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Green Algae and the Origins of Multicellularity in the Plant Kingdom

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Green Algae and the Origins of Multicellularity in the Plant Kingdom Downloaded from http://cshperspectives.cshlp.org/ on October 8, 2021 - Published by Cold Spring Harbor Laboratory Press 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 Editors: Patrick J. Keeling and Eugene V. Koonin Additional Perspectives on The Origin and Evolution of Eukaryotes available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016170 1 Downloaded from http://cshperspectives.cshlp.org/ on October 8, 2021 - Published by Cold Spring Harbor Laboratory Press 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 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016170 Downloaded from http://cshperspectives.cshlp.org/ on October 8, 2021 - Published by Cold Spring Harbor Laboratory Press 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
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