encompass the transition from unicellularity to simple multicellularity. Many of the innovations present in land plants have their roots in the cell and developmental biology of charophyte algae. Volvocine algae evolved an independent route to multicellularity that is captured by a graded series of increasing cell-type specialization and developmental com- plexity. The study of volvocine algae has provided unprecedented insights into the innova- tions required to achieve multicellularity.

he transition from unicellular to multicellu- and rotifers that are limited by prey size (Bell Tlar organization is considered one of the ma- 1985; Boraas et al. 1998). Reciprocally, increased jor innovations in eukaryotic evolution (Szath- size might also entail advantages in capturing ma´ry and Maynard-Smith 1995). Multicellular more or larger prey. organization can be advantageous for several There is some debate about how easy or reasons. Foremost among these is the potential difficult it has been for unicellular organisms for cell-type specialization that enables more to evolve multicellularity (Grosberg and Strath- efficient use of scarce resources and can open mann 2007). A conceptual division of multi- up new adaptive niches (Stanley 1973; Szath- cellularity into two classes, simple and complex, ma´ry and Maynard-Smith 1995; Ispolatov et has also been proposed (Knoll 2011). How- al. 2012). In addition, multicellularity allows ever, the argument that simple multicellulari- organismal size to scale independently of cell ty is easier to achieve than complex multicellu- size, thus freeing organisms from the constraints larity may be less compelling than it seems at of individual cells and allowing them to evolve first glance. In the 2-billion year history of fundamentally new relationships with their eukaryotic life, “simple” multicellularity has physical and biological surroundings (Beardall arisen about two dozen times (Grosberg and et al. 2009). A third potential advantage of mul- Strathmann 2007; Knoll 2011; Adl et al. 2012). ticellularity and increased organismal size is es- In contrast, complex multicellularity (defined cape from microscopic predators such as ciliates by three-dimensional body plans and multiple

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J.G. Umen

cell types) has only arisen a few times with “toolkits” available in unicellular ancestors, as animals and plants being clear examples, and well as on the specific circumstances and envi- fungi, brown algae and red algae achieving ronment in which multicellularity arose (Rokas somewhat lesser extents of complexity. In any 2008; Knoll 2011; Bowman 2013; Niklas and case, because complex multicellularity almost Newman 2013; Smolarkiewicz and Dhonukshe certainly evolved from simple multicellularity, 2013). By examining the origins of multicellu- the odds of going from simple to complex mul- larity in diverse lineages, it can be determined ticellularity are quite high (approximately one whether commonalities exist that transcend in 12), whereas the initial transition from uni- lineage-specific solutions to achieve multicellu- cellular to simple multicellular seems far more lar organization. difficult (one in thousands). Achieving the benefits of multicellularity re- UNIQUE ASPECTS OF MULTICELLULARITY quired evolutionary innovations. At minimum, IN PLANTS AND GREEN ALGAE multicellularity requires adhesive interactions between cells to maintain a coherent, physically Plants and animals are interesting focal groups connected form. Many multicellular organisms because they arose from unicellular ancestors maintain not only adhesive connections be- that appear to have had very different propen- tween cells, but also physical bridges that allow sities or success rates in experimenting with the transfer of cytoplasmic materials directly multicellular organization. The closest unicellu- between adjacent cells and mediate cell–cell lar ancestors to animals, the choanoflagellates, communication. Diffusible extracellular mole- show a limited degree of colonial or multicellu- cules such as hormones are another means of lar organization outside of their one big hit in signaling between cells that is common in mul- the metazoan lineage (Dayel et al. 2011; Alegado ticellular organisms. In addition to adhesion and King 2014). The streptophytes (charophyte and cell–cell communication, the overall size algae þ embryophytes [land plants]) and their and shape of multicellular organisms typically sister group, the chlorophytes (green algae), follows a defined architecture or patterning that have repeatedly generated multicellular taxa as involves spatially coordinated growth and divi- well as macroscopic unicellular forms that show sion among groups of cells. A final requirement many of the traits that are typically considered for differentiated multicellular organization is hallmarks of multicellularity (Fig. 1) (De Clerck regulation of reproductive potential. Reproduc- et al. 2012; Leliaert et al. 2012). This diversity in tion in multicellular organisms is often con- the green lineage represents a potential treasure fined to a subset of cells (germ cells or stem trove of information on the evolution of multi- cells). This division of labor serves at least two cellular development. A second reason to focus purposes: First, by partitioning or restricting on plants and algae involves the fundamental reproductive capacity to a subset of cells, genetic constraint that a cell wall places on the ability conflicts associated with a transition of fitness of cells to move and reorganize spatially. This from individual cells to cooperating groups of constraint, which is not present in metazoans, cells can be mitigated (Michod and Roze 2001). has shaped the means by which multicellular Second, in multicellular organisms with inde- organization arose in the green lineage. terminate body plans such as land plants, vege- tative stem cells play a critical role in integrating Cellular Diversity in the Green Lineage internal and external signals to regulate and es- tablish overall organismal architecture (Smolar- Among unicellular green algae are found spec- kiewicz and Dhonukshe 2013). tacular amounts of cellular diversification An outstanding question in the evolution of (Lewis and McCourt 2004; Leliaert et al. 2012). multicellularity is its early origins. It is increas- The ancestral species in the green lineage were ingly clear that the path to multicellular evolu- likely to be small unicellular marine biflagellates tion is dependent on the genetic and cellular that originated around 1 billion years ago (De

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Multicellularity in Green Algae and Plants

Cellular/multicellular Chlorophytes Differentiated organization cell types? Ulvophyceae Unicellular Cladophorales Y Small cluster Dasycladales NA Bryopsidales NA Sheet/blade Trentepohliales Y N Sarcinoid Ignatius clade Ulvales/Ulotrichales Y Unbranched filament Oltmannsiellopsidales N Branched filament Chlorophyceae Y Large spheroidal Oedogoniales Large multinucleate Chaetophorales Y (siphonocladous) Chaetopeltidales N Multicellular/multinucleate Sphaeropleales Y (siphonocladous) Chlamydomonadales Giant uninucleate Volvocales Y Complex two dimensional Trebouxiouphyceae Oocystaceae N Branched three Chlorellales N dimensional Microthamniales N Trebouxiales N Prasiola N Botryococcus clade N Prasinophytes Pedinophyceae Green Chlrodendrophyceae lineage Picocystis clade Mamiellales Dolichomastigales Pyramimonadales Monomastigales Pycnococcaceae Clade VIII Clade IX Prasinococcales Neophoselmidophyceae Palmophylalles N

Streptophytes Charophyte algae Mestostigmatophyceae

Chlorokybophyceae N Kelbsormidiophyceae N

Charophyceae Y

Zygnematophyceae N

Coleochaetophyceae Y

Embryophytes Y (land plants)

Glaucophytes

Red algae

Figure 1. Multicellularity and morphological complexity in the green lineage. Simplified cladogram based on data in Leliaert et al. (2012) and De Clerck et al. (2012) showing relationships among the green lineage (chlorophytes and streptophytes) and their sister groups, red algae and glaucophytes, which together comprise the Archaeplastida. The major classes in the green lineage are in bold and, in some cases, further expanded into subgroups. Note that the prasinophytes are a paraphyletic grouping of the most primitive chlorophyte algae. The streptophytes are divided into the charophyte algae (a paraphyletic grade) and the embryophytes (land plants). Tothe right are depicted the most complex type of cellular/multicellular organization in each clade and whether cell type differentiation occurs in multicellular forms. NA, not applicable for giant unicellular forms.

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J.G. Umen

Clercket al. 2012), and this form is still prevalent the latter involves formation of new cross-walls among modern aquatic algae. A well-studied and plasma membrane at the overlap region example of a unicellular biflagellate is Chlamy- between parallel microtubules emanating from domonas reinhardtii whose highly stereotyped each daughter nucleus after mitosis. cell architecture is described later in this review. Chlorophyte and charophyte algae general- Figure 1 shows a simplified phylogenetic tree ly have haploid dominant life cycles with 1n ga- depicting the major lineages of green algae and metophyte cells that can reproduce vegetative- their land plant relatives discussed in this review. ly (i.e., asexually). In gametophyte or haploid Reductions in cell size and cellular complex- dominant life cycles, growth and prolifera- ity have occurred multiple times among green tion are generally restricted to the haploid (1n) lineage resulting in small coccoid species such phase, whereasthe diploid (2n)phase is azygotic as Ostreococcus that have lost flagella and prob- spore. Nonetheless, the Ulvophytes (a predom- ably underwent genomic reduction and stream- inantly multicellularorderof chlorophyte algae) lining (Derelle et al. 2006). On the other hand, contain genera with a significant diploid sporo- some of the largest and most complex single phytic stage. This derived state of sporophytic cells on earth are found among green algae, growth and development also evolved indepen- including species such as Acetabularia whose dently in the embryophytes (land plants) in wine-cup-shaped cells are measured in centime- which the gametophyte stagewas concomitantly ters (Mine et al. 2008). Additional cellular diver- reduced and the sporophyte dominant life cycle sity in microalgae includes different cell shapes predominates (Niklas and Kutschera 2009). such as crescents, rectangles, ovoids, elongated Many species also have a sexual cycle in spines, and flattened discs. Some species have no which at least one of the gametes is a unicellu- cell wall, whereas walled species use a variety of lar biflagellate. Anisogamy and oogamy (sperm wall polymers including cellulose, pectins, chi- and egg-mating systems) evolved more than tin-like molecules, or hydroxyproline-rich gly- once in different chlorophyte subgroups from coproteins. Besides sugar-polymer-based walls, isogamous mating systems seen in most unicel- some species cover themselves with hard calci- luar species. Although aflagellate gametes are fied scales (Popper et al. 2011; Domozych et al. found in some charophyte algae such as Zyg- 2012; Leliaert et al. 2012). nematales that mate via a specialized process Cell division in green organisms can occur called conjugation (Graham et al. 2009; Seki- through binary fission, but a form of division moto et al. 2012), the ancestral state for sexual called multiple fission (or palintomy) is also reproduction in early land plants was presum- common in chlorophyte algae (Pickett-Heaps ably isogamy with oogamous mating evolving 1975; Sˇetlı´k and Zachleder 1984; Graham et al. in advanced orders (McCourt et al. 2004). The 2009). In multiple fission cell cycles, mother subsequent evolution of aflagellate, desiccation- cells divide more than once in rapid succession resistant pollen in advanced land plants freed to produce 2n daughters (2,4,8,16, ...) within a their male gametes from the requirement for single mother cell wall. Multiple fission has been moisture and allowed them to disperse through exploited by green algae as a means of forming the air or via animal pollinators. multicellular colonies, most notably in the vol- vocine algae that are discussed below. Different Macroscopic Complexity in Green Algae mechanisms of cytokinesis have also evolved in Evolved Using Different Strategies the green lineage including a specialized micro- tubule structure called the phycoplast, as well Green algae challenge the notion that equates as an analogous structure, the phragmoplast, multicellularity with organismal complexity. which is used in streptophytes (Pickett-Heaps Described below are three strategies used in 1976). The former mechanism involves mem- the green lineage to achieve macroscopic com- brane furrowing guided by microtubules that plexity, two of which do not involve conven- are parallel to the plane of division, whereas tional multicellularity.

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Multicellularity in Green Algae and Plants

Multicellular Algae over, some green algae are both multicellular and coenocytic (termed siphonocladous) be- Independent transitions to multicellularity or cause they are composed of multiple cells, each macroscopic forms occurred multiple times in of which contains multiple nuclei (e.g., Clado- the chlorophyte lineage (Fig. 1). True multicel- phora). Cytoplasmic continuity and develop- lular forms are characterized by having separate mental patterning in coenocytic macroscopic cells, each with its own nucleus, plasma mem- algae are beyond the scope of this review, but brane, and cell wall. Streptophytes and many are covered in other recent reviews (Balusˇka multicellular chlorophyte algae are organized et al. 2004; Cocquyt et al. 2010; Niklas et al. in this manner. It should be noted that connec- 2013). tions between neighboring cells (e.g., plasmo- desmata) evolved multiple times in the green lineage and provide direct cytoplasmic continu- CHAROPHYTE GREEN ALGAE AND ity between cells in many multicellular algae THE ORIGINS OF LAND PLANT and land plants, thus allowing them some de- MULTICELLULARITY gree of supracellular organization (Raven 1997). Some common multicellular forms are un- Overview connected groups of cells embedded in extra- Charophyte algae have long been recognized as cellular matrix, short chains, unbranched and the closest algal relatives of land plants based branched filaments with and without differen- on cellular and morphological features (Stewart tiated cell types, geometric networks, large leaf- and Mattox 1975). This view has been corrob- like blades, discoidal colonies, and spheroidal orated and refined using molecular phyloge- colonies (Fig. 1). netics that have begun to clarify relationships within charophyte algae and with their sister Giant Uninucleate Algae clade, the land plants (embryophytes) (Turmel An alternative form of complex and macroscop- et al. 2002; Finet et al. 2010; Wodniok et al. ic unicellular organization is found in giant uni- 2011; Laurin-Lemay et al. 2012; Timme et al. cellular algae that possess a single nucleus. The 2012; Zhong et al. 2013). most well-known species of this type are in the A number of land plant multicellular traits genus Acetabularia (an ulvophyte) that is fa- originated within the streptophytes (charo- mous for transplantation experiments demon- phyte algae þ embryophytes). These include strating nuclear control over cell morphology apical meristems, cells that undergo asymmetric (Mandoli 1998; Mine et al. 2008). division and differentiation, complex branch- ing patterns, matrotrophic support for a multi- cellular sporophyte, and plasmodesmata that Coenocytic Algae form symplastic connections between cells. Ad- Coenocytic algae (also referred to as siphonous ditional cellular and biochemical traits that are algae) are large single cells that contain multi- streptophyte specific include a hexameric cellu- ple nuclei housed within a common cytoplasm. lose synthase complex that synthesizes the pri- The sizes of these forms are measured in centi- mary cell wall, the phragmoplast as a mecha- meters and meters making them some of the nism for cytokinesis, synthesis, and transport largest single cells on earth. Despite their lack of phytohormones, and several metabolic spe- of multicellular organization, coenocytic algae cializations (Graham 1996; Graham et al. 2000; can form remarkably complex structures with Waters 2003; Becker and Marin 2009). multiple types of specialized subdomains. For Later changes and innovations that oc- example, the multinucleate cells of the marine curred within the embryophytes well after they alga Caulerpa reach meters in size and contain achieved multicellularity include three-dimen- three distinct tissue types that function similarly sional growth and cell division to produce com- to roots, stems, and leaves (Jacobs 1970). More- plex tissues and organs, cuticular waxes, and

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J.G. Umen

stomatal poresto control evaporative losses, vas- land plants is unresolved, but it is clear that cular transport systems, root and shoot apical the most developmentally complex order, Char- meristems, transition to a sporophyte dominant ophyceae (stoneworts), is probably not the clos- life cycle, specialized and complex hormonal est relative of the embryophyte lineage (Wod- signaling, nonflagellated and desiccation-re- niok et al. 2011; Laurin-Lemay et al. 2012; sistant male gametes (i.e., pollen), flowers, and Timme et al. 2012; Zhong et al. 2013). Despite lignified secondary cell walls (Langdale and this ambiguity and the likelihood of both char- Harrison 2008). Interestingly, molecular evi- acter loss and gain in the extant charophyte algal dence for proteins related to some of these later orders, some of the steps leading to multicellu- innovations in embryophytes have been found larity in the embryophytes can still be inferred. in charophytes as described below. To date, there are no sequenced charophyte It has been argued that the existing charo- genomes, so molecularevidence regarding genes phyte algal orders are actually the remnants of a and pathways that are shared within strepto- terrestrial invasion that gave rise to land plants, phytes is somewhat piecemeal. Current under- but whose members were outcompeted by the standing of molecular evolution of charophytes embryophytes. The remaining extant orders of algae has been guided mostly by expressed se- charophyte algae ended up secondarily aquatic quence tag (EST) sequences and directed inves- where they were able to compete more effec- tigations of specific gene families (Simon et al. tively than on land (Stebbins and Hill 1980). 2006; Timme and Delwiche 2010; Vannerum Although this idea is difficult to test directly, et al. 2011; Wodniok et al. 2011). the finding that a nominally aquatic charophyte species, Coleochaete orbicularis, can grow in ter- Key Innovations in the Streptophyte restrial environments and even show adaptive Transition to Multicellularity changes in body plan under these conditions supports this idea (Graham et al. 2012). It has Given the uncertainties surrounding the phy- also been argued that early streptophytes were logeny of charophyte algae and the apparent preadapted to the colonization of land by be- gain and loss of some traits, the order of topics ing the first algal group to conquer freshwater listed below is meant only to convey a plausible habitats, whereas chlorophyte algae, which pre- picture of how multicellular innovations were dominate in marine environments, moved into acquired in the embyrophyte lineage as summa- freshwater much later (Becker and Marin 2009). rized in Figure 2. A closer examination of charophyte evolu- tion may provide an outline for understand- The Closest Unicellular Relative of Land Plants ing some of the early multicellular innovations in the embryophytes. It is important to note The unicellular ancestor of Streptophytes was that the extant charophyte lineages are highly a freshwater biflagellate whose most similar ex- diverged from each other and have probably tant relative is in the genus Mesostigma (Bhat- undergone secondary character losses that com- tacharya et al. 1998; Marin and Melkonian 1999; plicate comparisons and inferences about the Lemieux et al. 2000, 2007; Rodriguez-Ezpeleta progression to multicellularity in the embryo- et al. 2006). Mesotigma does not produce cellu- phytes (McCourt et al. 2004; Timme et al. 2012; lose or any type of cell wall, but instead has cal- Bowman 2013). Moreover, the fossil record of cified scales. It divides by furrowing rather than charophyte algae is incomplete and does not through formation of a phragmoplast (Manton extend earlier than that of land plants, so is and Ettl 1965). This ancestral form likely had not a reliable source of information on timing an open mitosis as observed in early diverging for emergence of early embryophytes whose charophytes (Stewart and Mattox 1975; Pickett- earliest fossils appear 500 million years ago Heaps 1976). A systematic investigation of its (Leliaert et al. 2012). As noted above, the char- genetic toolkit has not been performed, but sev- ophyte algal order that is most closely related to eral studies have identified streptophyte-spe-

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Multicellularity in Green Algae and Plants

Mestostigmatophyceae

Chlorokybophyceae Cellulose wall

Klebsormidiophyceae Filamentous growth

Charophyceae Complex cell wall, phragmoplast, plasmodesmata, polarized growth, asymmetric division, stem cells, oogamy, Zygnematophyceae matrotrophy, phytohormones, three-dimensional patterning, Coleochaetophyceae apical growth

Embryophytes Multicellular embryo, sporophyte dominant life cycle, (land plants) stomata, waxy cuticle, vasculature, multicellular organs, meristems with >2 cutting faces, seeds, flowers

Figure 2. Multicellular innovations in charophyte algae and embryophytes. Simplified cladogram based on data in Leliaert et al. (2012) showing relationships among major orders of charophyte algae and embryophytes. Tothe right are shown multicellular innovations associated with different groups. Note that reductions or losses of traits occurred in some orders of advanced charophyte algae (Charophyceae, Zygnematophyceae, Colechaeto- phyceae), most notably in the Zygnematophyceae (McCourt et al. 2004), so the set of innovations in this group may not apply to all three orders.

cific gene families in Mesostigma (Nedelcu et al. ple selective advantages. Filaments can be used 2006; Petersen et al. 2006; Simon et al. 2006; to anchor colonies in place efficiently while al- Grauvogel and Petersen 2007). A genome se- lowing maximal contact with the surrounding quence and development of molecular genetic environment along each cell’s surface,a property tools would allow deeper investigation into the that is likely to be useful for nutrient exchange in cell biology of these unicellular plant relatives both aquatic and terrestrial habitats (Niklas and how much of the developmental toolkit for 2000). Filaments would also serve as protection Embyrophytes was present in their most recent- against grazing predators by being too large to ly diverged unicellular ancestor. ingest, an idea that has been tested experimen- tally with filamentous bacteria (Gu¨de 1979; Shi- kano et al. 1990). A third advantage of filaments Filamentous Growth and Cytokinesis is their utility for nutrient foraging because they The early multicellular forms produced by direct growth along a vector that maximizes ex- primitive embyrophytes were probably undif- ploration of surrounding space. Even without ferentiated filaments, a growth habit that is still resource sharing between cells (i.e., symplastic common in many green algal lineages including connections), the clonal nature of filaments en- extant charophyte algae such as Klebsormi- sures a benefit to growth-directed foraging be- diales, which are among the three most primi- cause all cells in the filament share the same tive orders of this grade. In all orders except genotype. Mesostigmaphyceae, charophyte algae lost mo- Filament formation requires at least one tility in the vegetative stage, but with the ex- axis of cell polarity to ensure that growth oc- ception of Zygnematales, retained flagellated curs longitudinally and the plane of cytokine- zoospores (Stewart and Mattox 1975). The pre- sis is perpendicular to the plane of growth. An valence of filamentous forms in both aquat- innovation required for filamentation in char- ic and terrestrial environments and diverse algal ophytes involved the deposition of common cell lineages suggests that filamentation has multi- wall material between daughters. Descriptive

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J.G. Umen

and comparative studies have been performed a filament or thallus (body) grow, and the di- on cytokinesis in primitive filamentous charo- rectionality of growth. Species from both the phytes that occurs after an open mitosis, but Coleochaetophyceae and Charophyceae have does not appear to involve a phragmoplast or spatially regulated division planes. Coleochae- phycoplast (Floyd et al. 1972; Pickett-Heaps tales show diverse vegetative forms that include 1976; Lokhorst and Star 1985; Katsaros et al. flat, disk-shaped thalli, branched filaments, and 2011). The phragmoplast is still considered an pseudoparenchymatous filaments that are held important innovation and originated in the together within an extracellular matrix (Gra- Zygnematales, a transitional group wherein dif- ham et al. 2009). The discoid species Coleo- ferent types of cytokinetic patterns coexist. chaete orbicicularis grows outward by a com- Some groups in this order divide centripetally bination of cell expansion and either anti- or (e.g., filamentous desmids) (Hall et al. 2008) periclinal cell divisions along its marginal cells whereas others, such as the genus Spirogyra, ap- (Cook 2004). Cell division planes are set accord- pear to use a reduced but recognizable phrag- ing to a set of simple rules based on position moplast (Fowke and Pickett-Heaps 1969; Gal- within the thallus, cell size, and cell shape (Du- way and Hardham 1991), although with some puy et al. 2010). Moreover, the division plane functional distinction from embryophyte orientation behavior of C. orbicularis can be phragmoplasts (Sawitzky and Grolig 1995). It modeled as an energy minimization function is not known whether the shared wall between that can also be applied to embryophytes where primitive filamentous charophyte algal cells it may be an inherited mechanism that specifies are specialized in any way, but it is known that a default pattern of symmetrical cell division their walls lack many of the complex carbohy- (Besson and Dumais 2011). drate polymers present in advanced charophytes Asymmetric and/or branched histogenet- and embryophytes (Sørensen et al. 2010, 2011; ic cell divisions are critical for development in Domozych et al. 2012). The more advanced the Coleochatelaes and Charales (Graham 1996; charophyte algae (Charophyceae, Coleochaeto- Graham et al. 2000), although little is known phyceae) do have a recognizable phragmoplast how such divisions are controlled. In angio- that resembles those of embryophytes (Pickett- sperms, asymmetric divisions are also crucial Heaps 1967; Marchant and Pickett Heaps 1973). for development and regulated by different ge- Coincident with the evolution of the phragmo- netic pathways depending on tissue type (De plast in advanced charophyte algae is the ap- Smet and Beeckman 2011). Although a ho- pearance of what might be a preprophase band molog of a gene required for asymmetric divi- of microtubules that marks the future plane of sion in Arabidopsis zygotes, GNOM, has been cell division (Galway and Hardham 1991). De- identified in Coleochaetes, the significance of tailed molecular information on primitive char- this finding is unknown (Timme and Delwiche ophyte cell division is still limited, but these ear- 2010). The relationships between charophyte ly filamentous divisions in Spirogyra described algal asymmetric cell divisions and those in em- above may have paved the way for evolution of bryophytes remain to be investigated. the phragmoplast and preprophase band as an Although more distantly related to land efficient mechanism for marking division sites plants than Coleochaetphyceae and Zygnema- and subdividing cells with a rigid wall. tophyceae, Charaophyceae (e.g., Chara and Ni- tella) (Fig. 2) show morphologies and growth patterns that more closely resemble those of Regulated Division Plane, Cellular land plants. These similarities include a long, Differentiation, and Polarized Growth branched body axis and indeterminate api- Contrasting with simple filamentous forms in cal meristem cell. Charophyceans do not have which cell growth occurs similarly in all constit- multicellular tissues, but their giant multinucle- uent cells, polarized growth involves some form ated cells show differentiation into specialized of tissue organization that dictates which cells in types including long intermodal cells, nodal

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Multicellularity in Green Algae and Plants

cells that undergo asymmetric cell divisions to that remodeling of plasmodesmata is important form branches, and rhizoid cells that act as for maintaining and coordinating cell division holdfasts and show tip-polarized growth synchrony and developmental fate (Kwiatkow- (Cook et al. 1998; Braun and Limbach 2006). ska 2003). In both embryophytes and charo- Charophyceae also have male (antheridia) and phyte algae, plasmodesmata can be formed dur- female (oogonia) sexual reproductive structures ing cytokinesis or secondarily in interphase cells (see below) that are formed by complex division by remodeling of walls and fusion of adjacent patterns to generate simple three-dimension- plasma membranes (Hepler 1982; Franceschi al multicellular tissues (Fritsch 1948; Pickett- et al. 1994), but the molecular details of plas- Heaps 1968; Kwiatkowska 2003; Graham et al. modesmata formation in charophyte algae and 2009). their degree of similarity to embryophyte plas- Polarized gravitropic growth of the apical modesmata have not been established (Faulkner meristem and rhizoid cells in Chara and Nitella et al. 2005; Timme and Delwiche 2010). has been investigated, particularly with respect to actin cytoskeletal dynamics (Braun and Lim- Hormonal Signaling bach 2006). However, little is known about other developmental patterning cues in charo- Phytohormones are essential regulators of plant phytes such as light signaling (Rethy 1968; development and environmental responses. Be- Dring 1988). The discovery of plant hormones sides contributing to developmental plasticity, in some charophyte algal species (see below) small diffusible hormones facilitate long-dis- suggests that phytohormones may be an early tance communication that may occur on a mac- innovation that enabled the evolution of char- roscopic scale to coordinate responses across ophyte multicellularity. tissues and cell types in a multicellular organ- ism. The presence of growth-promoting phy- tohormones in algae has been investigated in Symplastic Connections and Intercellular diverse taxa (Bradley 1991; Johri 2004; Tara- Communication khovskaya et al. 2007; Stirk et al. 2013a,b), but In land plants, plasmodesmata connect adja- the molecular bases of phytohormone action in cent cells allowing metabolites and some mac- algae is not well understood. Physiological stud- romolecules to pass between them, as well as ies on the effects of plant hormones have shown allow tissue-level interactions among cells (Lu- that charophyte algae produce and respond to cas and Lee 2004). Plasmodesmata are found several phytohormones, indicating an early or- in two of the advanced orders of charophyte igin of these chemical signals. Because genome algae, Coleochaetophyceae and Charophyceae, sequences are not available, inferences about but intercellular connections in algae are wide- the presence of known signaling and biosyn- spread and not unique to charophytes (Stewart thetic machinery for Embyrophyte phytohor- and Mattox 1975; Raven 1997). In primitive mones in charophyte algae can only be made embryophytes, connections between adjacent from the presence of gene families, but not cells would enable communication, allow me- from their absence. tabolite/resource sharing, and promote cell Indole derivatives (e.g., indole acetic acid) specialization. The multifaceted roles of plas- in the auxin family are produced in Chara modesmata in shaping plant development and (Sztein et al. 2000) and are known to affect de- evolution has been reviewed recently (Lucas and velopment byaltering shoot elongation, branch- Lee 2004; Herna´ndez-Herna´ndez et al. 2012). ing, and rhizoid elongation, for example (Ima- Information on how intercellular communica- hori and Iwasa 1965; Kla¨mbt et al. 1992; Cooke tion modulates development in charophyte al- et al. 2002), and may act through changes in gae is limited, but has been studied in some cytoskeletal organization (Jin et al. 2008). Di- depth in male reproductive tissue (antheridia) rectional transport of auxin in long, giant inter- in Chara, in which there is compelling evidence modal cells of Chara has been shown recently,

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J.G. Umen

suggesting that this phenomenon may be an- of angiosperms and developmental control of cient (Boot et al. 2012; Raven 2013). Some of branching architecture (de Saint Germain et the auxin biosynthetic enzymes entered the al. 2013). In the Bryophyte Physcomitrella, SLs green lineage before the streptophyte–chloro- influence branching and sensing of adjacent phyte divergence, but the response and trans- colonies (Proust et al. 2011). Remarkably, SLs port proteins characteristic of the well-studied have been identified in the Charophyceae (but auxin-signaling networks in angiosperms first not other charophyte algae orders) and assays of appeared in charophytes, and the full comple- SL-treated Chara revealed a developmental re- ment of core auxin-signaling proteins became sponse of rhizoid cell elongation (Ruyter-Spira established in early embryophytes (Lau et al. and Bouwmeester 2012). 2009; Prigge et al. 2010; De Smet et al. 2011; Much less is known about other land plant Wodniok et al. 2011). hormones in charophyte algae including brassi- Abscisic acid (ABA) is an isoprenoid- nosteroids, cytokinins, and ethylene. Brassino- derived stress and drought hormone whose steroids and cytokinins have been detected in function can be traced back to the earliest em- charophyte algae, and at least one study has bryophyte clade, the bryophytes (Cutler and reported an effect of cytokinins on growth of Rodriguez 2010; Khandelwal et al. 2010; Hauser Chara (Imahori and Iwasa 1965). Ethylene is et al. 2011). Although its function in land plants reported to bind to Chara (Wang et al. 2006), is associated with the transition to terrestrial life, whereas some ethylene biosynthesis and per- ABA is also produced by a wide variety of aquat- ception genes were found in charophyte algae ic green algae, although its function in these ESTs (Timme and Delwiche 2010; Wodniok algae is unknown (Hartung 2010). G protein– et al. 2011), but data on the effect of ethylene coupled receptor G proteins in plants have been in charophyte algae growth or physiology is cur- linked to ABA signaling in Arabidoposis and have rently unavailable. recently been identified in Chara, but not in any chlorophyte algae (Pandey and Assmann 2004; Oogamous Sexual Reproduction Hackenberg et al. 2013). Studies on spore ger- mination in Chara suggest a possible inhibitory In complex multicellular organisms, sexual re- role for ABA in this process that is antagonized production is typically oogamous with small by another hormone, gibberrellic acid (GA), motile sperm and large immotile eggs, whereas which also promotes growth (Imahori and Iwasa unicellular or simple multicellular organisms 1965; Sabbatini et al. 1987; Sederias and Colman are typically isogamous (having equal-sized 2007). The apparently antagonistic roles of GA gametes). Various explanations for the evolu- and ABA in Chara are reminiscent of similar tion of anisogamy and oogamy have been put roles in Angiosperm seed germination, suggest- forth (Randerson and Hurst 2001), but one of ing an ancient role for this hormonal system in the earliest by Parker may be particularly rele- regulating dormancy that may have preceded vant to the evolution of multicellularity (Parker a role for ABA in drought responses. GA has et al. 1972). The crux of this argument is the also been reported to affect growth and develop- fitness advantage of making a large zygotic cell ment of male reproductive cells (antheridia) in that is capable of forming a functioning multi- Chara by up-regulating sperm production and cellular progeny. Disruptive selection drives one endoreplication of support cells (Kwiatkowska gamete type to be much larger than a single cell et al. 1998). Classical GA-signaling and percep- so that it can provide resources to the zygote, tion proteins have not been found in charophyte and the other to be as small and numerous as algae (Vandenbussche et al. 2007), although ge- possible to ensure efficient fertilization. nomic information is unavailable so this nega- Sexual reproduction in charophyte algae has tive result awaits confirmation. been described in the higher orders Charophy- Strigolactones (SLs) are cyclic derivatives of ceae, Zygnematophyceae, and Coleochaetophy- carotenoids that have roles in biotic interactions ceae, but has not been observed in the lower

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Multicellularity in Green Algae and Plants

orders in which it is assumed to be isogamous and nutrient transport (Graham and Wilcox (McCourt et al. 2004). It is also assumed that 1983; Delwiche et al. 1989). The molecular de- charophyte algae have a haploid dominant life tails of these junctions and how they form is cycle similar to most chlorophyte algae and not known, but their presence in advanced primitive embryophytes, although this assump- charophyte algae and similarity to embryophyte tion has been questioned (Haig 2010). Zygne- maternal-zygotic junctions suggests a common matales have the best-studied sexual cycles in origin. the charophyte algae, but have secondarily lost flagella and reproduce through isogamous con- Multicellular Innovations in Land Plants jugation (Graham et al. 2009; Sekimoto et al. that May Be Rooted in the Green Lineage 2012). Both Charophyceae and Coleochaeto- phyceae have oogamous sexual cycles with spe- The above innovations in the charophyte algae cialized egg and sperm cells. Very little is known can be directly tied to the transition to multi- about the genetics of sex determination in these cellularity in the streptophyte lineage. Other two orders in which sexual development is important properties of embryophytes that are usually monoecious (male and female gametes not directly related to acquisition of multicellu- formed in the same organism). As mentioned larity may also have roots in charophyte algae above, the Charophyceae have particularly strik- and the green lineage. Cellulosic walls are found ing and elaborate reproductive tissues (male an- throughout the green algal lineage and in other theridia and female oogonia) that include both taxa, but a hexameric cellulose synthase com- gametic cells and support cells (Fritsch 1948; plex evolved uniquely in streptophytes (Tsekos Pickett-Heaps 1968; Sawa and Frame 1974; 1999). Other distinctive characteristics of em- Beilby and Casanova 2014). Understanding the bryophyte cell walls, including complex carbo- genetic programs that give rise to reproductive hydrate polymer linkages, first appeared in ad- tissues in charophyte algae and how they relate vanced charophyte green algae (Van Sandt et al. to those of embryophytes may shed light on 2007; Popper et al. 2011; Sørensen et al. 2011; whether oogamy is a synapomorphic trait with- Domozych et al. 2012; Proseus and Boyer 2012). in streptophytes. The recent discovery of expansin genes in the Zygnematophycean alga Micrasterias suggests that these critical cell wall remodeling proteins Matrotrophic Support of the Zygote from embryophytes originated in charophyte A conserved feature in embryophytes is mater- algae (Cosgrove 2000; Vannerum et al. 2011). nal support provided to zygotes and sporophyte Lignified secondary walls were a critical inno- embryos after fertilization (Ligrone et al. 1993). vation in land plants for desiccation tolerance, This innovation may be related to oogamy be- load-bearing structural integrity, and decay re- cause it increases resource allocation to a devel- sistance (Boyce et al. 2004). Although charo- oping multicellular offspring. The attachment phyte algae do not have secondary walls, lignin and nourishment of the developing embryo by or lignin-like molecules have been identified maternal tissue may have been crucial for estab- in this group and may contribute to resistance lishing a later change in embrophyte evolution, against microbial attack (Gunnison and Alex- the sporophyte dominant life cycle (Graham ander 1975; Delwiche et al. 1989; Sørensen et and Wilcox 2000). The best-documented oc- al. 2011). Sporopollenin is a complex molecule currence of matrotrophy in charophyte algae found in the walls of angiosperm pollen that comes from studies of Coleochate in which the protects cells from physical and chemical deg- developing zygote remains associated with the radation (Ariizumi and Toriyama 2011; Wallace vegetative thallus (Graham 1984). These studies et al. 2011). However, the origins of sporo- identified regions of the vegetative maternal pollenin-like molecules goes as far back as the cells specifically at the zygote interface that ap- charophyte algae in which sporopollenin-like peared specialized for maximal cell–cell contact substances were identified in the zygotes of Co-

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J.G. Umen

leochate (Delwiche et al. 1989). Both lignin- and ophyte developmental patterning (Smaczniak sporopollenin-like substances are found outside et al. 2012). MIKC-type MADS box genes are of the streptophyte lineage, so without molecu- also present in advanced charophyte orders in lar data about the origins of biosynthetic genes which their expression was analyzed (Tanabe for these compounds in charophyte algae, the et al. 2005). In Chara, MADS-box gene expres- possibility of convergence or horizontal transfer sion was restricted to reproductive tissues (an- into embryophytes cannot be ruled out (Brooks theridia and oogonia), whereas expression was and Shaw 1978; Emiliani et al. 2009; Martone detected at multiple stages in a Zygnematophy- et al. 2009). cean, Closterium. In bryophytes, MIKC MADS Although not directly associated with the box genes are incompletely characterized, but transition to multicellularity in land plants, appear to have roles in both gametophyte and the alteration of generations is a hallmark of sporophyte development (Quodt et al. 2007; the embryophytes in which simple, multicel- Singer et al. 2007; Zobell et al. 2010). lular sporophytes first appeared (Graham and Homeodomain leucine zipper (HD-ZIP) Wilcox 2000). Interestingly, the genetic program transcription factors regulate diverse aspects of that directs sporophyte development in the angiosperm sporophyte development including bryophyte moss Physcomitrella is directed by shoot apical meristem identity, abaxial-adaxial a KNOX family homeodomain transcription leaf patterning, and epidermal development factor whose homologs in the chlorophyte (Elhiti and Stasolla 2009). The origin of two alga C. reinhardtii direct development of the major groups of HD-ZIP proteins (class III dormant diploid zygospore formed after fertil- and class IV) has been traced back to charophyte ization (Lee et al. 2008; Nishimura et al. 2012; algae (Floyd et al. 2006; Zalewski et al. 2013). Sakakibara et al. 2013). The role of these home- Although HD-ZIP proteins are also found in odomain proteins in charophyte algae has not bryophytes, their function in lower plants is been examined, but they are predicted to par- not well characterized (Sakakibara et al. 2001; ticipate in zygote development. Prigge and Clark 2006). Interestingly, a micro- RNA binding site that regulates expression of class III HD-ZIP expression in angiosperms is How Much of the Embryophyte Molecular conserved in lower plants, but not in Chara, Genetic Toolkit Originated in Charophyte suggesting that gene family expansion and reg- Algae? ulatory evolution contributed to functional Although data are incomplete, some progress novelty in embryophyte HD-ZIPs (Floyd et al. has been made in identifying charophyte algal 2006; Floyd and Bowman 2007). Wuschel-like homologs of key developmental regulators used homeodomain proteins that are important for by embryophytes (Bowman et al. 2007; Pires Angiosperm shoot apical meristem identity are and Dolan 2012; Bowman 2013). Without com- also present in charophyte algae, but their role plete genome sequences this list is relatively in this group and bryophytes has not been ex- short and incomplete, but provides a sample plored (Timme and Delwiche 2010). of potential discoveries that might be made with increased knowledge of charophyte algal VOLVOCINE ALGAE: A LIVING SNAPSHOT genomes and developmental patterning mech- OF MULTICELLUAR EVOLUTION anisms. MADS-box transcription factors are found Overview of Volvocine Algae within and outside the green lineage, but a spe- Volvocine algae provide an interesting contrast cific MADS protein subtype, MIKC, defined by to embryophytes whose body plans are con- the presence of four characteristic domains, structed through polarized growth and cell di- is found only in streptophytes and underwent vision of indeterminate meristems. Instead, a dramatic expansion in the embryophytes in multicellular volvocine algae undergo a single which members control many aspects of spor- series of embryonic cell divisions and morpho-

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Multicellularity in Green Algae and Plants

genesis to produce a determinate body plan. The simplest colonial species are in the ge- How and why did volvocine algae evolve this nus Gonium that form planar colonies of be- form of multicellularity? The answer to this tween four and 16 cells that show a slight cur- question can, potentially, be found by examin- vature and have their flagella positioned on the ing the cell biology of unicellular volvocine al- convex side of the colony. The next step in the gae such as C. reinhardtii, which closely approx- volvocine lineage was the formation of spheroi- imate the ancestral state of this lineage. dal colonies of 16 to 32 cells with a defined Volvocine algae are particularly well suited interior and exterior as typified in the genus for investigating the origins of multicellularity. Pandorina. In the genus Eudorina, larger spher- They are monophyletic and contain genera that oidal colonies of 32 to 64 cells are formed by the are unicellular and multicellular. Two of the key addition of an extensive secreted extracellular volvocine species, unicellular C. reinhardtii and matrix (ECM) in which cells of the colony are multicellular Volvox carteri, are model organ- embedded. The addition of ECM in Eudorina isms with sequenced genomes and established allows the colonies to increase in volume with- molecular-genetic toolkits that make them out any significant change in cell number or amenable to molecular and genetic experimen- size. Up to the genus Eudorina, all the cells in tation (Merchant et al. 2007; Prochnik et al. a colony are reproductive; they grow as flagellat- 2010; Umen and Olson 2012). V.carteri mutants ed cells to provide motility and then synchro- with developmental phenotypes have been es- nously divide to produce a set of new daughter pecially illuminating for understanding the mo- colonies. Starting with the genus Pleodrina, col- lecular genetic origins of multicellularity (Kirk onies begin to show germ-soma differentiation. 1998, 2003). In most species of Pleodorina, there is a clearly The genus Chlamydomonas has more than visible anteroposterior axis with anterior cells 600 species whose properties are typical of uni- ceasing growth and remaining permanently cellular chlorophytes. Although the genus is flagellated to serve a nonreproductive motility now recognized as polyphyletic, the model function. The posterior cells in a Pleodorina col- species C. reinhardtii is closely related to multi- ony show a partial division of labor. They start cellular volvocine algae that together form a out as flagellated cells, but continue to grow monophyletic clade with C. reinhardtii as an and, subsequently, retract their flagella and di- outgroup (Fig. 3A) (Pro¨schold et al. 2001, vide into new colonies. The partial germ-soma 2005; Herron and Michod 2008; Nakada et al. division of labor shown by Pleodorina becomes 2008). The last common ancestor of this clade a fixed dichotomy in the genus Volvox whose was estimated to have lived 200 million years colonies can contain up to 50,000 cells in ago (Herron et al. 2009), but it is worth noting some species and in which there are dedicated that the single fossil chlorophyte alga used for groups of sterile somatic cells and reproductive calibration in the above dating study has pro- germ cells. The progression from simpler colo- duced incongruences in other analyses and may nial forms to Volvox was probably stepwise as not be part of the taxonomic group it was orig- outlined in the volvocine lineage hypothesis, inally identified with (Berney and Pawlowski but variations of this progression led to at least 2006). Multicellular or colonial volvocine algal three independent origins of Volvox-like colony genera can be arranged in a stepwise progression organization, each with distinct properties (Fig. of increasing cell number, colony size, and de- 3) (Nozaki et al. 2006b; Herron and Michod gree of cell-type specialization (Fig. 3B). This 2008; Coleman 2012). simplistic arrangement that is termed the volvo- cine lineage hypothesis is probably a good ap- The Cell Biology of Chlamydomonas proximation of how complexity evolved within specific sublineages, but does not reflect the fact The key to understanding the proximal mecha- that some grades of organization such as Volvox nisms underlying multicellularity in Volvocine arose several times independently (Fig. 3A). algae lies in the cell biology of their unicellular

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AB

Chlamydomonas reinhardtii Gonium sociale Gonium Gonium pectorale Organismal polarity and basal body rotation Volvolina steinii Genetic modulation of cell number Incomplete cytokinesis Pandorina morum Cell–cell attachments Platydorina caudata Partial inversion Volvox globator Pandorina Volvox rousseletti Volvox barberi Full inversion Yamagishiella unicocca Eudorina elegans Eudorina Pleodorina thompsonii ECM expansion Eudorina unicocca Pleodorini starii Pleodorini indica Partial germ-soma Eudorina illinoisensis division of labor Anisogamy Eudorina cylindrica Pleodorina Eudorina elegans Volvox gigas Oogamy Volvox powersii Asymmetric division Pleodorina japonica Bifurcated embryonic cell cycle Complete germ-soma division of labor Pleodorina californica Volvox aureus Volvox obversus Volvox carteri Volvox africanus Volvox dissipatrix Volvox tertius Volvox carteri

Figure 3. Multicellular innovations in the volvocine algae. (A) Cladogram based on data in Kirk (2005) and Umen and Olson (2012) showing representative volvocine algal lineages with shading used to highlight different levels of organization in each genus. Note that the genus Volvox is polyphyletic with at least three independently derived clades. (B) Simplified cladogram based on data in Kirk (2005) showing key innovations in the steps leading from C. reinhardtii to V. carteri. Schematic cartoons of each genus are also shown.

ancestor that was similar to C. reinhardtii. C. and Dutcher 1989). Basal bodies also coordi- reinhardtii is a walled biflagellate with a pair of nate the placement of the cell division plane apical flagella and single large cup-shaped chlo- and the microtubule-based phycoplast used roplast situated basally that occupies around for cytokinesis (Johnson and Porter 1968; Ehler 2/3 of the cell volume. C. reinhardtii cells have et al. 1995; Ehler and Dutcher 1998). Besides a highly polarized and stereotyped organization apical-basal polarity, C. reinhardtii cells also centered on their two basal bodies that reside have radial polarity that is evident from an eye- just under the plasma membrane at the cell an- spot located equatorially and always positioned terior. The basal bodies nucleate the flagella and along the four-membered microtubule rootlet organize the internal microtubule cytoskeleton emanating from the younger of the two basal whose principal axes are defined by two- and bodies (Holmes and Dutcher 1989). The eye- four-membered microtubule rootlets (Holmes spot allows swimming cells to perceive the di-

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rection of illumination and signal to the flagella that overcomes this constraint and is one of the to enable phototaxis (Hegemann 2008). The most remarkable aspects of volvocine algal de- basic cellular architecture and polarity of C. velopment and evolution. reinhardtii cells is conserved in colonial species A third aspect of multiple fission that has with some modifications, and is likely to have impacted the evolution of multicellularity in played a role in establishing organismal-level Volvocine algae is the relationship between cell polarity. size and division. In C. reinhardtii, there is in- The wall surrounding C. reinhardtii cells is herent flexibility in cell division so that num- composed mostly of hydroxyproline-rich glyco- bers of daughters can range from 2 (1 division) proteins (HRGPs) that form rod-shaped poly- to 16 or even 32 (4 or 5 divisions) depending proline-II helices with globular domains at on mother cell size. A sizer mechanism oper- one or both ends (Adair et al. 1987; Lee et al. ates to ensure that the appropriate number of 2007). As described below, HRGPs are also ma- S phase and mitosis cycles is executed to pro- jor components of the extracellular matrix of duce daughters of uniform size (Donnan and Volvox and other colonial volvocine algae (Hall- John 1983; Umen 2005). In multicellular spe- mann 2003). cies, cell number per colony is much less vari- Like many green algae, Chlamydomonas able, so the flexibility seen in C. reinhardtii has cells and nearly all volvocine algae divide by a been overridden by a more stereotyped relation- mechanism called multiple fission (or palint- ship between mother cell size and the initiation omy) that is described in the Unique Aspects of cell division to maintain colony uniformity. of Multicellularity in Plants and Green Algae As noted above, during division, Chlamydo- section and whose features are intimately relat- monas cells resorb their flagella and cannot ed to multicellularity in volvocine algae. Most swim. Although this temporary lack of motility important, multiple fission produces clonal probably does not impact the fitness of Chla- clusters of 2n daughter cells within a common mydomonas, it may do so for the larger colo- mother cell wall at the end of every division nial volvocine genera such as Pleodorina and cycle. Clonality (versus aggregation) aligns the Volvox that are thought to have evolved germ- fitness of each genome in the colony and largely soma specialization as a response to their ances- obviates genetic conflicts between cells over re- tral flagellation constraint (Koufopanou 1994). productive potential (Buss 1987; Queller 2000). As colonies grow larger, embryonic cell divi- Multiple fission also explains why cell number sions take longer to complete, meaning that per colony in volvocine algae is usually a power they must endure increasing lengths of time of 2 (i.e., 4,8,16,32,64,128, ...). spent immotile and sinking in the water column A second important feature of multiple fis- during mitosis. The evolution of a permanently sion is the spiral-like pattern of successive cleav- flagellated caste of somatic cells to provide con- age divisions caused by rotation of the mitotic tinuous motility is an innovation that is likely spindle axis by 90˚ in daughters with respect to have enabled the evolution of ever-larger col- to mothers after each division cycle. As a result, onies without suffering the cost of lost motility postmitotic daughter cells end up clustered in a during cell division. configuration with their basal bodies and flagel- la oriented inward (Johnson and Porter 1968; Kirk et al. 1991). Although this inside-out con- Multicellular Innovations in the Volvocine Lineage Are Modifications of Unicellular figuration presents no obstacle for individual Volvocine Algal Cell Biology C. reinhardtii cells that soon hatch from their mother cell wall and swim their separate ways, it In his review of multicellularity and the evolu- is a topological constraint for colonial species in tion of Volvox, Kirk (2005) outlines 12 steps that which cells remain connected through cytoplas- define the minimum changes or innovations re- mic bridges. The morphogenetic process of in- quired to convert a C. reinhardtii-type cell to a version that is discussed below is an innovation multicellular V. carteri spheroid. These innova-

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tions are described below in an updated context growth conditions (Donnan and John 1983; that is informed by knowledge of the genomes John 1987). Colonial species, on the other from these two species and new findings that hand, have more stereotyped numbers of di- have been published in the interim. Two addi- visions to produce colonies that typically tional innovations (anisogamy and oogamy) vary in cell number by a factor of 2 (Cole- have also been added (Nishii and Miller 2010). man 2012). Moreover, unlike Chlamydomo- Six of the 12 innovations outlined by Kirk nas cells that are competent to divide as soon (2005) occur in the initial multicellular transi- as they double in size, cells in colonial spe- tion from Chlamydomonas to Gonium. The fact cies must grow large enough between repro- that half of the innovations in the lineage oc- ductive cycles so that new colonies can be curred at this step suggests that forming small formed with the appropriate number of cells. integrated functional colonies might be the In Chlamydomonas, the retinoblastoma tu- most difficult aspect of the transition to multi- mor suppressor pathway controls cell size cellularity. The idea of a bottleneck at this step is and division number (Umen and Good- consistent with the finding that the simplest enough 2001; Umen 2005; Fang et al. 2006), colonial forms are all basal to the more complex and may have been modified in colonial spe- volvocine genera. This basal positioning can cies to increase the minimum size threshold be interpreted to mean that Gonium-like colony at which division can occur. organization evolved successfully just once, and 2. Incomplete cytokinesis. Incomplete cytoki- the more complex volvocine genera arose just nesis is observed in all colonial volvocine once from among the Goniaceae (Herron and species and can result in either temporary Michod 2008; Hayama et al. 2010). The appar- or perduring cytoplasmic connections or ent difficulty of the transition between uni- bridges between postmitotic cells. Ultra- cellular Chlamydomonas and colonial Gonium structural studies show that the bridges are appears to contradict findings of experimental spatially organized within and between cells, evolution in which unicellular yeasts and Chla- and contain specialized substructures that mydomonas could be converted to facultative may represent mechanical reinforcements colonial forms in a short number of generations and/or facilitate intercellular communica- by artificial selection (Ratcliff et al. 2012, 2013). tion much like plasmodesmata in plants. However, this discrepancy is not so paradoxical Bridges can also be removed or resolved as considering the degree of evolved functionality occurs postembryonically in some species that arose in Gonium that distinguishes it from (Green et al. 1981; Coleman 2012). the disorganized cell aggregates produced dur- ing experimental evolution. It may be easy to 3. and 4. Organismal polarity and basal body form such aggregates, but they may not truly rotation. 16-cell Gonium colonies that have a recapitulate the first steps that led to the evolu- planar 4 4 arrangement of cells show po- tion of Gonium-like colonies. larity that is evident by comparing the ar- Some of the innovations below are grouped rangements of basal bodies and flagella of together in cases in which they are related, so the interior versus peripheral cells. The four cells numbering does not correspond to that de- on the interior of the colony have their basal scribed by Kirk (2005), but the progression is bodies oriented with 180˚ rotational sym- the same. metry and beat in opposite directions in a breast stroke motion just as they do in Chla- 1. Genetic modulation of cell number. As de- mydomonas. The 12 cells on the edge, how- scribed above, Chlamydomonas cells show ever, rotate their basal bodies and flagella to a inherent flexibility in mother cell size and parallel orientation that cause the colony to number of mitotic cell divisions, producing rotate in a pinwheel-like fashion as it swims two daughters under poor growth condi- forward (Greuel and Floyd 1985). The basal tions and up to 16 daughters under favorable body reorientation observed in Gonium pe-

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ripheral cells occurs in all of the motile cells (termed type B inversion) differ substantially of spheroidal volvocine genera and is crucial (Ho¨hn and Hallmann 2011) and underscore for coordinated swimming (Hoops 1984; the fact that these two species belong to inde- Ueki et al. 2010). Visible signs of organismal pendent clades of Volvox (Fig. 3A). In both types polarity are present in other aspects of colo- of inversion, cytoplasmic bridges are crucial for ny development in larger volvocine genera maintaining mechanical integrity of the cell that appear during inversion, germ-soma sheets and fixed relationships between neigh- differentiation, and asymmetric cell division boring cells. as described below. V. carteri inversionless mutants have pro- vided insights into the processes governing 5. and 6. Partial and complete inversion. As a type A inversion. One such mutant, invA, affects result of the spiral division pattern of volvo- a volvocine algal kinesin that localizes to the cy- cine algal cells described above, postmitotic toplasmic bridge region of cells (Nishii 2003). embryos have their apical ends and basal The function of InvA protein is postulated to bodies clustered on the interior of the em- involve moving the cytoplasmic bridges relative bryo (or the concave surface for Gonium). to the rest of the cell along longitudinal micro- This configuration of interior-facing basal tubules to effect cell-shape changes and tissue bodies and flagella must be reversed by in- bending. It is noteworthy that the highly similar version for the embryo to swim. Inversion C. reinhardtii ortholog of invA, IAR1, can func- involves a coordinated series of cell-shape tionally substitute for invA in Volvox despite changes resulting in a complete reversal of C. reinhardtii lacking any known process anal- embryonic curvature. Although inversion ogous to inversion (Nishii and Miller 2010). has been best studied in Volvox, it has also Additional inv loci define a second extraembry- been observed in all other colonial volvocine onic function required for inversion associated genera (Hallmann 2006a). The partial in- with enlargement of the glycoproteinvesicle that version process that causes a reversal of cur- encapsulates each embryo. When this vesicle vature in Gonium embryos is presumably fails to enlarge as it does in invB and invC related to the process of full inversion in mutants, the inverting embryo is physically con- spheroidal volvocine embryos inwhich a hol- strained and becomes stuck midway through low ball of cells turns itself completely inside inversion (Ueki and Nishii 2008, 2009). invB out. and invC encode enzymes involved in sugar Full inversion of spheroidal colonies has transport or metabolism and both have C. rein- been examined carefully in V.carteri and V.glo- hardtii orthologs. It is likely that the C. rein- bator (Viamontes and Kirk 1977; Nishii and hardtii orthologs of invB and invC proteins are Ogihara 1999; Nishii 2003; Ueki and Nishii involved in cell wall biosynthesis, but this idea 2009; Ho¨hn and Hallmann 2011), which use remains to be tested. different but related mechanisms to invert. 7. and 8. Transformation of the cell wall into In both species, inversion is driven by coordi- ECM and ECM expansion. Although indi- nated cell-shape changes that move through the vidual Gonium cell walls have a tripartite spheroid along the anteroposterior axis and structure similar to that of Chlamydomonas, drive cell sheet bending and involution. Inver- theyalso have an added outer layer that main- sion in many ways parallels gastrulation in an- tains colony cohesion and contains special- imals in which similar cell-shape changes are ized regions of electron-dense material at used to remodel the hollow, ball-like blastula cell–cell attachment points (Nozaki 1990). and generate primordial embryonic germ layers of the gastrula (Solnica-Krezel and Sepich Further modifications of the ECM are 2012). The sequence of events and types of found in the more complex colonial genera. cell-shape changes that drive inversion in V.car- These include formation of a colony boundary teri (termed type A inversion) and V. globator layer in spheroidal genera (Pandorina, Eudori-

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na, Pleodorina, and Volvox) that resembles the fin 1979). regA is a nuclear protein that is related tripartite structure of the cell wall surrounding to transcriptional repressors and expressed in individual Chlamydomonas and Gonium cells. somatic cells and required to maintain their In Eudorina, Pleodorina, and Volvox, the ECM fate (Kirk et al. 1999; Stark et al. 2001). regA is expanded to fill large spaces between cells and belongs to a family of VARL (Volvocine algae within the colony interior (Coleman 2012). Al- regA-like) proteins with 14 members in Volvox though Volvox colonies have more than one and 12 in Chlamydomonas (Duncan et al. 2006, thousand cells, ECM expansion accounts for 2007). Phylogenies of VARL proteins indicate .99% of their volume and makes them six or- complex patterns of gene duplication and loss ders of magnitude larger than an individual in both algal lineages, with no ortholog of regA C. reinhardtii cell. ECM expansion in volvocine present in C. reinhardtii. It has been hypothe- algae has some parallels with vacuolar expan- sized that VARLproteins evolved in unicellular sion in land plants that also allows massive or- and simple colonial species to coordinate tem- ganismal growth without the addition of new poral cell differentiation with environmental cells or significant protein biomass (Robaglia cues (Nedelcu and Michod 2006). et al. 2004). Although the ECM in volvocine A second class of mutants in V. carteri is at algal colonies appears transparent to the eye, it lag loci (late gonidia), whose gene products has an elaborate internal structure that has been have not been identified. In lag mutants, cells investigated in detail for V.carteri in which each that are normally destined to form gonidia in- cell has its own ECM domain and the colony as a stead adopt a somatic or quasi-somatic cell fate whole has distinguishable layers of ECM (Kirk and become flagellated and stop growing. Even- et al. 1986; Hallmann 2003). Paralleling this tually, however, lag mutant gonidia withdraw ECM expansion has been a notable increase in their flagella and redifferentiate as reproductive the number of ECM genes from two families in cells (Kirk 1988). V.carteri relative to counterparts in C. reinhard- The phenotypes of regA and lag mutants tii (Prochnik et al. 2010). The expanded families suggest that establishment and maintenance of are pherophorins that have structural and sig- cell fate in V.carteri are separable functions con- naling roles (Hallmann 2006b) and the VMPs trolled by multiple loci (Kirk 1988). Continued (Volvox metalloproteinases) that function in work on these mutants and isolation of new ECM remodeling (Heitzer and Hallmann 2002). regulatory loci promises to further clarify the There are dozens of other uncharacterized vol- origins of cell-type specification in this lineage. vocine algal protein families that are differen- tially expanded in V.carteri that may also play a 11. and 12. Asymmetric cell division and a role in multicellularity (Prochnik et al. 2010). bifurcated cell division program. As de- scribed above, the genus Volvox is poly- 9. and 10. Partial and complete germ-soma phyletic with germ-soma differentiation differentiation. Perhaps the most well-stud- established by different mechanisms in sep- ied multicellular innovation in volvocine al- arate groups (Desnitski 1995; Coleman gae is the differentiation of germ and somatic 2012). In V. carteri and its close relatives, cell types that is observed in the genera Pleo- the vegetative germ line is established early dorina and Volvox. in embryonic development by means of The genetic basis for germ-soma differenti- asymmetric cell divisions. At embryonic di- ation has been investigated in V.carteri in which vision 6 (32 ! 64 cell stage), a subset of 16 developmental mutants exist that alter cell fate. anterior cells in the embryo divides asym- In regA (somatic regenerator) mutants, somatic metrically to produce a large and small cells form normally after embryogenesis, but daughter. The large daughters divide asym- then redifferentiate into gonidia; they withdraw metrically one or two more times and then their flagella, grow, and subsequently divide cease dividing, whereas the smaller daugh- into new embryos (Starr 1970; Huskey and Grif- ters continue dividing five or six more

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times along with the remaining embryonic control cell size (Fang et al. 2006). Interestingly, cells that divide symmetrically. Asymmetric comparative genomic studies of cell cycle genes cell divisions combined with early exit from revealed an expansion of the D-type cyclins the cell cycle of the large daughters results in V.carteri compared with C. reinhardtii (Proch- in an embryo with approximately 2000 nik et al. 2010). D-type cyclins in plants and small cells and 16 large cells. The 16 large animals are activating subunits for cyclin-de- cells will mature and differentiate as gonid- pendent kinases that regulate retinoblastoma- ia, whereas the small cells become somatic related proteins through phosphorylation (Gut- (Kirk et al. 1991). zat et al. 2012). Whether the expanded D-cyclin repertoire in V.carteri enabled modifications of Mutants that disrupt asymmetric cell divi- the embryonic cell division program or contrib- sion have been identified and at least one locus, utes to germ-soma differentiation remains to be glsA, has been cloned (Miller and Kirk 1999). determined. glsA is in a conserved family of eukaryotic pro- teins that contain a dnaJ-like chaperone domain 13. and 14. Anisogamy and oogamy. Volvo- that mediates an essential interaction with cine algae recapitulate the transition from HSP70-type heat shock proteins (Cheng et al. isogamy to anisogamy to oogamy and are a 2005), as well as SANT domains that mediate model system in which to investigate the chromatin association in V. carteri (Pappas and evolution of these traits (Nozaki et al. Miller 2009). Although glsA is distributed uni- 2000; Umen 2011). C. reinhardtii is isoga- formly through the embryo, its HSP70A partner mous with two mating types, plus and mi- is distributed in a decreasing anterior-to-poste- nus, that are determined by a complex, mul- rior concentration gradient at the time of asym- tigenic mating locus (MT), with MTþ and metric division and may provide positional MT2 haplotypes (Umen 2011; De Hoff cues for localizing asymmetric cell divisions to et al. 2013). Gonium and Pandorina are the anterior of the embryo (Cheng et al. 2005). also isogamous, whereas Eudorina and re- During mitosis, glsA localizes to the spindle lated genera show a mixture with some suggesting that it might be directly involved in isogamous species and anisogamous spe- spindle positioning, but this localization was cies (Coleman 2012). The larger and more insufficient to mediate its function that may complex spheroids in the genus Pleodorina also involve transcriptional or translational reg- are anisogamous, whereas all Volvox species ulation (Cheng et al. 2005; Pappas and Miller are oogamous (Nozaki 1996). Other than 2009). Although it is not known to divide asym- C. reinhardtii MT, V.carteri is the only other metrically, C. reinhardtii has a glsA ortholog, volvocine algal mating locus characterized GAR1, that can complement a glsA mutant to date. V.carteri MT is syntenic with Chla- (Cheng et al. 2003). The function of GAR1 in mydomonas MT, but its male and female C. reinhardtii is not known, but the above find- haplotypes are genetically more complex ing suggests that at least some of the machinery and share several properties with sex chro- for asymmetric cell division existed in the uni- mosomes (Ferris et al. 2010). The develop- cellular ancestor of colonial volvocine algae. mental and evolutionary bases for oogamy Elegant experiments involving manipula- and anisogamy that are controlled by MT tion of embryonic division and daughter cell remain to be determined, but may involve size showed that cell size (rather than position the transcription factor MID (minus dom- within the embryo) is the primary determinant inance) that specifies sexual differentiation of cell fate in V. carteri (Kirk et al. 1993). The in Chlamydomonas and is found in either nature of this cell-size signal and how it controls the minus mating type or males of all vol- subsequent differentiation is unknown, but it vocine algae examined to date (Ferris and may be coupled to the retinoblastoma pathway Goodenough 1997; Nozaki et al. 2006a; that functions in Chlamydomonas to sense and Hamaji et al. 2008, 2013).

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Future Perspectives for Volvocine Algae protein families and domain structures need and Multicellularity not underlie the innovations required to achieve multicellularity as evidenced by the similar- Volvocine algae allow detailed inferences to be ity between the C. reinhardtii and V. carteri made regarding the cell biological and develop- genomes (Prochnik et al. 2010), and shared or- mental events required for the transition to igins with C. reinhardtii of key developmen- multicellularity, but have only just begun to be tal regulators in V. carteri. Similar ideas have exploited to gain mechanistic insights into how emerged from investigating the origins of devel- underlying processes evolved. The finding that opmental pathways from land plants that arose developmental mutants in Volvox can be com- in charophyte algae or the earliest embryophyte plemented with orthologous genes from Chla- lineages (Preston et al. 2011; Pires and Dolan mydomonas should spur further research into 2012; Bowman 2013). Third, lineage-specific how these genes are used in Chlamydomonas protein families such as the Chlamydomonas and what has allowed their function to be al- cell wall/Volvox ECM proteins may provide a tered for development in Volvox. The genomes particularly rich source of raw material for evo- of other volvocine algae will also soon be se- lutionary innovation. Although very little is quenced and help clarify the origins of gene known about such proteins in the volvocine lin- families that contribute to developmental inno- eage, there are many examples of proteins whose vations in the lineage. The identification and origins are unique to the animal/choanoflagel- characterization of new developmental mutants late lineage that play key roles in metazoan de- and investigation of existing mutants in both velopment (King et al. 2008; Fairclough et al. V. carteri and C. reinhardtii promises to further 2013). It can be anticipated that full genome deepen our understanding of how multicellu- sequences of charophyte algae will reveal addi- larity and evolutionary innovation occur at an tional examples of such proteins that contribute unprecedented level of detail. to the evolution of land plants.

CONCLUDING REMARKS ACKNOWLEDGMENTS The specific mechanisms used to achieve mul- I thank Gavriel Matt and Patrick Keeling for ticellular innovation differ between lineages, comments and editorial suggestions on this but some of the emerging themes and principles manuscript, and Joe Heitman for helping discovered in charophyte and volvocine algae to involve me in this collection. Research on may be more universal. First, it is clear that volvocine algal cell biology and evolution in understanding the transition to multicellularity my laboratory is supported by National Insti- requires a detailed understanding of the life cy- tutes of Health grants R01GM092744 and cle, cell biology, and ecology of simpler ances- R01GM078376. tor(s) that gave rise to multicellular descendant lineages. Indeed, research into the origins of animal multicellularity have been transformed REFERENCES by investigating their closest unicellular ances- Reference is also in this collection. tors including choanoflagellates and others (King et al. 2008; Fairclough et al. 2013; Sebe- Adair WS, Steinmetz SA, Mattson DM, Goodenough UW, Pedros et al. 2013; Alegado and King 2014). Heuser JE. 1987. Nucleated assembly of Chlamydomonas and Volvox cell walls. J Cell Biol 105: 2373–2382. Gene family expansion and novel protein do- Adl SM, Simpson AGB, Lane CE, Lukesˇ J, Bass D, Bowser SS, main organization are observed in metazoans Brown MW, Burki F, Dunthorn M, Hampl V, et al. 2012. and embryophytes and associated with some The revised classification of Eukaryotes. J Eukaryot Mi- key innovations (Floyd and Bowman 2007; De- crobiol 59: 429–514. Alegado RA, King N. 2014. Bacterial influences on animal gnan et al. 2009; Srivastava et al. 2010). Howev- origins. Cold Spring Harb Perspect Biol doi: 10.1101/ er, wholesale changes in numbers or types of cshperspect.a016162.

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Ariizumi T, Toriyama K. 2011. Genetic regulation of spor- Cocquyt E, Verbruggen H, Leliaert F, De Clerck O. 2010. opollenin synthesis and pollen exine development. Annu Evolution and cytological diversification of the green sea- Rev Plant Biol 62: 437–460. weeds (Ulvophyceae). Mol Biol Evol 27: 2052–2061. Balusˇka F, Volkmann D, Barlow PW. 2004. Eukaryotic cells Coleman AW. 2012. A comparative analysis of the Volvoca- and their cell bodies: Cell theory revised. Ann Bot 94: ceae (Chlorophyta). J Phycol 48: 491–513. 9–32. Cook ME. 2004. Cytokinesis in Coleochaete orbicularis Beardall J, Allen D, Bragg J, Finkel Z, Flynn K, Quigg A, Rees (Charophyceae): An ancestral mechanism inherited by T, Richardson A, Raven J. 2009. Allometry and stoichi- plants. Am J Bot 91: 313–320. ometry of unicellular, colonial and multicellular phyto- Cook ME, Graham LE, Lavin CA. 1998. Cytokinesis and plankton. New Phytologist 181: 295–309. nodal anatomy in the charophycean green alga Chara Becker B, Marin B. 2009. Streptophyte algae and the origin zeylanica. Protoplasma 203: 65–74. of embryophytes. Ann Bot 103: 999–1004. Cooke TJ, Poli D, Sztein AE, Cohen JD. 2002. Evolutionary Beilby MJ, Casanova MT. 2014. The physiology of Characean patterns in auxin action. Plant Mol Biol 49: 319–338. cells. Springer, Berlin. Cosgrove DJ. 2000. Loosening of plant cell walls by expan- Bell G. 1985. The origin and early evolution of germ cells as sins. Nature 407: 321–326. illustrated by the Volvocales. In The origin and evolution Cutler SR, Rodriguez PL. 2010. Abscisic acid: Emergence of sex (ed. Halvorson HO, Monroy A), pp. 221–256. Alan of a core signaling network. Annu Rev Plant Biol 61: R. Liss, New York. 651–679. Berney C, Pawlowski J. 2006. A molecular time-scale for Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols eukaryote evolution recalibrated with the continuous mi- SA, McDonald K, King N. 2011. Cell differentiation and crofossil record. Proc Biol Sci 273: 1867–1872. morphogenesis in the colony-forming choanoflagellate Besson S, Dumais J. 2011. Universal rule for the symmetric Salpingoeca rosetta. Dev Biol 357: 73–82. division of plant cells. Proc Natl Acad Sci 108: 6294–6299. De Clerck O, Bogaert KA, Leliaert F. 2012. Diversity and Bhattacharya D, Weber K, An SS, Berning-Koch W. 1998. evolution of algae. In Advances in botanical research, Actin phylogeny identifies Mesostigma viride as a flagel- Vol. 64, pp. 55–86. Elsevier, Amsterdam. late ancestor of the land plants. J Mol Evol 47: 544–550. Degnan BM, Vervoort M, Larroux C, Richards GS. 2009. Boot KJM, Libbenga KR, Hille SC, Offringa R, van Duijn B. Early evolution of metazoan transcription factors. Curr 2012. Polar auxin transport: An early invention. J Exp Bot Opin Genet Dev 19: 591–599. 63: 4213–4218. De Hoff PL, Ferris P,Olson BJSC, Miyagi A, Geng S, Umen Boraas ME, Seale DB, Boxhorn JE. 1998. Phagotrophy by a JG. 2013. Species and population level molecular profil- flagellate selects for colonial prey: A possible origin of ing reveals cryptic recombination and emergent asym- multicellularity. Evol Ecol 12: 153–164. metry in the dimorphic mating locus of C. reinhardtii. Bowman JL. 2013. Walkabout on the long branches of plant PLoS Genet 9: e1003724. evolution. Curr Opin Plant Biol 16: 70–77. Delwiche CF, Graham LE, Thomson N. 1989. Lignin-like Bowman JL, Floyd SK, Sakakibara K. 2007. Green genes- compounds and sporopollenin coleochaete, an algal comparative genomics of the green branch of life. Cell model for land plant ancestry. Science 245: 399–401. 129: 229–234. Derelle E, Ferraz C, Rombauts S, Rouze´ P,Worden AZ, Rob- Boyce CK, Zwieniecki MA, Cody GD, Jacobsen C, Wirick S, bens S, Partensky F, Degroeve S, Echeynie´ S, Cooke R, Knoll AH, Holbrook NM. 2004. Evolution of xylem lig- et al. 2006. Genome analysis of the smallest free-living nification and hydrogel transport regulation. Proc Natl eukaryote Ostreococcus tauri unveils many unique fea- Acad Sci 101: 17555–17558. tures. Proc Natl Acad Sci 103: 11647–11652. Bradley PM. 1991. Plant hormones do have a role in con- de Saint Germain A, Bonhomme S, Boyer F-D, Rameau C. trolling growth and development of algae. J Phycol 27: 2013. Novel insights into strigolactone distribution and 317–321. signalling. Curr Opin Plant Biol 16: 583–589. Braun M, Limbach C. 2006. Rhizoids and protonemata of De Smet I, Beeckman T. 2011. Asymmetric cell division in characean algae: Model cells for research on polarized land plants and algae: The driving force for differentia- growth and plant gravity sensing. Protoplasma 229: tion. Nat Rev Mol Cell Biol 12: 177–188. 133–142. De Smet I, Voss U, Lau S, Wilson M, Shao N, Timme RE, Brooks J, Shaw G. 1978. Sporopollenin: A review of its Swarup R, Kerr I, Hodgman C, Bock R, et al. 2011. Un- chemistry, palaeochemistry and geochemistry. Grana raveling the evolution of auxin signaling. Plant Physiol 17: 91–97. 155: 209–221. Buss LW.1987. The evolution of individuality. Princeton Uni- Desnitski A. 1995. A review on the evolution of development versity Press, Princeton. in Volvox-morphological and physiological aspects. Eur J Cheng Q, Fowler R, Tam L-W, Edwards L, Miller SM. 2003. Protist 31: 241–247. The role of GlsA in the evolution of asymmetric cell Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulv- division in the green alga Volvox carteri. Dev Genes Evol skov P, Willats WG. 2012. The cell walls of green algae: 213: 328–335. A journey through evolution and diversity. Front Plant Cheng Q, Pappas V,Hallmann A, Miller SM. 2005. Hsp70A Sci 3. and GlsA interact as partner chaperones to regulate asym- Donnan L, John PC. 1983. Cell cycle control by timer and metric division in Volvox. Dev Biol 286: 537–548. sizer in Chlamydomonas. Nature 304: 630–633.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016170 21 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press

J.G. Umen

Dring MJ. 1988. Photocontrol of development in algae. evolution of intercellular communication in higher Annu Rev Plant Physiol Plant Mol Biol 39: 157–174. plants. Planta 192: 347–358. Duncan L, Nishii I, Howard A, Kirk D, Miller SM. 2006. Fritsch FE. 1948. The structure and reproduction of the algae. Orthologs and paralogs of regA, a master cell-type regu- Cambridge University Press, Cambridge. latory gene in Volvox carteri. Curr Genet 50: 61–72. Galway ME, Hardham AR. 1991. Immunofluorescent local- Duncan L, Nishii I, Harryman A, Buckley S, Howard A, ization of microtubules throughout the cell cycle in the Friedman NR, Miller SM. 2007. The VARL gene family green alga Mougeotia (Zygnemataceae). Am J Bot 78: and the evolutionary origins of the master cell-type reg- 451–461. ulatory gene, regA, in Volvox carteri. J Mol Evol 65: 1–11. Graham LE. 1984. Coleochaete and the origin of land plants. Dupuy L, Mackenzie J, Haseloff J. 2010. Coordination of Am J Bot 71: 603–608. plant cell division and expansion in a simple morphoge- Graham LE. 1996. Green algae to land plants: An evolution- netic system. Proc Natl Acad Sci 107: 2711–2716. ary transition. J Plant Res 109: 241–251. Ehler LL, Dutcher SK. 1998. Pharmacological and genetic Graham LE, Wilcox LW. 1983. The occurrence and phylo- evidence for a role of rootlet and phycoplast microtubules genetic significance of putative placental transfer cells in in the positioning and assembly of cleavage furrows in the green alga Coleochaete. Am J Bot 70: 113–120. Chlamydomonas reinhardtii. Cell Motil Cytoskeleton 40: 193–207. Graham LK, Wilcox LW. 2000. The origin of alternation of generations in land plants: A focus on matrotrophy and Ehler LL, Holmes JA, Dutcher SK. 1995. Loss of spatial hexose transport. Philos Trans R Soc Lond B Biol Sci 355: control of the mitotic spindle apparatus in a Chlamydo- 757–766; discussion 766–767. monas reinhardtii mutant strain lacking basal bodies. Ge- netics 141: 945–960. Graham LE, Cook ME, Busse JS. 2000. The origin of plants: Body plan changes contributing to a major evolutionary Elhiti M, Stasolla C. 2009. Structure and function of homo- radiation. Proc Natl Acad Sci 97: 4535–4540. domain-leucine zipper (HD-Zip) proteins. Plant Signal Behav 4: 86–88. Graham LE, Graham JM, Wilcox LW. 2009. Algae. Benja- min-Cummings, San Francisco. Emiliani G, Fondi M, Fani R, Gribaldo S. 2009. A horizontal gene transfer at the origin of phenylpropanoid metabo- Graham LE, Arancibia-Avila P, Taylor WA, Strother PK, lism: A key adaptation of plants to land. Biol Direct 4: 7. Cook ME. 2012. Aeroterrestrial Coleochaete (Strepto- Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, Rob- phyta, Coleochaetales) models early plant adaptation to ertson HM, Begovic E, Richter DJ, Russ C, Westbrook MJ, land. Am J Bot 99: 130–144. et al. 2013. Premetazoan genome evolution and the reg- Grauvogel C, Petersen J. 2007. Isoprenoid biosynthesis au- ulation of cell differentiation in the choanoflagellate Sal- thenticates the classification of the green alga Mesostigma pingoeca rosetta. Genome Biol 14: R15. viride as an ancient streptophyte. Gene 396: 125–133. Fang S-C, de los Reyes C, Umen JG. 2006. Cell size check- Green KJ, Viamontes GI, Kirk DL. 1981. Mechanism of point control by the retinoblastoma tumor suppressor formation, ultrastructure, and function of the cytoplas- pathway. PLoS Genet 2: e167. mic bridge system during morphogenesis in Volvox. J Cell Faulkner CR, Blackman LM, Cordwell SJ, Overall RL. 2005. Biol 91: 756–769. Proteomic identification of putative plasmodesmatal Greuel BT, Floyd GL. 1985. Development of the flagellar proteins from Chara corallina. Proteomics 5: 2866–2875. apparatus and flagellar orientation in the colonial green Ferris PJ, Goodenough UW. 1997. Mating type in Chlamy- alga Gonium pectorale (Volvocales). J Phycol 21: 358–371. domonas is specified by mid, the minus-dominance gene. Grosberg R, Strathmann R. 2007. The evolution of multi- Genetics 146: 859–869. cellularity: A minor major transition? Annu Rev Ecol Evol Ferris P, Olson BJSC, De Hoff PL, Douglass S, Casero D, Syst 38: 621–654. Prochnik S, Geng S, Rai R, Grimwood J, Schmutz J, Gu¨de H. 1979. Grazing by protozoa as selection factor for et al. 2010. Evolution of an expanded sex-determining activated sludge bacteria. Microb Ecol 5: 225–237. locus in Volvox. Science 328: 351–354. Gunnison D, Alexander M. 1975. Basis for the resistance of Finet C, Timme RE, Delwiche CF, Marle´taz F. 2010. Multi- several algae to microbial decomposition. Appl Microbiol gene phylogeny of the green lineage reveals the origin and 29: 729–738. diversification of land plants. Curr Biol 20: 2217–2222. Gutzat R, Borghi L, Gruissem W. 2012. Emerging roles of Floyd SK, Bowman JL. 2007. The ancestral developmental RETINOBLASTOMA-RELATED proteins in evolution tool kit of land plants. Int J Plant Sci 168: 1–35. and plant development. Trends Plant Sci 17: 139–148. Floyd GL, Stewart KD, Mattox KR. 1972. Cellular organiza- Hackenberg D, Sakayama H, Nishiyama T, Pandey S. 2013. tion, mitosis, and cytokinesis in the Ulotrichalean Alga, Characterization of the heterotrimeric G-protein com- Klebsormidium. J Phycol 8: 176–184. plex and its regulator from the green alga Chara braunii Floyd SK, Zalewski CS, Bowman JL. 2006. Evolution of class expands the evolutionary breadth of plant G-protein sig- III homeodomain-leucine zipper genes in streptophytes. naling. Plant Physiol 163: 1510–1517. Genetics 173: 373–388. Haig D. 2010. What do we know about Charophyte (Strep- Fowke LC, Pickett-Heaps JD. 1969. Cell division in Spiro- tophyta) life cycles? J Phycol 46: 860–867. gyra: II. Cytokinesis. J Phycol 5: 273–281. Hall JD, McCourt RM, Delwiche CF. 2008. Patterns of cell Franceschi VR, Ding B, Lucas WJ. 1994. Mechanism of plas- division in the filamentous Desmidiaceae, close green modesmata formation in characean algae in relation to algal relatives of land plants. Am J Bot 95: 643–654.

22 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016170 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press

Multicellularity in Green Algae and Plants

Hallmann A. 2003. Extracellular matrix and sex-inducing Ispolatov I, Ackermann M, Doebeli M. 2012. Division of pheromone in Volvox. Int Rev Cytol 227: 131–182. labour and the evolution of multicellularity. Proc Biol Hallmann A. 2006a. Morphogenesis in the family Volvoca- Sci 279: 1768–1776. ceae: Different tactics for turning an embryo right-side Jacobs WP.1970. Development and regeneration of the algal out. Protist 157: 445–461. giant coenocyte Caulerpa. Ann NY Acad Sci 175: 732– Hallmann A. 2006b. The pherophorins: Common, versatile 748. building blocks in the evolution of extracellular matrix Jin Q, Scherp P, Heimann K, Hasenstein KH. 2008. Auxin architecture in Volvocales. Plant J 45: 292–307. and cytoskeletal organization in algae. Cell Biol Int 32: 542–545. Hamaji T, Ferris PJ, Coleman AW, Waffenschmidt S, Taka- hashi F, Nishii I, Nozaki H. 2008. Identification of the John P. 1987. Control points in the Chlamydomonas cell minus-dominance gene ortholog in the mating-type lo- cycle. In Algal development (ed. Wiessner W, Robinson cus of Gonium pectorale. Genetics 178: 283–294. DG, Starr RC), Springer, Berlin. Johnson UG, Porter KR. 1968. Fine structure of cell division Hamaji T, Ferris PJ, Nishii I, Nishimura Y, Nozaki H. 2013. in Chlamydomonas reinhardi. Basal bodies and microtu- Distribution of the sex-determining gene MID and mo- bules. J Cell Biol 38: 403–425. lecular correspondence of mating types within the isog- amous genus Gonium (Volvocales, Chlorophyta). PLoS Johri MM. 2004. Possible origin of hormonal regulation in ONE 8: e64385. green plants. Proc Natl Acad Sci India B 70: 335–365. Katsaros CI, Varvarigos V, Gachon CMM, Brand J, Moto- Hartung W. 2010. The evolution of abscisic acid (ABA) and mura T, Nagasato C, Ku¨pper FC. 2011. Comparative ABA function in lower plants, fungi and lichen. Funct immunofluorescence and ultrastructural analysis of mi- Plant Biol 37: 806. crotubule organization in Uronema sp., Klebsormidium Hauser F,Waadt R, Schroeder JI. 2011. Evolution of abscisic flaccidum, K. subtilissimum, Stichococcus bacillaris and acid synthesis review and signaling mechanisms. Curr S. chloranthus (Chlorophyta). Protist 162: 315–331. Biol 21: R346–R355. Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud P-F, Hayama M, Nakada T,Hamaji T,Nozaki H. 2010. Morphol- Pan A, Quatrano RS. 2010. Role of ABA and ABI3 in ogy, molecular phylogeny and taxonomy of Gonium desiccation tolerance. Science 327: 546. maiaprilis sp. nov. (Goniaceae, Chlorophyta) from Japan. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chap- Phycologia 49: 221–234. man J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. Hegemann P. 2008. Algal sensory photoreceptors—Annual 2008. The genome of the choanoflagellate Monosiga bre- review of plant biology. Annu Rev Plant Biol 59: 167. vicollis and the origin of metazoans. Nature 451: 783– Heitzer M, Hallmann A. 2002. An extracellular matrix-lo- 788. calized metalloproteinase with an exceptional QEXXH Kirk DL. 1988. The ontogeny and phylogeny of cellular dif- metal binding site prefers copper for catalytic activity. J ferentiation in Volvox. Trends Genet 4: 32–36. Biol Chem 277: 28280–28286. Kirk DL. 1998. Volvox. Cambridge University Press, Cam- Hepler PK. 1982. Endoplasmic reticulum in the formation bridge. of the cell plate and plasmodesmata. Protoplasma 111: Kirk DL. 2003. Seeking the ultimate and proximate causes of 121–133. Volvox multicellularity and cellular differentiation. Integr Herna´ndez-Herna´ndez V, Niklas KJ, Newman SA, Benı´tez Comp Biol 43: 247–253. M. 2012. Dynamical patterning modules in plant devel- Kirk DL. 2005. A twelve-step program for evolving multi- opment and evolution. Int J Dev Biol 56: 661–674. cellularity and a division of labor. BioEssays 27: 299–310. Herron MD, Michod RE. 2008. Evolution of complexity in Kirk DL, Birchem R, King N. 1986. The extracellular matrix the volvocine algae: Transitions in individuality through of Volvox: A comparative study and proposed system of Darwin’s eye. Evolution 62: 436–451. nomenclature. J Cell Sci 80: 207–231. Herron MD, Hackett JD, Aylward FO, Michod RE. 2009. Kirk DL, Kaufman MR, Keeling RM, Stamer KA. 1991. Ge- netic and cytological control of the asymmetric divisions Triassic origin and early radiation of multicellular volvo- that pattern the Volvox embryo. Dev Suppl 1: 67–82. cine algae. Proc Natl Acad Sci 106: 3254–3258. Kirk MM, Ransick A, McRae SE, Kirk DL. 1993. The rela- Ho¨hn S, Hallmann A. 2011. There is more than one way to tionship between cell size and cell fate in Volvox carteri. J turn a spherical cellular monolayer inside out: Type B Cell Biol 123: 191–208. embryo inversion in Volvox globator. BMC Biol 9: 89. Kirk MM, Stark K, Miller SM, Mu¨ller W,Taillon BE, Gruber Holmes JA, Dutcher SK. 1989. Cellular asymmetry in Chla- H, Schmitt R, Kirk DL. 1999. regA, a Volvox gene that mydomonas reinhardtii. J Cell Sci 94: 273–285. plays a central role in germ-soma differentiation, encodes Hoops HJ. 1984. Somatic cell flagellar apparatuses in two a novel regulatory protein. Development 126: 639–647. species of Volvox (Chlorophyceae). J Phycol 20: 20–27. Kla¨mbt D, Knauth B, Dittmann I. 1992. Auxin dependent Huskey RJ, Griffin BE. 1979. Genetic control of somatic cell growth of rhizoids of Chara globularis. Physiol Plant 85: differentiation in Volvox analysis of somatic regenerator 537–540. mutants. Dev Biol 72: 226–235. Knoll AH. 2011. The multiple origins of complex multicel- Imahori K, Iwasa K. 1965. Pure culture and chemical regu- lularity. Annu Rev Earth Planet Sci 39: 217–239. lation of the growth of charophytes. Phycologia 4: 127– Koufopanou V. 1994. The evolution of soma in the Volvo- 134. cales. Am Nat 143: 907–931.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016170 23 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press

J.G. Umen

Kwiatkowska M. 2003. Plasmodesmal changes are related to Martone PT, Estevez JM, Lu F, Ruel K, Denny MW, Somer- different developmental stages of antheridia of Chara ville C, Ralph J. 2009. Discovery of lignin in seaweed species. Protoplasma 222: 1–11. reveals convergent evolution of cell-wall architecture. Kwiatkowska M, Wojtczak A, Poptoriska K. 1998. Effect of Curr Biol 19: 169–175. GA3 treatment on the number of spermatozoids and McCourt RM, Delwiche CF, Karol KG. 2004. Charophyte endopolyploidy levels of non-generative cells in Anther- algae and land plant origins. Trends Ecol Evol (Amst) idia of Chara vulgaris L. Plant Cell Physiol 39: 1388–1390. 19: 661–666. Langdale JA, Harrison CJ. 2008. Developmental transitions Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz during the evolution of plant form. In Evolving pathways: SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Key themes in evolutionary developmental biology (ed. Mare´chal-Drouard L, et al. 2007. The Chlamydomonas Minelli A), pp. 299–316. Cambridge University Press, genome reveals the evolution of key animal and plant Cambridge. functions. Science 318: 245–250. Lau S, Shao N, Bock R, Jurgens G, De Smet I. 2009. Auxin Michod RE, Roze D. 2001. Cooperation and conflict in the signaling in algal lineages: Fact or myth? Trends Plant Sci evolution of multicellularity. Heredity 86: 1–7. 14: 182–188. Miller SM, Kirk DL. 1999. glsA, a Volvox gene required for Laurin-Lemay S, Brinkmann H, Philippe H. 2012. Origin of asymmetric division and germ cell specification, encodes land plants revisited in the light of sequence contamina- a chaperone-like protein. Development 126: 649–658. tion and missing data. Curr Biol 22: R593–R594. Mine I, Menzel D, Okuda K. 2008. Morphogenesis in giant- Lee J-H, Lin H, Joo S, Goodenough U. 2008. Early sexual celled algae. Int Rev Cell Mol Biol 266: 37–83. origins of homeoprotein heterodimerization and evolu- Nakada T,Misawa K, Nozaki H. 2008. Molecular systematics / tion of the plant KNOX BELL family. Cell 133: 829–840. of Volvocales (Chlorophyceae, Chlorophyta) based on Lee J-H, Waffenschmidt S, Small L, Goodenough U. 2007. exhaustive 18S rRNA phylogenetic analyses. Mol Phylo- Between-species analysis of short-repeat modules in cell genet Evol 48: 281–291. wall and sex-related hydroxyproline-rich glycoproteins of Nedelcu AM, Michod RE. 2006. The evolutionary origin of Chlamydomonas. Plant Physiol 144: 1813–1826. an altruistic gene. Mol Biol Evol 23: 1460–1464. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen Nedelcu AM, Borza T, Lee RW. 2006. A land plant-specific H, Delwiche CF, De Clerck O. 2012. Phylogeny and mo- multigene family in the unicellular Mesostigma argues for lecular evolution of the green algae. Crit Rev Plant Sci 31: its close relationship to Streptophyta. Mol Biol Evol 23: 1–46. 1011–1015. Lemieux C, Otis C, Turmel M. 2000. Ancestral chloroplast Niklas KJ. 2000. The evolution of plant body plans—A bio- genome in Mesostigma viride reveals an early branch of mechanical perspective. Ann Bot 85: 411–438. green plant evolution. Nature 403: 649–652. Niklas KJ, Kutschera U. 2009. The evolution of the land Lemieux C, Otis C, Turmel M. 2007. A clade uniting the plant life cycle. New Phytologist 185: 27–41. green algae Mesostigma viride and Chlorokybus atmophy- ticus represents the deepest branch of the Streptophyta in Niklas KJ, Newman SA. 2013. The origins of multicellular chloroplast genome-based phylogenies. BMC Biol 5: 2. organisms. Evol Dev 15: 41–52. Lewis LA, McCourt RM. 2004. Green algae and the origin of Niklas KJ, Cobb ED, Crawford DR. 2013. The evo-devo of land plants. Am J Bot 91: 1535–1556. multinucleate cells, tissues, and organisms, and an alter- Ligrone R, Duckett JG, Renzaglia KS. 1993. The gameto- native route to multicellularity. Evol Dev 15: 466–474. phyte-sporophyte junction in land plants. In Advances Nishii I. 2003. A kinesin, InvA, plays an essential role in in Botanical Research, Vol.19, pp. 231–318. Elsevier, Am- Volvox morphogenesis. Cell 113: 743–753. sterdam. Nishii I, Miller SM. 2010. Volvox: Simple steps to develop- Lokhorst GM, Star W. 1985. Ultrastructure of mitosis and mental complexity? Curr Opin Plant Biol 13: 646–653. cytokinesis in Klebsormidium Mucosum nov. comb., for- Nishii I, Ogihara S. 1999. Actomyosin contraction of the merly Ulothrix Verrucosa (Chlorophyta). J Phycol 21: posterior hemisphere is required for inversion of the Vol- 466–476. vox embryo. Development 126: 2117–2127. Lucas WJ, Lee J-Y. 2004. Plasmodesmata as a supracellular Nishimura Y, Shikanai T, Nakamura S, Kawai-Yamada M, control network in plants. Nat Rev Mol Cell Biol 5: 712– Uchimiya H. 2012. Gsp1 triggers the sexual developmen- 726. tal program including inheritance of chloroplast DNA Mandoli DF. 1998. Elaboration of body plan and phase and mitochondrial DNA in Chlamydomonas reinhardtii. change during development of Acetabularia: How is the Plant Cell 24: 2401–2414. complex architecture of a giant unicell built? Annu Rev Nozaki H. 1990. Ultrastructure of the extracellular matrix of Plant Physiol Plant Mol Biol 49: 173–198. Gonium (Volvocales, Chlorophyta). Phycologia 29: 1–8. Manton I, Ettl H. 1965. Observations on the fine structure of Nozaki H. 1996. Morphology and evolution of sexual repro- Mesostigma viride lauterborn. Bot J Linn Soc 59: 175–184. duction in the Volvocaceae (Chlorophyta). J Plant Res Marchant HJ, Pickett Heaps JD. 1973. Mitosis and cytoki- 109: 353–361. nesis in Coleochaete scutata. J Phycol 9: 461–471. Nozaki H, Misawa K, Kajita T, Kato M, Nohara S, Watanabe Marin B, Melkonian M. 1999. Mesostigmatophyceae, a new MM. 2000. Origin and evolution of the colonial volvo- class of streptophyte green algae revealed by SSU rRNA cales (Chlorophyceae) as inferred from multiple, chloro- sequence comparisons. Protist 150: 399–417. plast gene sequences. Mol Phylogenet Evol 17: 256–268.

24 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016170 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press

Multicellularity in Green Algae and Plants

Nozaki H, Mori T, Misumi O, Matsunaga S, Kuroiwa T. Proseus TE, Boyer JS. 2012. Pectate chemistry links cell ex- 2006a. Males evolved from the dominant isogametic pansion to wall deposition in Chara corallina. Plant Sig- mating type. Curr Biol 16: R1018–R1020. nal Behav 7: 1490–1492. Nozaki H, Ott FD, Coleman AW. 2006b. Morphology, mo- Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, lecular phylogeny and taxonomy of two new species of Yoneyama K, Nogue F, Rameau C. 2011. Strigolactones Pleodorina (Volvoceae, Chlorophyceae). J Phycol 42: regulate protonema branching and act as a quorum sens- 1072–1080. ing-like signal in the moss Physcomitrella patens. Devel- Pandey S, Assmann SM. 2004. The Arabidopsis putative G opment 138: 1531–1539. protein-coupled receptor GCR1 interacts with the G pro- Queller DC. 2000. Relatedness and the fraternal major tran- tein asubunit GPA1 and regulates abscisic acid signaling. sitions. Philos Trans R Soc Lond B Biol Sci 355: 1647– Plant Cell 16: 1616–1632. 1655. Pappas V,Miller SM. 2009. Functional analysis of the Volvox Quodt V, Faigl W, Saedler H, Mu¨nster T. 2007. The MADS- carteri asymmetric division protein GlsA. Mech Dev 126: domain protein PPM2 preferentially occurs in gametan- 842–851. gia and sporophytes of the moss Physcomitrella patens. Parker GA, Baker RR, Smith VG. 1972. The origin and evo- Gene 400: 25–34. lution of gamete dimorphism and the male-female phe- Randerson JP, Hurst LD. 2001. The uncertain evolution of nomenon. J Theor Biol 36: 529–553. the sexes. Trends Ecol Evol 16: 571–579. Petersen J, Teich R, Becker B, Cerff R, Brinkmann H. 2006. Ratcliff WC, Denison RF, Borrello M, Travisano M. 2012. The GapA/B gene duplication marks the origin of Strep- Experimental evolution of multicellularity. Proc Natl tophyta (charophytes and land plants). Mol Biol Evol 23: Acad Sci 109: 1595–1600. 1109–1118. Ratcliff WC, Herron MD, Howell K, Pentz JT, Rosenzweig F, Pickett-Heaps JD. 1967. Ultrastructure and differentiation Travisano M. 2013. Experimental evolution of an alter- in Chara sp: II. Mitosis. Aust J Biol Sci 20: 883–894. nating uni- and multicellular life cycle in Chlamydomo- Pickett-Heaps JD. 1968. Ultrastructure and differentiation nas reinhardtii. Nat Commun 4: 2742. in Chara sp: III. Formation of the antheridium. Aust J Biol Raven JA. 1997. Miniview: Multiple origins of plasmodes- Sci 21: 255–274. mata. Eur J Phycol 32: 95–101. Pickett-Heaps JD. 1975. Green alage, structure, reproduction Raven JA. 2013. Polar auxin transport in relation to long- and evolution in selected genera. Sinauer, Sunderland, distance transport of nutrients in the Charales. J Exp Bot MA. 64: 1–9. Pickett-Heaps J. 1976. Cell division in eucaryotic algae. Bio- Rethy R. 1968. Red (R), far-red (FR) photoreversible effects Science 26: 445–450. on the growth of Chara sporelings. Z Pflanzenphysiol 59: Pires ND, Dolan L. 2012. Morphological evolution in land 100–102. plants: New designs with old genes. Philos Trans R Soc Robaglia C, Menand B, Lei Y,Sormani R, Nicolaı¨M, Gery C, Lond B Biol Sci 367: 508–518. Teoule´ E, Deprost D, Meyer C. 2004. Plant growth: The Popper ZA, Michel G, Herve´ C, Domozych DS, Willats translational connection. Biochem Soc Trans 32: 581– WGT,Tuohy MG, Kloareg B, Stengel DB. 2011. Evolution 584. and diversity of plant cell walls: From algae to flowering Rodriguez-Ezpeleta N, Philippe H, Brinkmann H, Becker B, plants. Annu Rev Plant Biol 62: 567–590. Melkonian M. 2006. Phylogenetic analyses of nuclear, Preston JC, Hileman LC, Cubas P. 2011. Reduce, reuse, and mitochondrial, and plastid multigene data sets support recycle: Developmental evolution of trait diversification. the placement of Mesostigma in the Streptophyta. Mol Am J Bot 98: 397–403. Biol Evol 24: 723–731. Prigge MJ, Clark SE. 2006. Evolution of the class III HD-Zip Rokas A. 2008. The origins of multicellularity and the early gene family in land plants. Evol Dev 8: 350–361. history of the genetic toolkit for animal development. Prigge MJ, Lavy M, Ashton NW, Estelle M. 2010. Physcomi- Annu Rev Genet 42: 235–251. trella patens auxin-resistant mutants affect conserved el- Ruyter-Spira C, Bouwmeester H. 2012. Strigolactones affect ements of an auxin-signaling pathway. Curr Biol 20: development in primitive plants. The missing link be- 1907–1912. tween plants and arbuscular mycorrhizal fungi? New Phy- Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, tologist 195: 730–733. Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, et al. Sabbatini MR, Argu¨ello JA, Ferna´ndez OA, Bottini RA. 2010. Genomic analysis of organismal complexity in the 1987. Dormancy and growth-inhibitor levels in oospores multicellular green alga Volvox carteri. Science 329: 223– of Chara contraria A. Braun ex Ku¨tz. (Charophyta). 226. Aquat Bot 28: 189–194. Pro¨schold T, Marin B, Schlo¨sser UG, Melkonian M. 2001. Sakakibara K, Nishiyama T, Kato M, Hasebe M. 2001. Iso- Molecular phylogeny and taxonomic revision of Chlamy- lation of homeodomain-leucine zipper genes from the domonas (Chlorophyta): I. Emendation of Chlamydomo- moss Physcomitrella patens and the evolution of homeo- nas Ehrenberg and Chloromonas Gobi, and description of domain-leucine zipper genes in land plants. Mol Biol Evol Oogamochlamys gen. nov. and Lobochlamys gen. nov. Pro- 18: 491–502. tist 152: 265–300. Sakakibara K, Ando S, Yip HK, Tamada Y, Hiwatashi Y, Pro¨schold T, Harris EH, Coleman AW. 2005. Portrait of a Murata T, Deguchi H, Hasebe M, Bowman JL. 2013. species: Chlamydomonas reinhardtii. Genetics 170: 1601– KNOX2 genes regulate the haploid-to-diploid morpho- 1610. logical transition in land plants. Science 339: 1067–1070.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016170 25 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press

J.G. Umen

Sawa T, Frame PW. 1974. Comparative anatomy of Charo- Starr RC. 1970. Control of differentiation in Volvox. Symp phyta: I. Oogonia and oospores of Tolypella—With spe- Soc Dev Biol 29: 59–100. cial reference to the sterile oogonial cell. Bull Torrey Bot Stebbins GL, Hill G. 1980. Did multicellular plants invade Club 136–144. the land? Am Nat 115: 342–353. Sawitzky H, Grolig F. 1995. Phragmoplast of the green alga Stewart KD, Mattox KR. 1975. Comparative cytology, evo- Spirogyra is functionally distinct from the higher plant lution and classification of the green algae with some phragmoplast. J Cell Biol 130: 1359–1371. consideration of the origin of other organisms with chlo- Sebe-Pedros A, Irimia M, del Campo J, Parra-Acero H, Russ rophylls a and b. Botan Rev 41: 104–135. C, Nusbaum C, Blencowe BJ, Ruiz-Trillo I. 2013. Regu- Stirk WA,Ba´lint P,Tarkowska´ D, Nova´k O, Strnad M, O¨ rdo¨g lated aggregative multicellularity in a close unicellular V, van Staden J. 2013a. Hormone profiles in microalgae: relative of metazoa. Elife 2: e01287. Gibberellins and brassinosteroids. Plant Physiol Biochem Sederias J, Colman B. 2007. The interaction of light and low 70: 348–353. temperature on breaking the dormancy of Chara vulgaris Stirk WA, O¨ rdo¨gV,Nova´k O, Rolcˇı´k J, Strnad M, Ba´lint P, oospores. Aquat Bot 87: 229–234. van Staden J. 2013b. Auxin and cytokinin relationships in Sekimoto H, Abe J, Tsuchikane Y. 2012. New insights into 24 microalgal strains 1. J Phycol 49: 459–467. the regulation of sexual reproduction in Closterium. Int Szathma´ry E, Smith JM. 1995. The major evolutionary tran- Rev Cell Mol Biol 297: 309–338. sitions. Nature 374: 227–232. Sˇetlı´k I, Zachleder V. 1984. The multiple fission cell repro- Sztein AE, Cohen JD, Cooke TJ. 2000. Evolutionary patterns ductive patterns in algae. In The microbial cell cycle in the auxin metabolism of green plants. Int J Plant Sci (ed. Nurse P, Streiblova´ E), pp. 253–279. CRC, Boca 161: 849–859. Raton, FL. Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani Shikano S, Luckinbill LS, Kurihara Y.1990. Changes of traits M, Henschel K, Mu¨nster T, Theissen G, Nozaki H, Ito in a bacterial population associated with protozoal M. 2005. Characterization of MADS-box genes in char- predation. Microb Ecol 20: 75–84. ophycean green algae and its implication for the evolu- Simon A, Glo¨ckner G, Felder M, Melkonian M, Becker B. tion of MADS-box genes. Proc Natl Acad Sci 102: 2436– 2006. ESTanalysis of the scaly green flagellate Mesostigma 2441. viride (Streptophyta): Implications for the evolution of Tarakhovskaya ER, Maslov YI, Shishova MF. 2007. Phyto- green plants (Viridiplantae). BMC Plant Biol 6: 2. hormones in algae. Russ J Plant Physiol 54: 163–170. Singer SD, Krogan NT, Ashton NW. 2007. Clues about the ancestral roles of plant MADS-box genes from a func- Timme RE, Bachvaroff TR, Delwiche CF. 2012. Broad phy- tional analysis of moss homologues. Plant Cell Rep 26: logenomic sampling and the sister lineage of land plants. 1155–1169. PLoS ONE 7: e29696. Smaczniak C, Immink RGH, Angenent GC, Kaufmann K. Timme RE, Delwiche CF.2010. Uncovering the evolutionary 2012. Developmental and evolutionary diversity of plant origin of plant molecular processes: Comparison of Co- MADS-domain factors: Insights from recent studies. De- leochaete (Coleochaetales) and Spirogyra (Zygnematales) velopment 139: 3081–3098. transcriptomes. BMC Plant Biol 10: 96. Smolarkiewicz M, Dhonukshe P. 2013. Formative cell divi- Tsekos I. 1999. The sites of cellulose synthesis in algae: Di- sions: Principal determinants of plant morphogenesis. versity and evolution of cellulose-synthesizing enzyme Plant Cell Physiol 54: 333–342. complexes. J Phycol 35: 635–655. Solnica-Krezel L, Sepich DS. 2012. Gastrulation: Making Turmel M, Ehara M, Otis C, Lemieux C. 2002. Phylogenetic and shaping germ layers. Annu Rev Cell Dev Biol 28: relationships among streptophytes as inferred from chlo- 687–717. roplast small and large subunit rRNA gene sequences. J Phycol 38: 364–375. Sørensen I, Domozych D, Willats WGT. 2010. How have plant cell walls evolved? Plant Physiol 153: 366–372. Ueki N, Nishii I. 2008. Idaten is a new cold-inducible Sørensen I, Pettolino FA, Bacic A, Ralph J, Lu F,O’Neill MA, transposon of Volvox carteri that can be used for tagging Fei Z, Rose JKC, Domozych DS, Willats WGT. 2011. The developmentally important genes. Genetics 180: 1343– charophycean green algae provide insights into the early 1353. origins of plant cell walls. Plant J 68: 201–211. Ueki N, Nishii I. 2009. Controlled enlargement of the gly- Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier coprotein vesicle surrounding a Volvox embryo requires MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hell- the InvB nucleotide-sugar transporter and is required for sten U, et al. 2010. The Amphimedon queenslandica ge- normal morphogenesis. Plant Cell 21: 1166–1181. nome and the evolution of animal complexity. Nature Ueki N, Matsunaga S, Inouye I, Hallmann A. 2010. How 466: 720–726. 5000 independent rowers coordinate their strokes in or- Stanley SM. 1973. An ecological theory for the sudden or- der to row into the sunlight: Phototaxis in the multicel- igin of multicellular life in the late precambrian. Proc Natl lular green alga Volvox. BMC Biol 8: 1–21. Acad Sci 70: 1486–1489. Umen JG. 2005. The elusive sizer. Curr Opin Cell Biol 17: Stark K, Kirk DL, Schmitt R. 2001. Two enhancers and one 435–441. silencer located in the introns of regA control somatic cell Umen JG. 2011. Evolution of sex and mating loci: An ex- differentiation in Volvox carteri. Genes Dev 15: 1449– panded view from Volvocine algae. Curr Opin Microbiol 1460. 14: 634–641.

26 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016170 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press

Multicellularity in Green Algae and Plants

Umen JG, Goodenough UW. 2001. Control of cell division Wallace S, Fleming A, Wellman CH, Beerling DJ. 2011. Evo- by a retinoblastoma protein homolog in Chlamydomo- lutionary development of the plant spore and pollen wall. nas. Genes Dev 15: 1652–1661. AoB Plants 2011: plr027. Umen JG, Olson BJSC. 2012. Genomics of volvocine algae. Wang W, Esch JJ, Shiu S-H, Agula H, Binder BM, Chang C, In Genomic insights into the biology of algae (ed. Piganeau Patterson SE, Bleecker AB. 2006. Identification of impor- G), Vol. 64, pp. 185–243. Elsevier, Amsterdam. tant regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor Vandenbussche F, Fierro AC, Wiedemann G, Reski R, Van of Arabidopsis. Plant Cell 18: 3429–3442. Der Straeten D. 2007. Evolutionary conservation of plant gibberellin signalling pathway components. BMC Plant Waters ER. 2003. Molecular adaptation and the origin of land plants. Mol Phylogenet Evol 29: 456–463. Biol 7: 65. Wodniok S, Brinkmann H, Glo¨ckner G, Heidel AJ, Philippe Vannerum K, Huysman MJJ, De Rycke R, Vuylsteke M, H, Melkonian M, Becker B. 2011. Origin of land plants: Leliaert F, Pollier J, Lu¨tz-Meindl U, Gillard J, De Veylder do conjugating green algae hold the key? BMC Evol Biol L, Goossens A, et al. 2011. Transcriptional analysis of cell 11: 104. growth and morphogenesis in the unicellular green alga Zalewski CS, Floyd SK, Furumizu C, Sakakibara K, Steven- Micrasterias (Streptophyta), with emphasis on the role of son DW,Bowman JL. 2013. Evolution of the class IV HD- expansin. BMC Plant Biol 11: 128. Zip gene family in streptophytes. Mol Biol Evol 30: 2347– Van Sandt VST, Stieperaere H, Guisez Y, Verbelen J-P, Vis- 2365. senberg K. 2007. XET activity is found near sites of Zhong B, Liu L, Yan Z, Penny D. 2013. Origin of land plants growth and cell elongation in bryophytes and some green using the multispecies coalescent model. Trends Plant Sci algae: New insights into the evolution of primary cell wall 18: 492–495. elongation. Ann Bot 99: 39–51. Zobell O, Faigl W, Saedler H, Munster T. 2010. MIKC Viamontes G, Kirk D. 1977. Cell shape changes and the MADS-Box proteins: Conserved regulators of the game- mechanism of inversion in Volvox. J Cell Biol 75: 719– tophytic generation of land plants. Mol Biol Evol 27: 730. 1201–1211.

Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016170 27 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press

Green Algae and the Origins of Multicellularity in the Plant Kingdom

James G. Umen

Cold Spring Harb Perspect Biol 2014; doi: 10.1101/cshperspect.a016170 originally published online October 16, 2014

Subject Collection The Origin and Evolution of Eukaryotes

The Persistent Contributions of RNA to Eukaryotic Origins: How and When Was the Eukaryotic Gen(om)e Architecture and Cellular Mitochondrion Acquired? Function Anthony M. Poole and Simonetta Gribaldo Jürgen Brosius Green Algae and the Origins of Multicellularity in Bacterial Influences on Animal Origins the Plant Kingdom Rosanna A. Alegado and Nicole King James G. Umen The Archaeal Legacy of Eukaryotes: A Missing Pieces of an Ancient Puzzle: Evolution of Phylogenomic Perspective the Eukaryotic Membrane-Trafficking System Lionel Guy, Jimmy H. Saw and Thijs J.G. Ettema Alexander Schlacht, Emily K. Herman, Mary J. Klute, et al. Origin and Evolution of the Self-Organizing The Neomuran Revolution and Phagotrophic Cytoskeleton in the Network of Eukaryotic Origin of Eukaryotes and Cilia in the Light of Organelles Intracellular Coevolution and a Revised Tree of Gáspár Jékely Life Thomas Cavalier-Smith On the Age of Eukaryotes: Evaluating Evidence Protein Targeting and Transport as a Necessary from Fossils and Molecular Clocks Consequence of Increased Cellular Complexity Laura Eme, Susan C. Sharpe, Matthew W. Brown, Maik S. Sommer and Enrico Schleiff et al. Origin of Spliceosomal Introns and Alternative How Natural a Kind Is ''Eukaryote?'' Splicing W. Ford Doolittle Manuel Irimia and Scott William Roy

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Protein and DNA Modifications: Evolutionary What Was the Real Contribution of Imprints of Bacterial Biochemical Diversification Endosymbionts to the Eukaryotic Nucleus? and Geochemistry on the Provenance of Insights from Photosynthetic Eukaryotes Eukaryotic Epigenetics David Moreira and Philippe Deschamps L. Aravind, A. Maxwell Burroughs, Dapeng Zhang, et al. The Eukaryotic Tree of Life from a Global Bioenergetic Constraints on the Evolution of Phylogenomic Perspective Complex Life Fabien Burki Nick Lane

For additional articles in this collection, see http://cshperspectives.cshlp.org/cgi/collection/

Copyright © 2014 Cold Spring Harbor Laboratory Press; all rights reserved