Current Biology Vol 21 No 14 R554 invaginations, has been observed and propulsion of endocytic vesicles. requires release of actin filament fragments. Mol. Biol. Cell 21, 2905–2915. in yeast [8] and in dynamin-deleted Future research will undoubtedly focus 10. Sirotkin, V., Berro, J., Macmillan, K., Zhao, L., animal cells [11], although in both on the mechanisms that target actin and Pollard, T.D. (2010). Quantitative analysis of systems endocytic invaginations are assembly to the neck of the budding the mechanism of endocytic actin patch assembly and disassembly in fission yeast. tubular rather than spherical. Physical endocytic vesicle and possible Mol. Biol. Cell 21, 2894–2904. parameters, such as membrane feedback mechanisms linking actin 11. Ferguson, S.M., Raimondi, A., Paradise, S., Shen, H., Mesaki, K., Ferguson, A., tension [16], size of endocytosed assembly with the progress Destaing, O., Ko, G., Takasaki, J., Cremona, O., material [17] and scission activity of membrane invagination. et al. (2009). Coordinated actions of actin and of dynamins [11], likely contribute to BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell 17, the shape of endocytic invaginations. 811–822. An interesting question for future References 12. Dawson, J.C., Legg, J.A., and Machesky, L.M. 1. Galletta, B.J., Mooren, O.L., and Cooper, J.A. (2006). Bar domain proteins: a role in research is whether the actin (2010). Actin dynamics and endocytosis in tubulation, scission and actin assembly in organization around tubular yeast and mammals. Curr. Opin. Biotechnol. clathrin-mediated endocytosis. Trends Cell invaginations is similar to the actin 21, 604–610. Biol. 16, 493–498. 2. Kaksonen, M., Toret, C.P., and Drubin, D.G. 13. Suetsugu, S. (2010). The proposed functions structures around spherical (2006). Harnessing actin dynamics for of membrane curvatures mediated by the BAR invaginations observed by clathrin-mediated endocytosis. Nat. Rev. Mol. domain superfamily proteins. J. Biochem. 148, Cell Biol. 7, 404–414. 1–12. Collins et al. [4]. 3. Merrifield, C.J. (2004). Seeing is believing: 14. Wu, M., Huang, B., Graham, M., Raimondi, A., The role of actin in endocytosis imaging actin dynamics at single sites of Heuser, J.E., Zhuang, X., and De Camilli, P. in animal cells has been questioned endocytosis. Trends Cell Biol. 14, 352–358. (2010). Coupling between clathrin-dependent 4. Collins, A., Warrington, A., Taylor, K.A., and endocytic budding and F-BAR-dependent on the basis of the relatively mild Svitkina, T. (2011). Structural organization tubulation in a cell-free system. Nat. Cell Biol. effects of actin-disrupting drugs on of the actin cytoskeleton at sites of 12, 902–908. clathrin-mediated endocytosis. Curr. Biol. 21, 15. Krendel, M., Osterweil, E.K., and endocytosis [1,2]. Collins et al. [4] now 1167–1175. Mooseker, M.S. (2007). Myosin 1E interacts show that treatment of their cells with 5. Suetsugu, S. (2009). The direction of actin with synaptojanin-1 and dynamin and is concentrations of actin-disrupting polymerization for vesicle fission suggested involved in endocytosis. FEBS Lett. 581, from membranes tubulated by the EFC/F-BAR 644–650. drugs sufficient to eliminate most actin domain protein FBP17. FEBS Lett. 583, 16. Aghamohammadzadeh, S., and Ayscough, K.R. structures fails to completely eliminate 3401–3404. (2009). Differential requirements for actin during 6. Yarar, D., Waterman-Storer, C.M., and yeast and mammalian endocytosis. Nat. Cell actin collars around clathrin-coated Schmid, S.L. (2005). A dynamic actin Biol. 11, 1039–1042. structures. This observation, together cytoskeleton functions at multiple stages of 17. Kirchhausen, T. (2009). Imaging endocytic with the observed association of actin clathrin-mediated endocytosis. Mol. Biol. Cell clathrin structures in living cells. Trends Cell 16, 964–975. Biol. 19, 596–605. with at least 43% of clathrin structures, 7. Pollard, T.D., and Cooper, J.A. (2009). Actin, provides further evidence that the role a central player in cell shape and movement. Science 326, 1208–1212. Department of Cell and Developmental of actin in endocytosis in animal cells 8. Idrissi, F.Z., Grotsch, H., Fernandez- might have been under-appreciated. Golbano, I.M., Presciatto-Baschong, C., Biology, State University of New York (SUNY) By providing high-resolution images Riezman, H., and Geli, M.I. (2008). Distinct Upstate Medical University, 750 East Adams acto/myosin-I structures associate with Street, Syracuse, NY 13210, USA. of actin networks at the sites of endocytic profiles at the plasma membrane. E-mail: [email protected] clathrin-mediated endocytosis, Collins J. Cell Biol. 180, 1219–1232. 9. Berro, J., Sirotkin, V., and Pollard, T.D. (2010). et al. [4] clarify the role of actin Mathematical modeling of endocytic actin in promoting invagination, scission patch kinetics in fission yeast: disassembly DOI: 10.1016/j.cub.2011.06.029

Plant Genomics: Homoplasy Heaven Imagine if the one-time transition from splitting H2StoH2O as a source in a Lycophyte Genome of electrons in an early cyanobacterium had not occurred some two to three billion years ago. It would be hard to The recent genomic sequencing of Selaginella, a member of the lycophyte argue that Earth without molecular lineage of vascular plants, opens up all kinds of new opportunities to examine oxygen would be quite the same place the patterns of evolutionary innovation and the creation of the basic bauplan as we find it now. Life would have of plants. continued to evolve, but, in an atmosphere entirely devoid of oxygen, William E. Friedman1,2 Gould was correct in many it is reasonable to posit that the course fundamental ways; his arguments would not have led ‘‘inevitably’’ to the Steven Gould famously argued in opposed the deterministic, point we now occupy, some 4.5 billion Wonderful Life [1] that, if the tape of progressive, and highly teleological years after the planet was born. life (beginning with the Burgess views of evolutionary history as The same could be said for the Shale fauna) could be replayed, it one long slog leading ultimately and endosymbiotic event that led to the would always and inevitably turn out inevitably to the origin of humans. It capture of a purple bacterium that differently. Historical contingency is difficult to believe that certain rare ultimately established itself in the is a powerful and often stochastic evolutionary historical events have nucleated cells of eukaryotes and determinate of the course of not been critical in setting the subsequently served as the evolutionary innovation. Certainly, subsequent course of evolution. mitochondrion. Indeed, myriad events Dispatch R555

in the course of evolutionary history Vascular plants show us (and humble us) with the news that our own existence hangs by a mere thread of potentially rare EuphyllophytesEuphyllophytes LycophytesLycophytes and highly improbable events. Yet, the existence of homoplasy — multiple origins of functionally equivalent and ‘similar’ structures — s e t reminds us that there may indeed be y h p

certain paths of evolutionary innovation o s c e y s s that are essentially inevitable [2]. Take, l ms p t r o for instance, the two major clades of n erms osse

vascular land plants: the lycophytes p orm m f s esce i mosses l r nospe i and the euphyllophytes (Figure 1). The e o b k n m i b u o l common ancestor of these major p r C divisions of land plant biodiversity was Liverworts Mosses Hornworts Moniliformopses M Gy Gymnosperms Angio Angiosperms Club mosses mosses S Spike lycophytes A Arborescent a small, leafless, rootless plant with dichotomizing axes (telomes), that lived upon the surface of a relatively soil-free terrestrial world in the Silurian (Figure 2). At some point in the Silurian, a single speciation event occurred that ultimately gave rise to the lycophytes and the euphyllophytes. Although lycophytes now comprise a mere fraction of the total number of extant vascular plant species (somewhat over 1,000 out of more than 300,000), they dominated most of the world Current Biology through the end of the Permian and, by all paleobotanical accounts, slightly Figure 1. Phylogenetic relationships of extant land plants. outpaced the euphyllophytes in the Vascular plants comprise two major lineages that were established in the Silurian: lycophytes race towards greater morphological and euphyllophytes. Euphyllophytes include the moniliformopses (ferns and horsetails), complexity [3]. gymnosperms (conifers, gnetophytes, Ginkgo, and cycads) and flowering plants (angio- As currently inferred from the fossil sperms). Roots with root caps appear to have evolved once in a common ancestor of extant and phylogenetic record, subsets euphyllophytes and once in a common ancestor of lycophytes, given that fossilized early of both the lycophytes and the members of both the euphyllophytes and lycophytes appear to be rootless [6]. Leaves likely euphyllophytes independently acquired evolved more than one time in the moniliformopses [15] and once in a common ancestor of seed plants and their closest, now extinct, relatives. While all large (arborescent) lycophytes ‘roots’ with ‘root caps’ [4], ‘leaves’ are now extinct, the clade is still represented by the extant genus Isoetes. formed in precise phyllotactic patterns at a shoot apical meristem, a ‘vascular cambium’ capable of forming additional two major lineages of vascular plants of lycophytes and euphyllophytes vascular tissues that are permissive of have independently arrived at based on the use of similar ancestral arborescent growth habits, and ‘seeds’, fundamentally identical bauplans. toolkits (in essence, a form of structures in which the maternal Given the dominance of parallelism), or are they the result sporophyte produced indehiscent euphyllophytes (and particularly of different and novel assemblies megasporangia with single functional angiosperms) on present day Earth, of molecular genetic toolkits that megaspores retained within an it is not surprising that most efforts at are suggestive of a pathway of enveloping sporophytic structure [5–7]. deciphering the molecular biology convergence? Answers to these Perhaps even more remarkably, these and genomic platforms that underlie questions will ultimately depend on homoplasious developmental and the generation of plant morphology, a clear reconstruction of the structural innovations occurred in anatomy, and cell biology have been ancestral genetic toolkit for land both lineages between the Late focused on model systems in the plants [10] and an understanding of Silurian and the end of the Devonian flowering plants. Equally unsurprising how it was deployed over the [7]. Indeed, it is likely that leaves evolved is that efforts to sequence whole subsequent course of evolutionary at least twice (and probably several genomes have also focused largely history. times more) in euphyllophytes [6,7].The on key members of the angiosperms. A recent publication in Science by vascular cambium evolved once in the But, this limitation of study systems Banks et al. [11] of the first lycophyte lycophytes and as many as three precludes the opportunity to critically (Selaginella) genome to be fully separate times in the euphyllophytes address the very basis of sequenced marks the start of a [6,8], all within the evolutionary instant developmental innovation and tremendous set of opportunities to of a mere twenty or so million years! homoplasy over the course of gain insights into the history of the In a world of potentially infinite evolutionary history. Are the separately independent and often homoplasious morphospace, it is striking that the evolved roots, leaves [9], and cambia evolution of two groups of plants that Current Biology Vol 21 No 14 R556

evolution await the further availability of whole genome sequencing efforts across the broad spectrum of land Cambium evolves plant phylogenetic diversity. (one time) Nevertheless, for now, the most basic Roots and leaves evolve division in vascular plant history has been bridged — and the opportunity is 10 cm 1 m ripe for intense collaboration among genomicists, molecular geneticists, Lycophytes developmental morphologists and anatomists, and paleobotanists. It is time for botanists to reflect on the tape of life!

1 cm References Euphyllophytes 1. Gould, S.J. (1989). Wonderful Life: The Burgess Shale and the Nature of History (New York: Cambium evolves W.W. Norton & Company). (several times) 2. Sanderson, M.J., and Hufford, L. (1996). Homoplasy: The Recurrence of Similarity Roots and leaves evolve in Evolution (San Diego: Academic Press). 3. Gensel, P.G. (2008). The earliest land plants. 10 cm 1 m Annu. Rev. Ecol. Evol. Syst. 39, 459–477. 4. Raven, J.A., and Edwards, D. (2001). Roots: evolutionary origins and biogeochemical significance. J. Exp. Bot. 52, 381–401. 5. Pigg, K.B. (2001). Isoetalean lycopsid evolution: Current Biology from the Devonian to the present. Am. Fern J. 91, 99–114. 6. Friedman, W.E., Moore, R.C., and Figure 2. Reconstruction of the hypothesized common ancestor of euphyllophytes and Purugganan, M.D. (2004). The early evolution of plant development. Am. J. Bot. 91, 1726–1741. lycophytes. 7. Boyce, C.K. (2010). The evolution of plant This ancestral organism (far left), in its sporophytic phase, did not produce roots and leaves. development in a paleontological context. The entire body consisted of dichotomizing axes (telomes; green) and is likely to have crept Curr. Opin. Plant Biol. 13, 102–7. along the ground (dashed line) with plagiotropic telomic systems in addition to upright 8. Stein, W.E., Mannolini, F., VanAller Hernick, L., Landing, E., and Berry, C.M. (2007). Giant systems of photosynthetic axes. Early in the evolutionary history of euphyllophytes and lyco- cladoxylopsid trees resolve the enigma of phytes, a subclade in each lineage acquired roots with root caps and leaves. In lycophytes, the the Earth’s earliest forest stumps at Gilboa. leaves are typically simple and single-veined, while the leaves of early euphyllophytes were Nature 446, 904–907. often dichotomously veined. These differences in leaf anatomy and morphology are thought 9. Floyd, S.K., and Bowman, J.L. (2006). Distinct to reflect the separate evolutionary developmental paths that led to the innovations of leaves developmental mechanisms reflect the independent origins of leaves in vascular in euphyllophytes and lycophytes. Note also that the rooting systems of lycophytes typically plants. Curr. Biol. 16, 1911–1917. branch dichotomously from their tips, as opposed to the rooting systems of euphyllophytes, 10. Floyd, S.K., and Bowman, J.L. (2007). The in which endogenous formation of lateral roots occurs subapically. Again, these differences ancestral developmental tool kit of land plants. may (or may not) reflect the independent origins of rooting systems in these two vascular plant Int. J. Plant Sci. 168, 1–35. clades. Finally, the origin of arborescence (via a vascular cambium) evolved many separate 11. Banks, J.A., Nishiyama, T., Hasebe, M., Bowman, J.L., Gribskov, M., dePamphilis, C., times in euphyllophytes and once among lycophytes. Albert, V.A., Aono, N., Aoyama, T., and Ambrose, B.A. (2011). The Selaginella genome identifies genetic changes associated with have amazingly similar bauplans. It is the authors point out, this important the evolution of vascular plants. Science 332, even possible that future work based landmark allows us to begin the 960–963. 12. Rensing, S.A., Lang, D., Zimmer, A.D., Terry, A., on the opportunities made available process of reconstructing the ancestral Salamov, A., Shapiro, H., Nishiyama, T., by the Selaginella genome, which will genetic toolkit of vascular plants. Perroud, P.F., Lindquist, E.A., and Kamisugi, Y. (2008). The Physcomitrella genome reveals unfold in the next decade, may even Encouragingly, it follows on the heels evolutionary insights into the conquest of land weigh in on important paleobotanical of the draft genome sequence of the by plants. Science 319, 64–69. questions. While most evidence moss Physcomitrella [12]. But, it is 13. Ponting, C.P. (2008). The functional repertoires of metazoan genomes. Nat. Rev. Genet. 9, points to the independent origins also a sobering reminder of how far 689–698. of roots in lycophytes and plant biologists still have to go before 14. Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M.E., Mitros, T., euphyllophytes, at least a few a sufficient number of phylogenetically Richards, G.S., Conaco, C., Dacre, M., and paleobotanists and evolutionary diverse genomes are available to Hellsten, U. (2010). The Amphimedon morphologists are willing to consider the broader community of plant queenslandica genome and the evolution of animal complexity. Nature 466, 720–726. the possibility that the fossil record is developmentalists and evolutionists. 15. Galtier, J. (2010). The origins and early sufficiently incomplete to allow for the Unlike our zoological brethren, whose evolution of the megaphyllous leaf. Int. J. Plant possibility that the common ancestor sequenced genomes cover a broad Sci. 171, 641–661. of euphyllophytes and lycophytes spectrum of metazoan diversity [13,14], 1Department of Organismic and Evolutionary may have had roots [3]. If true, surely plant biologists still await fully Biology, Harvard University, 26 Oxford there must be telltale signs left behind sequenced genomes for most major Street, Cambridge, MA 02138, USA. 2Arnold in the footprints of the genome. lineages, including liverworts, ferns, Arboretum of Harvard University, 1300 Publication of the lycophyte horsetails, conifers, cycads and Centre Street, Boston, MA 02131, USA. genome by Banks and her colleagues Ginkgo. Thus, many key insights E-mail: [email protected] around the world is certainly cause into the remarkably similar and for celebration among botanists. As homoplasious paths of developmental DOI: 10.1016/j.cub.2011.05.055