the evolution of the land plant life cycle

Tansley review

The evolution of the land plant lifecycle

Author for correspondence:Karl J. Niklas

Tel: 001 607 255 8727Email: [email protected]

Received: 20 July 2009Accepted: 1 September 2009

Karl J. Niklas1 and Ulrich Kutschera2

1Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA; 2Institute of Biology,

University of Kassel, Heinrich-Plett-Strasse 40, D-34109 Kassel, Germany

New Phytologist (2010) 185: 2741doi: 10.1111/j.1469-8137.2009.03054.x

Key words: alternation of generations,archegonia, Chara, Cooksonia,homeodomain gene networks, homology,life cycle evolution, MADS-box genes.

Summary

The extant land plants are unique among the monophyletic clade of photosyn-

thetic eukaryotes, which consists of the green algae (chlorophytes), the charophy-

cean algae (charophytes), numerous groups of unicellular algae (prasinophytes)

and the embryophytes, by possessing, firstly, a sexual life cycle characterized by an

alternation between a haploid, gametophytic and a diploid, sporophytic multicellu-

lar generation; secondly, the formation of egg cells within multicellular structures

called archegonia; and, thirdly, the retention of the zygote and diploid sporophyte

embryo within the archegonium. We review the developmental, paleobotanical

and molecular evidence indicating that: the embryophytes descended from a

charophyte-like ancestor; this common ancestor had a life cycle with only a haploid

multicellular generation; and the most ancient (c. 410 Myr old) land plants (e.g.

Cooksonia, Rhynia and Zosterophyllum) had a dimorphic life cycle (i.e. their hap-

loid and diploid generations were morphologically different). On the basis of these

findings, we suggest that the multicellular reproductive structures of extant charo-

phytes and embryophytes are developmentally homologous, and that those of the

embryophytes evolved by virtue of the co-option and re-deployment of ancient

algal homeodomain gene networks.

Contents

Summary 27

I. Introduction 28

II. Developmental constraint or a phyletic legacy? 29

III. Green plant phylogeny 29

IV. The ancestral green plant life cycle 31

V. Haplobiontic or diplobiontic life cycles? 32

VI. Pseudo-archegonia, plasmodesmata, and parenchyma 33

VII. Genomic re-deployment and embryophyte reproduction 35

VIII. Developmental homologies? 35

IX. Isomorphic or dimorphic? 36

X. Conclusions 38

Acknowledgements 39

References 39

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The Authors (2009)Journal compilation New Phytologist (2009)

New Phytologist (2010) 185: 2741 27www.newphytologist.org

I. Introduction

One of the most important biological events in the historyof life was the successful colonization of the terrestrial land-scape by green, multicellular plants and their subsequentrapid diversification during the early Paleozoic (Chaloner,1970; Graham, 1993, 1996; Niklas, 1997; Raven &Edwards, 2001; Taylor et al., 2009). This key event, whichwas unknown to Darwin (1859), paved the way for terres-trial animal evolution, altered geomorphology by accelerat-ing soil formation and modifying hydrology patterns, andthus irrevocably changed the Earths climate (Chaloner &Lawson, 1985; Willis & McElwain, 2002). Authorities

differ regarding when the land plants first appeared(Fig. 1a). Some lines of evidence indicate that microfossilassemblages of spores from the Lower Middle Ordovicianare the oldest remains of terrestrial plant life, whereas otherspoint to a SilurianEarly Devonian invasion (Gray et al.,1974; Gray, 1985; Strother et al., 1996; Beck & Strother,2001; Wellman et al., 2003), although reports of Neoprote-rozoic terrestrial soil crusts containing photosyntheticorganisms (of a cyanobacterial nature?) must be considered(see Knauth & Kennedy, 2009). What can be said withmore certainty is that the modern-day descendants of thefirst successful land plants comprise a monophyletic group,the Embryophyta (Kingdom Plantae). The living repre-

(a) (b)

Fig. 1 Reconstruction of an ancient aquaticterrestrial landscape, with the earliest multicellular land plants, adapted from a drawing of Z. Buri-an (c. 1945) (a). Comparison between the diplobiontic and haplobiontic life cycles with some representative botanical examples (embryo-phytes and two aquatic charophytes, Coleochaete and Chara, respectively) (b). In the diplobiontic life cycle, the haploid and diploid phases(gametophyte, G, and sporophyte, S, respectively) are multicellular. In the haplobiontic-haploid life cycle, only the haploid phase is multicellu-lar. The haplobiontic-diploid life cycle (in which the diploid phase exclusively expresses multicellularity, such as in our species and other animals)is not shown. n = number of chromosomes per haploid cell.

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sentatives of this taxon include the paraphyletic nonvascularplant lineages (colloquially referred to as the bryophytes)and the tracheophytes (i.e. lycophytes, ferns, horsetails andseed plants).

Numerous lines of evidence support the contention thatthe embryophytes are monophyletic and closely related tothe green algae (Kingdoms Protista and Protoctista). How-ever, the embryophytes are unique among all extant lineagesin possessing three important and interrelated reproductiveattributes. First, they possess a sexual life cycle that requiresan alternation between a multicellular haploid generation,which produces sperm and egg cells (the gametophyte), anda multicellular diploid generation, which produces meiosp-ores with sporopollenin-rich walls (the sporophyte). Sec-ond, they develop multicellular, parenchymatous structuresthat produce eggs and sperm (called archegonia and antheri-dia, respectively). Third, they retain the fertilized egg (i.e.the zygote) within the archegonium, wherein the sporo-phyte embryo is nurtured and protected (Walbot & Evans,2003). The retention of the diploid embryo within thearchegonium is the reason why the land plants are calledembryophytes and why the older literature referred tothem as the Archegoniatae (Campbell, 1905; Bower, 1908).

II. Developmental constraint or a phyleticlegacy?

Whether the archegoniate diplobiontic life cycle was essen-tial for (or merely coincidental to) the evolutionary and eco-logical success of the first multicellular land plants remainsproblematic. The retention of this life cycle may reflect adevelopmental constraint or a phyletic legacy, that is, a fea-ture that either could not be or was not lost once acquiredby the last common ancestor to all embryophytes. Alterna-tively, this life cycle may have been retained because it con-ferred functional advantages that prefigured (or wererequisite for) survival and reproductive success in an aerialand potentially desiccating habitat (Fig. 1a). Ad hoc adap-tive scenarios can be easily constructed to argue in favor ofthe latter, whereas recent insights from plant developmentalgenomics suggest that very ancient algal gene networks wereco-opted during the evolution of the embryophyte life cycleand multicellular body plan (Niklas & Kutschera, 2009).

In the light of this uncertainty, this article has two goals.The first is to review the available phycological, paleobotan-ical, developmental and molecular data that shed light onhow the archegoniate diplobiontic life cycle may haveevolved. The second is to explore how these data influencethe interpretations of developmental homologies amongembryophyte reproductive structures (i.e. antheridia, arche-gonia and sporangia). These goals dictate the structure ofthis article, which conforms to a concept map dominatedby three axes (Fig. 2). The first of these axes focuses on theenvironmental context in which early land plants evolved,

grew and reproduced. The environmental context is pivotalto tracing the evolution of any life cycle, because the mostancient embryophytes required access to liquid water forthe successful fertilization of their eggs. The second axisfocuses on the plant body plan and the transition from theunicellular to the multicellular condition. All the availableinformation indicates that the ancestral condition for eachof the major green plant lineages involved a unicellularbody plan, and that multicellularity is a derived evolution-ary condition. The third axis deals directly with the lifecycle concept. For the purposes of our review, only two lifecycles are relevant, one in which two multicellular genera-tions occur and another in which only one multicellulargeneration exists, i.e. the diplobiontic and haplobiontic lifecycles, respectively (see Fig. 1b). Because terminology, suchas diplobiontic and haplobiontic, may be unfamiliar tosome (and used in different ways by others), we provide def-initions for these and other technical words and phrases asused in the context of this article (Table 1).

III. Green plant phylogeny

Concept maps help to establish logical transformationalalternatives among critical character states (e.g. terrestrial vsaquatic, unicellular vs multicellular; haplobiontic vs diplo-biontic life cycles). However, taken in isolation, they cannotidentify the polarity of evolutionary transformations (e.g.aquatic to terrestrial vs terrestrial to aquatic). For our pur-pose, a stringent cladistic hypothesis is required, because thephylogenetic relationships among the various green plantlineages are very complex and because a well-supportedcladogram provides a framework with which to deduce the

Fig. 2 Concept map with three major themes (axes) underlying asequential exposition (steps 16) of the evolution of the land plantlife cycle. H-d, haplobiontic-diploid; H-h, haplobiontic-haploid. Theaquaticterrestrial axis is illustrated in Fig. 1a. See text for details.

NewPhytologist Tansley review Review 29



evolutionary transitions leading to the embryophyte lifecycle. In this section, we review the phylogenetic relation-ships among the green plant lineages as a prelude to map-ping life cycle evolutionary transformations. All currentpalaeobotanical, cytological, physiological and moleculardata indicate that the green algae (i.e. the Chlorophyta sensuSmith, 1950) and the Embryophyta share a last commonancestor (Mattox & Stewart, 1984; Mishler & Churchill,1985; McCourt, 1995; Karol et al., 2001; Scherp et al.,2001; Lewis & McCourt, 2004; Archibald, 2009), whichwas a unicellular flagellate that evolved as a result of ancientendosymbiotic events involving a prokaryotic host cell anda cyanobacterial-like photoautotroph (Bhattacharya &Medlin, 1995; Kutschera & Niklas, 2004, 2005, 2008)(Fig. 3). Numerous lines of evidence further show that theembryophytes descended from a last common ancestorshared with the Coleocheatophyceae, Charophyceae andpossibly other lineages (such as the Zygnemophyceae and

Klebsormidiophyceae), which collectively comprise thegreen algae colloquially called the charophytes (Karolet al., 2001; McCourt et al., 2004). Taken in isolation, theColeocheatophyceaeCharophyceae lineage is relativelysmall in terms of species numbers and includes species withunicellular and multicellular body plans, some of which areadapted to, or at least capable of tolerating, some desicca-tion (Fig. 3).

The evidence for the monophyly of the charophyteembryophyte lineage (collectively referred to as the strepto-phytes) is extensive. In addition to producing cell wallscontaining cellulose, chloroplasts with stacked grana andchlorophylls a and b, bi- or multiflagellated cells (whenmotile cells are present) and starch as their primary photo-synthate, the charophytes and embryophytes also share fea-tures not found in any other green algae, such as, forexample, several enzyme systems (e.g. glycolate oxidase),motor organelles with asymmetrically inserted flagella,

Table 1 Definitions of key words and phrases used in the context of this article

Antheridium The multicellular, sperm-producing structure of the embryophytes, consisting of a sterile jacketof cells surrounding spermatogenous cells

Archegonium The multicellular, egg-producing structure of the embryophytes, consisting of a neck,neck canal cells and a venter surrounding the egg

Body plan The phenotypic architecture that distinguishes one group of organisms from another;the processes that obtain an organisms organized growth and development

Dimorphic The presence of substantive phenotypic differences between the haploid and diploid phases(generations) in the life cycle of an organism; in phycology, heteromorphic(i.e. morphologically different haploid and diploid generations)

Diplobiontic A life cycle that involves the alternation of two multicellular phases(one haploid and another diploid) to complete sexual reproduction; also known as thealternations of generations and as the diplohaplontic life cycle, e.g. mosses and ferns

Gametangia Multicellular gamete-producing structures, e.g. antheridia, archegonia, globules and nuculesGametophyte The multicellular haploid phase in a plant life cycle that produces gametes (sperm or eggs, or both)Globule Sperm-producing multicellular organ of charalean algaeHaplobiontic A life cycle involving only one multicellular generationHaplobiontic-diploid A haplobiontic life cycle in which the only multicellular generation is diploid,

e.g. Homo sapiens and other vertebratesHaplobiontic-haploid A haplobiontic life cycle in which the only multicellular generation is haploid;

one in which the only diploid phase is the zygote; in phycology, equivalent tohaplontic, e.g. charophycean algae

Homologous One or more traits characterizing two or more phyletically related taxa that emerge asa result of shared highly conserved ancestral structures, genetic networks or mechanism(s)

Isomorphic The absence of substantive phenotypic differences between the haploid and diploid phases(generations) in the life cycle of an organism

Nucule Egg-producing multicellular structure of charalean algaeOogonium In phycology, a cell specialized to function as an eggParenchyma A tissue composed of not distinctly specialized and generally uniformly appearing living

cells with thin primary cell wallsParenchymatous tissue construction A tissue in which cells have the capacity to divide in any plain with respect to the principal

body axis and in which primary or secondary plasmodesmata develop at the majority of cellwalls shared among neighboring cells

Plasmodesmata Microscopic channels traversing the cell walls of embryophytes and some algae that enableintercellular symplastic transport and communication

Sporophyte The multicellular diploid phase in a plant life cycle that produces sporesStreptophytes An informal taxonomic term referring to the charophyteembryophyte lineageZygotic meiosis Meiosis occurring after the fertilization of the egg without any intervening mitotic cell divisions.

In multicellular algae, zygotic meiosis obtains a haplobiontic-haploid life cycle




dissimilar flagella roots with a multilayered structure, persis-tent mitotic spindles, open mitosis and phragmoplasts(Mattox & Stewart, 1984; Graham, 1993; McCourt, 1995;Graham & Wilcox, 2000; Karol et al., 2001; Scherp et al.,2001; McCourt et al., 2004).

Nevertheless, although all green plants are monophyletic,the most recent phylogenies consistently identify a deepgenomic dichotomy between the streptophytes and threecladistically well-supported lineages (i.e. the Chlorophyceae,Trebouxiophyceae and Ulvophyceae), which are collectivelyreferred to as the chlorophytes. Like the charophytes, thechlorophytes are ecologically diverse and include specieswith unicellular and multicellular body plans, some ofwhich can survive in subaerial or emergent habitats (Fig. 3).

The deep streptophytechlorophyte divide is occupiedby an assortment of lineages represented by unicellularspecies, collectively called prasinophytes (Fig. 3), whosephylogenetic relationships remain problematic (Sym &Pienaar, 1993; Lewis & McCourt, 2004). Although theexistence of six or seven prasinophyte lineages is sup-ported by molecular data (e.g. Zignone et al., 2002),these algae are best viewed as a grade of cellular organiza-tion emerging from the base of the green plant clade. Assuch, they have the potential to shed light on the featurescharacterizing the last common flagellate ancestor to theentire green plant tree of life.

IV. The ancestral green plant life cycle

The precise phylogenetic relationships among the prasin-ophytes, chlorophytes and streptophytes will undoubtedly

be modified as more taxa are examined and more dataare incorporated into cladistic analyses. However, givencurrent information, three conclusions can be drawn: thegreen plants are monophyletic; the phyletic dichotomyseparating the chlorophytes and the streptophytes is occ-upied by prasinophytes; and the streptophytes des-cended from a unicellular freshwater alga. Here, wereview data that support two additional conclusions: theancestral life cycle in all of the major green algal lineagesinvolved zygotic meiosis and was thus haplobiontic (Fig.1b); and the derived green plant diplobiontic life cycleevolved at least twice, once among the chlorophytes(Ulvophyceae) and again among the streptophytes (charo-phytes and embryophytes).

These assertions are based on two lines of evidence. First,among extant unicellular and multicellular green algae (i.e.prasinophytes, chlorophytes and charophytes) for whichsexual reproduction has been documented, most have a lifecycle in which the only diploid cell is the zygote (Smith,1950; Bold & Wynne, 1978; Graham & Wilcox, 2000;Lee, 2008). Second, although sexual reproduction has beendocumented for very few species in the basal prasinophytelineages, those that have been corroborated involve zygoticmeiosis (e.g. Nephroselmis olivacea; Suda et al., 1989)(Fig. 4a). Thus, for the majority of green algae, the adultor mature organism in the sexual life cycle is haploid andfunctions reproductively as the gametophyte generation inthe embryophyte life cycle (Graham & Wilcox, 2000; Nik-las & Kutschera, 2009).

As noted, plant life cycles involving only one multicellu-lar individual are called haplobiontic (in contrast with

Fig. 3 Phylogenetic relationships among themajor green plant lineages based on an anal-ysis of DNA sequence data. Dichotomousbranches shown as broken lines indicateweakly supported portions of the tree. Thephyletic position of the Mesostigmato-phyceae is particularly problematic (denotedby ?). The distributions of different habitatpreferences, body plans and life cycles areindicated by symbols (see lower box).Adapted from Lewis & McCourt (2004).




diplobiontic life cycles with two multicellular individuals;Fig. 1b). Two variants of the haplobiontic life cycle are pos-sible. One in which the multicellular generation is diploid(the haplobiontic-diploid life cycle; Hd) and one in whichthe haploid generation is exclusively multicellular (haplobi-ontic-haploid; Hd) (see Fig. 2, node 4). Therefore, lifecycles involving zygotic meiosis are classified as haplobion-tic-haploid (Table 1). Clearly, no multicellular generationexists in the case of unicellular algae. The sexually matureindividual functions either indirectly or directly (i.e. with orwithout intervening mitotic cell divisions) as the adultorganism and as a gamete. Therefore, the haplobiontic vsdiplobiontic terminology is largely irrelevant. Nevertheless,the life cycles of unicellular algae, such as Nephroselmis oliv-acea, and multicellular algae, such as Monostroma grevillei,are fundamentally the same (Fig. 4a,b, respectively). Bothare defined by zygotic meiosis. The only fundamentaldistinction that conceptually separates the two life cycles

is whether (and where) multicellularity is developmentallyexpressed.

In contrast with the broad phyletic distribution of ha-plobiontic-haploid life cycles, diplobiontic life cycles occurin only one green algal lineage the Ulvophyceae (Fig. 3).Three of the six orders within this class are reported tocontain species with diplobiontic life cycles (i.e. the Clad-opherales, Trentepohliales and Ulvales; see Graham &Wilcox, 2000; Lewis & McCourt, 2004; Lee, 2008 andreferences therein). Among these species, some diplobion-tic life cycles are isomorphic (e.g. Ulva), whereas othersare dimorphic (e.g. Derbesia). However, even among thevarious Ulvophyceae, the diplobiontic life cycle appears tobe an evolutionarily derived condition, because moleculardata suggest that the Ulotrichales are basal in the Ulvophy-ceae (OKelly et al., 2004), and because ulotrichalean algaehave haplobiontic-haploid life cycles, e.g. Ulothrix andMonostroma (Fig. 4b). The haplobiontic-haploid life cycleis also well represented among the acellular (siphonous)ulvophycean marine algae. These lines of evidence indicatethat the diplobiontic life cycles of the Embryophyta andUlvophyceae are the result of convergent evolution (seeFig. 3).

V. Haplobiontic or diplobiontic life cycles?

Was the last common ancestor to the Charophyceae andEmbryophyta unicellular or multicellular? This question isimportant because its answer provides an insight into theevolution of the embryophyte life cycle. Consider that, ifthe last common ancestor were unicellular, the capacity formulticellularity could have evolved in either the haploid ordiploid generation, or both simultaneously (Fig. 5a,b) apossibility that opens the door to many conceivable lifecycle variants as the ancestral condition. Alternatively, if thelast common ancestor were multicellular and had a life cycleinvolving delayed zygotic meiosis, the diploid generation inthe embryophyte life cycle (i.e. the sporophyte) would be anevolutionary innovation.

The phyletic distribution of unicellular species at the baseof the streptophyte lineage highlights the problematic nat-ure of the answer to this question, as illustrated by the cla-distic position of the monotypic Mesostigmatophyceae(Fig. 3). Mesostigma vivida is an asymmetrical cell that wasoriginally classified as a charophyte on the basis of its flagel-lar ultrastructure (Melkonian, 1989). Subsequent molecularanalyses of 18S rRNA sequences indicated that the genuswas closely related to Chaetosphaeridum, which led to theestablishment of a new class, the Mesostigmatophyceae(Marin & Melkonian, 1999). However, Delwiche et al.(2002) demonstrated that Chaetosphaeridum is a charophyteand, on the basis of rbcl sequences, concluded that Mesostig-ma is a sister taxon to the streptophytes. Subsequently, Yo-shii et al. (2003) argued that Mesostigma represents an early

(a)

(b)

Fig. 4 Diagrammatic comparison of the life cycles of the prasino-phyte Nephroselmis olivacea (adapted from Suda et al., 1989) (a)and the ulotrichean alga Monostroma grevillei (adapted fromGraham & Wilcox, 2000) (b).




evolutionary lineage and placed the Mesostigmatophyceaeamong the prasinophytes (Fig. 3).

The phylogenetic position of Mesostigma remains conten-tious (see Lewis & McCourt, 2004). However, its phyleticposition at the base of the chlorophytestreptophytedivide, in tandem with the antiquity of lineages containingnumerous semi-aquatic and terrestrial unicellular species(i.e. Chlorokybophyceae, Klebsormidiophyceae and Zy-nemophyceae), suggests that a variety of life cycles may haveevolved (and disappeared) over the early course of charo-phycean evolution (see Fig. 3). Indeed, one intriguing lineof speculation is the prospect that important life cycle evolu-tionary innovations occurred among unicellular or filamen-tous charophytes serving as phycobionts in ancient lichen-like organisms. Currently, no lichen is known to contain acharophycean phycobiont (Friedl & Bhattacharya, 2006).However, it is possible that the ancient co-evolutionary his-tory of the land plants and mycorrhiza was prefigured by amutually beneficial relationship between ancient charo-phytes and fungi that can be broadly thought of as lichen-like symbiotic organisms (McCourt et al., 2004).

Although the nature of the most ancient land plant lifecycle cannot be asserted currently, the available evidenceindicates that the ancestor to the streptophytes was multi-

cellular and possessed a haplobiontic-haploid life cyclesimilar to that of Coleochaete and Chara. If this suppositionis true, the land plant sporophyte generation was an evolu-tionary innovation resulting from delayed zygotic meiosisand the intercalation of one or more mitotic cellular divi-sions. Put differently, the first embryophyte sporophyte wasa multicellular zygote. Whether this life cycle first appearedin an aquatic, semi-aerial or aerial environment is conjec-tural. Although the transition from a haplobiontic-haploidto a diplobiontic life cycle may have come at a cost withregard to the growth of the haploid generation (as indicatedby studies on mosses; see Ehrlen et al., 2000; Rydgren &kland, 2002), the diplobiontic life cycle confers adaptivebenefits across a broad range of habitats and environmentalconditions (e.g. the numerical amplification of zoospores ormeiospores resulting from possibly rare fertilization events,and the possibility to occupy two different niches in thesame general environment), as attested by the reproductiveand ecological success of ulvophycean algae and embryo-phytes with free-living gametophytes.

Nevertheless, if the evolutionary transformation from ahaplobiontic-haploid to a diplobiontic life cycle occurred ina fresh water or terrestrial habitat, which is almost a cer-tainty, the first sporophytes would hardly qualify as landplants, as they would have grown on maternal gametophytesattached, in turn, to a hydrated substrate, and thus are moreproperly thought of as air plants (see Fig. 1a).

VI. Pseudo-archegonia, plasmodesmata andparenchyma

Whether the first charophycean algae to evolve a diplobion-tic life cycle were archegoniates is another challenging andunresolved question. The fossil record of the earliest landplants is especially sparse and problematic, and there isnothing in the diplobiontic life cycle concept that stipulatesthe manner in which sperm or eggs are produced (Wellmanet al., 2003). In addition, as noted earlier, the diplobionticlife cycle is not unique to the embryophytes (see Fig. 3).However, it is very likely that the last common ancestor tothe streptophytes had reproductive structures that func-tioned in some, if not many, ways like the antheridia andarchegonia of embryophytes, such as Equisetum (Lycopodia-cae), a seedless land plant (Fig. 6a,b).

This assertion rests on three observations. The zygotes ofmany, albeit not all, species in the Coleochaetophyceae andall species in the Charophyceae are retained by the gameto-phyte, during which many species nourish and protect themfor short, albeit developmentally substantive, periods oftime; and the most evolutionarily derived charophyceanspecies, such as stoneworts of the genus Chara, have multi-cellular and morphologically complex gametangia (Fig.6c,d). In the case of Coleochaete (see Fig. 1b), sterilefilaments develop around the oogonium after fertilization.

(b)

(a)

Fig. 5 Diagrammatic rendering of the hypothetical transformationof an ancient prasinophyte life cycle (a) (depicted as that of Nephro-selmis olivacea; see Fig. 4a) into a diplobiontic life cycle (b). Delayedzygotic meiosis and the intercalation of mitotic divisions results in amulticellular sporophyte and mitotic divisions of meiospores beforeplasmogamy results in a multicellular gametophyte.




In the case of charalean species, sterile cells envelop theoogonium before fertilization. Indeed, the sperm-producingorgan of Chara (the globule) is functionally (and develop-mentally) similar in many ways to the antheridium, whereasthe egg-producing structure (the nucule) can be called apseudo-archegonium on the basis of its capacity to protectand provide the egg and zygote with nourishment for a notinconsiderable time (Fig. 6c,d).

Another physiologically important feature shared by thecharophytes and embryophytes is the capacity to form plas-modesmata (Graham, 1982), which has evolved indepen-dently many times in different algal lineages and inde-pendently within the Chlorophyceae and again in theCharophyceae (Raven, 1997). Among the streptophytes, theability to form these symplastic connections among adjoin-ing cells is restricted to the Coleochaetophyceae (specificallyColeochaete, see Fig. 1b), Charophyceae (Fig. 6c,d) and theEmbryophyta (Brown et al., 1994; Cook et al., 1998). Theability to form plasmodesmata permits active polar transportof large molecular weight solutes across adjoining cell walls,

which facilitates the targeting and nutrition of specializedcells (see Jansen, 2001; Lucas et al., 2001). It can also play apivotal role in the physiological control of embryogenesis.More detailed studies are required to determine whether cha-rophycean plasmodesmata are typically primary or secondaryin nature. The former develop during cytokinesis and cellwall deposition; the latter develop after cytokinesis and mayappear after secondary wall deposition. Whether primaryor secondary plasmodesmata form during or after histo-genesis is important, because it helps to resolve whetherthe tissues in which plasmodesmata develop are truly par-enchymatous, and because primary and (complex) second-ary plasmodesmata have different protein-trafficking func-tions, which can influence organogenesis (e.g. Itaya et al.,1998). Regardless of these subtleties, primary plasmo-desmata have been demonstrated for at least one species ofChara (Brown et al., 1994; Cook et al., 1998), andultrastructural studies suggest that the nodal regions ofChara have a parenchymatous tissue structure (Pickett-Heaps, 1975; Cook et al., 1998).

(a) (b)

(c) (d)

Fig. 6 Comparisons among the antheridiumand archegonium of the vascular land plantEquisetum (a and b, respectively) and thereproductive organs (nucule and globule,with gamete-producing tissues) of the Chara-lean alga Chara (c and d, respectively). c,coronal cells; e, egg; g, globule; n, neck cells;nu, nucule; o, oogonium sc, spermatogenouscells; sj, sterile jacket cells; spc, sperm cells; v,venter.




VII. Genomic re-deployment and embryophytereproduction

The ability to form plasmodesmata and parenchyma is nota requisite for the formation of morphologically complexmulticellular structures, such as the gametangia of Chara(Fig. 6c,d). The nucule and globule of Chara and othercharalean algae are composed of branched filaments, whichonly give the appearance of having a parenchymatous tissueconstruction. However, the ability to form parenchyma andplasmodesmata is an important attribute of the embryo-phytes, because it establishes complex and physiologicallyintegrated symplastic interconnections via primary and sec-ondary plasmodesmata formation that are required for spo-rophyte embryogenesis and development.

Indeed, recent studies of homeodomain-containing tran-scription factor genes suggest that an intriguing genomicredeployment strategy has attended the evolution of thearchegoniate diplobiontic life cycle. For example, amongthe best known of these genes is the MADS-box gene fam-ily, which has been extensively studied in the floweringmodel organism Arabidopsis thaliana. This gene family isdivided into two subfamilies, referred to as type I and typeII. There are 45 type II genes, which are also referred to asMIKC factors (for MADS DNA-binding domain, interven-ing domain, keratin-like domain and C-terminal domain);the type II group can be further subdivided into MIKCC

and MIKC* genes on the basis of the inferred evolutionaryhistory of the family. MIKC* proteins tend to have longer Idomains and less-conserved K domains than do the MIKCC

proteins. Sequences encoding MIKCC and MIKC* factorshave been identified in bryophytes and lycopods, as well asin gymnosperms and angiosperms, which suggests that theMIKC* and MIKCC genes have evolved independently forat least 450 Myr. The expression of MIKC-type genes inangiosperms occurs only after the specification of thevegetative to inflorescence meristem transition, which ismediated by the transcription factor encoded by FLORICA-ULA LEAFY (FLO LFY). In ferns, FLO LFY homologs areexpressed predominantly in sporogenous meristematictissues, but MADS-box gene expression is not closely corre-lated, suggesting that these genes have not yet been subordi-nated to FLO LFY regulation. In the moss Physcomitrella,two FLO LFY paralogs (PpLFY-1 and PpLFY-2) arerequired for the first division of the zygote and early sporo-phyte embryogenesis (Henschel et al., 2002; Tanahashiet al., 2005), whereas MADS-box gene expression occursduring Chara globularis gametangium differentiation anddeclines after fertilization (Tanabe et al., 2005).

It is therefore reasonable to suggest that MADS-boxgenes originally functioned in the differentiation of haploidreproductive structures (e.g. the nucule and moss archego-nium) and were subsequently redeployed to function in theformation of sporophyte reproductive structures (e.g. the

fern sporangium). Such combinatorial homeodomain-basedtranscriptional control of reproduction may have extremelydeep phylogenetic roots. Ectopic expression of the homeo-proteins Gsp1 and Gsm1 in the plus and minus strains ofthe unicellular chlorophyte Chlamydomonas activates vege-tative haploid cells to form zygote-like structures (Lee et al.,2008). Likewise, Gsp1 and Gsp2 are members of the TALE(three amino acid loop extension) homeodomain-contain-ing transcription factors, which include the class 1 KNOXand class 2 KNOX proteins. Homeodomain gene networks,similar to those in land plants, have been reported for pra-sinophytes (e.g. Micromonas), which are postulated to revealthe attributes of the last common ancestor of all greenplants (Worden et al., 2009) (see Fig. 3).

VIII. Developmental homologies?

The recruitment and redeployment of homeodomain genenetworks underlying much of the evolution of strepto-phyte reproduction may help to explain why charaleangametangia and embryophyte antheridia, archegonia andsporangia share the same fundamental developmental cho-reography (Fig. 7).

Perhaps the most obvious shared attribute of these multi-cellular structures is that each develops from a single super-ficial meristematic initial. In the case of charalean globuleand nucule, this initial is a nodal cell (Fig. 7a); in the caseof embryophytes, it is typically an epidermal cell (Fig. 7b).Charalean antheridium induction involves an unequal divi-sion of the nodal initial cell. The smaller of the two deriva-tives develops into a stalk; the larger, apical cell undergoes aseries of cellular divisions that eventually produce externalshield cells that surround stalks and branched structures(manubria) from which sperm filaments radiate (Pickett-Heaps, 1975). The development of the charalean nuculealso begins from a single nodal cell that undergoes unequalcell divisions to form a basal stalk and the tube cells thatgyrate around a centrally located oogonium (Pickett-Heaps,1975). In much the same way, sporangial inductioninvolves periclinal division of one or more epidermal cells.Among eusporangiate species, the innermost derivativesgive rise to sporogenous cells, whereas the outermostdevelop into the sporangium wall (Fig. 7b). Embryophytegametangia (antheridia and archegonia) development alsobegins when a single epidermal cell undergoes a periclinaldivision. The innermost cells resulting from this divisiondevelop into spermatogenous cells, or the neck canal andegg cells (for details, see Campbell, 1905; Bower, 1908;Gifford & Foster, 1989).

Numerous differences exist in the development of eu-and leptosporangia and in the development of antheridiaand archegonia. For example, the sporogenous cell initialsin the eusporangium develop from the innermost periclinalderivatives of the superficial sporangial initials, whereas the




sporogenous cells of the leptosporangium trace their devel-opmental origins to outer periclinal derivative cells. Like-wise, charalean and embryophyte development differ inmany ways. For example, the charalean oogonium occupiesan apical (albeit enveloped) position, whereas the embryo-phyte egg cell develops from a hypodermal derivative.Likewise, the nucule and globule have a pseudo-parench-ymatous (filamentous) tissue construction, whereas sporan-gia, antheridia and archegonia are parenchymatous (Gifford& Foster, 1989; Graham & Wilcox, 2000).

Nevertheless, we suggest that there is sufficient develop-mental and molecular evidence to conclude that theembryophyte sporangium is homologous to the antherid-ium archegonium as a result of homeodomain gene net-work recruitment from the gametophyte generation andredeployment in the sporophyte generation. In this context,we use the concept of homology sensu Shubin et al. (1997),namely a correspondence in growth and differentiationresulting from highly conserved and deeply ancestral geneticmechanisms. Likewise, we believe that archegonia and an-theridia are developmentally homologous to charalean gam-etangia, i.e. embryophyte gametangia are homologous tothe nucule and globule (Fig. 7). This perspective is consis-tent with current knowledge of the molecular developmen-tal biology of streptophyte reproductive structures. It is alsoconsistent with the evolution of the embryophyte diplo-

biontic life cycle from the haplobiontic-haploid life cycle ofa charalean common ancestor. The alternative assertion thatembryophyte sporangia are homologous to leaves is far lesstenable (Kenrick & Crane, 1997a,b).

IX. Isomorphic or dimorphic?

We have argued that the ancient aquatic ancestor to allgreen eukaryotes (Kingdoms Protoctista and Plantae) was asingle-celled flagellate (Fig. 3) with a life cycle that alter-nated between a haploid generation that functioned as theadult + gamete and a more or less ephemeral single-celledzygote (Fig. 1b). The traditional botanical view precludesassigning such an organism a diplobiontic or a haplobionticlife cycle, because multicellularity is not expressed in this lifecycle. Nevertheless, this kind of organism has an alterna-tion of generations, albeit unicellular ones. Accordingly,any consideration of the life cycle of the earliest Urform(prototype) of all land plants necessarily begins by askingwhether the immediate ancestor to the streptophytes wasunicellular in both phases of its life cycle (as was its aquaticprecursor), or whether one or both of its life cycle phaseswas multicellular. This consideration is cast in botanical tra-dition by asking whether the life cycle was isomorphic (bothlife forms are the same) or dimorphic (two different lifeforms) (see Fig. 2, node 5; Table 1).

(b)

(a)

Fig. 7 Comparisons among the developmentof charalean gametangia (a) and the repro-ductive structures of embryophytes (b). Thecharalean globule and nucule each developfrom a single superficial nodal cell initial (a).The embryophyte eusporangium, antherid-ium and archegonium typically develop froman epidermal cell initial (b). Tissues directlyinvolved with reproduction (e.g. sperm, eggand sporogenous cells) are shaded.




There are obvious advantages to multicellularity for anorganism living in a subaerial environment, e.g. protectionagainst UV exposure and dehydration (Niklas, 1997;Raven, 1999, 2002). However, the most ancient green landplants may have inhabited the soil or evolved from a lichen-like organism, and thus may have been protected by mois-ture-laden boundary layers (Stebbins & Hill, 1980; Readet al., 2000). What is clear is that, over many generations,the land plants became multicellular, and we necessarilyneed to know whether this innovation occurred simulta-neously in both the gametophyte and sporophyte genera-tion, or whether one generation acquired multicellularitywhilst the other generation subsequently acquired this bodyplan.

On the basis of the distribution of life cycles amongextant green plants (Fig. 3), it is logical to argue that theseries of life phase transformations achieving multicellulari-ty began with the gametophyte generation, and that thezygotes of the ancestors of the first green land plants werepreprimed for meiosis. If true, the vegetative phase of thegametophyte generation is the primal (ancestral) and arche-typical home for land plant gene expression and gene net-work interactions, as well as the effects of heritablemutations on morphogenesis. Nevertheless, the alternativepossibility that multicellularity arose first in the diploid,sporophytic phase cannot be excluded, especially from agenetic perspective, as a single mitotic division before mei-otic cell division generates eight (not four) potentiallyrecombinant genotypes from each zygote (with consequentselective advantages), in contrast with a mitotic divisionafter meiosis, which generates two (not one) spore recombi-nant genotypes (with consequent effects on the stochasticloss of a desirable combination of genes).

Another conceptually important, but as yet unresolved,question is whether the most ancient embryophytes pos-sessed an isomorphic or a dimorphic life cycle (Fig. 2,nodes 5 and 6). Kenrick & Crane (1997a,b) and Steemanset al. (2009) have argued that the isomorphic alternation ofgenerations is the most ancient, in part based on three-dimensionally preserved gametophytes in the c. 410 Myrold Rhynie Chert (see Kerp et al., 2004; Taylor et al.,2005; Niklas & Kutschera, 2009). As discussed in the previ-ous section, the gametophytes and sporophytes of the mostancient embryophytes undoubtedly shared similar genomicand developmental repertories, just as they shared genomicsimilarities with their charalean common ancestor. Thus, inthe absence of phenomenologies, such as gene silencing, sexchromosomes or epigenetic effects, differences in ploidymay not have equated to significant gametophytesporo-phyte morphological differences. This perspective isstrengthened in the light of some modern-day mosses andferns, which can generate sporophyte morphologies directlyfrom their gametophytic cells (apogamy) and gametophytemorphologies directly from their sporophyte cells (apo-

spory). Apogamy and apospory show that the haploid anddiploid genomes contain much of the information requiredto construct both the gametophyte and the sporophyte bodyplans (Niklas & Kutschera, 2009).

A focus on apogamy rather than apospory is justified inthe context of our review, because the thesis developed thusfar is that the sporophyte generation evolved during thetransition from a charalean-like haplobiontic-haploid lifecycle to an embryophyte diplobiontic life cycle. Amongextant species, apogamy can be induced by cell trauma, lowlight intensities, suitable concentrations of sugar or auxin. Itcan also be induced by the deletion of the CURLY LEAF or-tholog in the moss Physcomitrella (PpCLF). Okano et al.(2009) have reported that gametophytic cells that usuallyform protonema or gametophore apical cells generate meri-stematic apical cells that form branched morphologies,which can be induced to form sporangium-like structureswith the exogenous application of PpCLF. The resultingmorphologies have been reported to be similar to veryancient tracheophytes, such as Zosterophyllum or Cooksonia(Figs 8 and 9).

These findings suggest that PpCLF regulatory gene net-works may have participated in the early evolution of theembryophyte sporophyte (Okano et al., 2009). Spontane-ous mutation of the CURLY LEAF ortholog attending fer-tilization and zygote formation among ancient strepto-phytes may have participated in delayed zygotic meiosis,and thus the formation of a multicellular diploid phase. It isnevertheless doubtful that the mutation of any single genewas sufficient for this important evolutionary transition.Likewise, it is uncertain whether the sporophyte generationevolved as a consequence of delayed zygotic meiosis orprecocious zygotic mitosis. Molecular analyses of angiospermmega- and microsporogenesis and mega- and microgameto-genesis indicate that numerous complex gene networks areinvolved in the initiation or suppression of meiosis. Forexample, the male sterile multiple archesporial cell (mac1)mutant in maize (Zea mays), which leads to the productionof extra diploid sporocytes in ovules and anthers, appears tocontribute to the restriction of the identity of cells compe-tent for meiotic division (see Sheridan et al., 1996; Walbot& Evans, 2003), whereas the Meiosis Arrested at Leptotene1(MEL1) gene in rice (Oryza sativa) is required for spo-rocycte meiosis (Nonomura et al., 2007). More data fromtaxa deeper within the streptophyte lineage are required toshed meaningful light on the gene networks that participatein early sporophyte embryogenesis.

Returning to the antiquity of the isomorphic vs diplobi-ontic life cycle, a number of lines of evidence indicate thatthe most ancient embryophyte life cycles were dimorphic.First, extant monoploid embryophytes do not developapogamous sporophytes, suggesting that gene duplicationand subsequent functional divergence presaged the evolu-tion of multicellular sporophytes, which is consistent with




the extensive analysis of the Physcomitrella patens genome(Rensing et al., 2008). Second, embryophyte sporophytesand gametophytes normally develop in very different physi-ological and mechanical environments. Young sporophytesdevelop within archegonia; free-living embryophyte ga-metophytes develop from dispersed meiospores. Third,numerous environmental factors influence early morpho-genesis that fosters dimorphism (Sinnott, 1960). Fourth, ifthe most ancient sporophytes were an intercalated multi-cellular generation, it is difficult to imagine that they weremorphologically elaborate indeed, they may have beennothing more than the functional equivalent of a sporan-gium (Niklas, 1997). Fifth, the different functional obliga-tions of the gametophyte and sporophyte generations wouldhave sustained and even amplified their ancestral di-

morphism. Sixth, the purported life cycles of RhynieChert plants (dated to 410 Myr), such as Rhynia, are notisomorphic (Kerp et al., 2004; Taylor et al., 2005; Niklas& Kutschera, 2009). Seventh, there is some evidence(albeit, at this point, very problematic) that more ancienttracheophytes, such as Zosterophyllum and Cooksonia(Figs. 8,9), may have had dimorphic life cycles (Probst,1986; Niklas & Banks, 1990; Remy et al., 1993; Gerrienneet al., 2006).

X. Conclusions

Many details regarding the phylogeny of the green plantlineages (chlorophytes and streptophytes) remain unre-solved and will require more data from more taxa, part-

(a) (b)

Fig. 8 (a) Upper part of a mature sporophyte(sporangium, indicated by an arrowhead) ofZosterophyllum rhenanum, an Early Devo-nian (c. 410 Myr old) vascular land plant. Afossilized spore is shown in the inset. (b)Reconstruction of the phenotype of a clusterof plants (adapted from Edwards, 1969; andProbst, 1986).

(a) (b)

Fig. 9 Purported sporophyte (sporangia indi-cated by arrowheads) attached to its game-tophyte (see arrow and shaded region ininset) of Cooksonia paranensis, an EarlyDevonian (c. 415 Myr old) vascular landplant (a) and reconstruction of the pheno-type (b). No vascular tissues or spores wererecovered from this fossil. Although sporeshave been isolated from similar structures onother fossils assigned to the same species, itremains possible that the entire fossil is agametophyte (adapted from Gerrienne et al.,2006).




icularly from those residing at the base of this ecologicallyrich clade. The broad phylogeny of the green plants isnevertheless sufficiently well resolved to permit a reason-ably stringent phyletic scaffold upon which to trace thecharacter transformations attending the evolution of theembryophyte diplobiontic life cycle. Using this approach,two conclusions emerge that will probably stand the testof future scrutiny. First, the ancestral organism for theentire green plant clade (and for the lineage leading to thecharophytes) was a flagellated eukaryotic photoautotroph(Fig. 3), and, second, the ancestral organism to the strep-tophytes (Coleochaetophyceae, Charophyceae, and Embry-ophyta) was a multicellular alga that had a haplobiontic-haploid life cycle and morphologically complex gametan-gia reminiscent of those of Chara (Fig. 6c,d). With far lesscertainty, we surmise that the earliest land plants(Figs 1a,8,9) had a dimorphic diplobiontic life cycle inwhich the haploid (gametophytic) phase dominated. Sub-sequent evolutionary divergence led to land plant formsthat retained this ancestral condition (represented today bythe extant bryophytes) and lineages in which the diploidgeneration became dominant (represented by all extant tra-cheophytes, notably the seed plants, Fig. 1b). Althoughspeculative, we further suggest that there is sufficientobservational and molecular data to indicate that thereproductive organs of embryophytes (i.e. archegonia, an-theridia, and eusporangia) are homologous structures(sensu Shubin et al., 1997) that, in turn are homologouswith the multicellular gametangia of the charalean algae(the nucule and globule) (Fig. 7). These homologiesappear to be the result of the co-option and re-deploymentof ancient algal gene networks.

Much speculation surrounds the properties of genes,gene networks, and even entire organisms that favor piv-otal evolutionary transformations that nevertheless con-serve structural and genomic homologies. Although theevidence is sparse, speculation favors the effects of regula-tory genes, in general, and transcription factors, in particu-lar, as the most probable drivers of evolutionaryinnovation (see Doebley & Lukens, 1998; Cronk, 2001).However, the few detailed studies of plant developmentalgene interactions are insufficient to justify this view to theexclusion of other potentially equally important mecha-nisms, as witnessed by the recent finding that the develop-mental patterning of the highly reduced angiosperm mega-gametophyte depends on an asymmetric, location-specificgradient of auxin synthesis (Pagnussat et al., 2009). Forthis reason, we conclude that future enquiries into thedevelopmental mechanism(s) by which the embryophytelife cycle evolved would profit from detailed diagnoses ofthe molecular drivers of the plant cell cycle, the inductionof meiotic versus mitotic cell division, and a host of otherfundamental phenomena. Scrutiny of meiotic gene candi-dates and factors that contribute to homologous chro-

mosome pairing will be a particularly important and fertilefield of inquiry (see Able et al., 2009).

Acknowledgements

We thank Dr. P. Gerienne for providing Fig. 9a and Dr. J.Raven (the University of Dundee, UK) for many useful sug-gestions. We also thank the College of Agriculture and LifeSciences (Cornell University, Ithaca, USA) and the Alexan-der-von Humboldt-Foundation (AvH, Bonn, Germany) forfinancial support (AvH-fellowship 2009, Stanford Califor-nia, USA to U. Kutschera).

References

Able JA, Crismani W, Boden SA. 2009. Understanding meiosis and the

implications for crop improvement. Functional Plant Biology 36: 575588.

Archibald JM. 2009. Green evolution, green revolution. Science 324: 191192.

Beck JH, Strother PK. 2001. Silurian spores and cryptospores from the

Arisaig group, Nova Scotia, Canada. Palynology 25: 127177.Bhattacharya D, Medlin L. 1995. The phylogeny of plastids: a review

based on comparisons of small-subunit ribosomal RNA coding regions.

Journal of Phycology 31: 489498.Bold HC, Wynne MJ. 1978. Introduction to the algae: structure and repro-

duction. Englewood Cliffs, NJ, USA: Prentice-Hall.Bower FO. 1908. The origin of a land flora. London, UK: Macmillan.Brown RC, Lemmon BE, Graham LE. 1994. Morphogenetic plastid

migration and microtubule arrays in mitosis and cytokinesis in the

green alga Coleochaete orbicularis. American Journal of Botany 8: 127133.

Campbell DH. 1905. The structure and development of mosses and ferns (Ar-chegoniatae). London, UK: Macmillan.

Chaloner WG. 1970. The rise of the first land plants. Biological Reviews45: 353377.

Chaloner WG, Lawson JD. (eds) 1985. Evolution and environment in thelate Silurian and early Devonian. London, UK: The Royal Society ofLondon.

Cook ME, Graham LE, Botha CEJ, Lavin CA. 1998. Comparative ultra-

structure of Chara and selected bryophytes: toward an elucidation of theevolutionary origin of plant plasmodesmata. American Journal of Botany84: 11691178.

Cronk QCB. 2001. Plant evolution and development in a post-genomic

context. Nature Reviews Genetics 2: 607617.Darwin C. 1859. On the origin of species by means of natural selection, or the

preservation of favoured races in the struggle for life. London: JohnMurray.

Delwiche CF, Karol KG, Cimino MT, Sytsma KJ. 2002. Phylogeny of

the genus Coleochaete (Coleochaetales, Charophyta) and related taxainferred by analysis of the chloroplast gene rbcl. Journal of Phycology 38:394403.

Doebley J, Lukens L. 1998. Transcriptional regulators and the evolution

of plant form. The Plant Cell 10: 10751082.Edwards D. 1969. Zosterophyllum from the lower old red sandstone of

South Wales. New Phytologist 68: 923931.Ehrlen J, Bisand I, Hedenas A. 2000. Cost of sporophyte production in

the moss Dicranum polysetum. Plant Ecology 149: 207217.Friedl T, Bhattacharya D. 2006. Origin and evolution of green lichen

algae. In: Seckbach J, ed. Cellular origin, Life in Extreme Habitats. Vol.

4. Symbiosis. New York, NY: Kluwer Academic Publishers, 341359.




Gerrienne P, Dilcher DL, Bergamaschi S, Milagres I, Pereira E, Rodri-

gues MAC. 2006. An exceptional specimen of the early land plant

Cooksonia paranensis, and a hypothesis on the life cycle of the earliesteutracheophytes. Review of Palaeobotany and Palynology 142: 123130.

Gifford EM, Foster AC 1989. Morphology and evolution of vascular plants.3rd edn. New York, NY, USA: W. H. Freeman.

Graham LE. 1982. The occurrence, evolution, and phylogenetic signifi-

cance of parenchyma in Coleochaete Breb. (Clorophyta). AmericanJournal of Botany 69: 447454.

Graham LE. 1993. Origin of land plants. New York, NY, USA: JohnWiley.

Graham LE. 1996. Green algae to land plants: An evolutionary transition.

Journal of Plant Research 109: 241251.Graham LE, Wilcox LW. 2000. Algae. Upper Saddle River, NJ, USA:

Prentice Hall.

Gray J 1985. The microfossil record of early land plants: advances in

understanding of early terrestrialization, 19701984. In: Chaloner WG,

Lawson JD, eds. Evolution and environment in the late Silurian and

early Devonian. Philosophical Transactions of the Royal Society of London309B: 167195.

Gray J, Laufeld S, Boucot AJ. 1974. Silurian trilete spores and spore tetr-

ads from Gotland: their implications for land plant evolution. Science185: 260263.

Henschel K, Kofuji R, Hasebe M, Saedler H, Munster T, Theien G.

2002. Two ancient classes of MIKC-type MADS-box genes are present

in the moss Physcomitrella patens. Molecular Biology and Evolution 19:801814.

Itaya A, Woo Y-M, Masuta C, Bao Y, Nelson RS, Ding B. 1998. Devel-

opmental regulation of intercellular protein trafficking through plasmo-

desmata in tobacco leaf epidermis. Plant Physiology 118: 373385.Jansen R-P. 2001. mRNA localization: messages on the move. Nature

Reviews of Molecular and Cell Biology 2: 247256.Karol KG, McCourt RM, Cimino MT, Delwiche CF. 2001. The closest

living relatives of land plants. Science 294: 23512353.Kenrick P, Crane PR. 1997a. The origin and early evolution of plants on

land. Nature 389: 3339.Kenrick P, Crane PR. 1997b. The origin and early diversification of land

plants: a cladistic study. Washington, DC, USA: Smithsonian InstitutionPress.

Kerp H, Trevin NH, Hass H. 2004. New gametophytes from the Early

Devonian Rhynie chert. Transactions of the Royal Society of Edinburgh:Earth Sciences 94: 411428.

Knauth LP, Kennedy MJ. 2009. The late Precambrian greening of the

Earth. Nature 460: 728732.Kutschera U, Niklas KJ. 2004. The modern theory of biological evolution:

an expanded synthesis. Naturwissenschaften 91: 255276.Kutschera U, Niklas KJ. 2005. Endosymbiosis, cell evolution, and specia-

tion. Theory in Biosciences 124: 124.Kutschera U, Niklas KJ. 2008. Macroevolution via secondary endosymbi-

osis: a Neo-Goldschmidtian view of unicellular hopeful monsters and

Darwins primordial intermediate form. Theory in Biosciences 127: 277289.

Lee RE 2008. Phycology. Cambridge, UK: Cambridge University Press.Lee JH, Lin HW, Joo S, Goodenough U. 2008. Early sexual origins of

homeodomain heterodimerization and evolution of the plant KNOX BELL family. Cell 133: 829840.

Lewis LA, McCourt RM. 2004. Green algae and the origin of land plants.

American Journal of Botany 91: 15351556.Lucas WJ, Yoo B-C, Kragler F. 2001. RNA as a long-distance information

macromolecule in plants. Nature Reviews of Molecular and Cell Biology 2:849856.

Marin W, Melkonian M. 1999. Mesostigmatophyceae, a new class of

streptophyte green algae revealed by SSU rRNA sequence comparisons.

Protist 150: 399417.

Mattox KR, Stewart KD. 1984. Classification of the green algae: a concept

based on comparative cytology. In: Irvine DEG, John DM, eds. The sys-tematics of green algae. London, UK: Academic Press, 2972.

McCourt RM. 1995. Green algal phylogeny. Trends in Ecology and Evolu-tion 10: 159163.

McCourt RM, Delwiche CF, Karol KG. 2004. Charophyte algae and land

plant origins. Trends in Ecology and Evolution 19: 661666.Melkonian M. 1989. Flagellar apparatus ultrastructure in Mesostigma viride

(Prasinophyceae). Plant Systematics and Evolution 164: 93122.Mishler BD, Churchill SP. 1985. Transition to a land flora: phyloge-

netic relationships of the green algae and bryophytes. Cladistics 1:305328.

Niklas KJ. 1997. The evolutionary biology of plants. Chicago, IL, USA:University of Chicago Press.

Niklas KJ, Banks HP. 1990. A reevaluation of the Zosterophyllophyta

with comments on the origin of lycopods. American Journal of Botany77: 274283.

Niklas KJ, Kutschera U. 2009. The evolutionary development of plant

body plans. Functional Plant Biology 36: 682695.Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika

H, Kurata N. 2007. A germ cell specific gene of the ARGONAUTE

family is essential for the progression of premeiotic mitosis and meiosis

during sporogenesis in rice. The Plant Cell 19: 25832594.OKelly CJ, Watanabe S, Floyd GL. 2004. Ultrastructure and phyloge-

netic relationships of Chaetopeltidales ord. nov. (Chlorophyta, Chloro-

phyceae). Journal of Phycology 30: 118128.Okano Y, Aono N, Hiwatashi Y, Murata T, Nishiyama T, Ishikawa T,

Kubo M, Hasebe M. 2009. A polycomb repressive complex 2 gene

regulates apogamy and likely played a role in the evolution of extended

diploid generation and branching in land plants. Annual Meeting of theBotanical Society of America (Abstract 945), pp. 21

Pagnussat GC, Alandete-Saez M, Bowman JL, Sunaresan V. 2009.

Auxin-dependent patterning and gamete specification in the Arabidopsisfemale gametophyte. Science 324: 16841689.

Pickett-Heaps JD. 1975. Green algae. Structure, reproduction and evolutionin selected genera. Sunderland, MA, USA: Sinauer.

Probst E. 1986. Deutschland in der Urzeit. Von der Entstehung des Lebensbis zum Ende der Eiszeit. Munchen, Germany: Bertelsmann Verlag.

Raven JA. 1997. Multiple origins of plasmodesmata. European Journal ofPhycology 32: 95101.

Raven JA. 1999. The size of cells and organisms in relation to the evolution

of embryophytes. Plant Biology 1: 212.Raven JA. 2002. Selection pressures on stomatal evolution. New Phytologist

153: 371386.

Raven JA, Edwards D. 2001. Roots: evolutionary origins and biogeochem-

ical significance. Journal of Experimental Botany 52: 381401.Read DJ, Duckett JG, Francis R, Ligrone R, Russell A. 2000. Symbiotic

fungal associations in lower land plants. Philosophical Transactions ofthe Royal Society of London, Series B, Biological Sciences 355: 815831.

Remy W, Geusel PG, Hass G. 1993. The gametophyte generation of some

Early Devonian plants. International Journal of Plant Science 154: 3538.Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H,

Nishiyama T, Perroud P-F, Lindquist EA, Kamisugi Y et al. 2008. ThePhyscomitrella genome reveals evolutionary insights into the conquest ofland by plants. Science 319: 6469.

Rydgren K, kland RH. 2002. Ultimate costs of sporophyte production

in the clonal moss Hylocomium spendens. Ecology 83: 15731579.Scherp P, Grotha R, Kutschera U. 2001. Occurrence and phylogenetic sig-

nificance of cytokinesis-related callose in green algae, bryophytes, ferns

and seed plants. Plant Cell Reports 20: 143149.Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya IN.

1996. The mac1 gene: controlling the commitment to the meioticpathway in maize. Genetics 142: 10091020.




Shubin N, Tabin C, Carroll SB. 1997. Fossils, genes and the evolution of

animal limbs. Nature 388: 629648.Sinnott EW. 1960. Plant morphogenesis. New York, NY, USA: McGraw-

Hill.

Smith GM. 1950. The freshwater algae of the United States. New York, NY,USA: McGraw-Hill.

Stebbins GL, Hill GJC. 1980. Did multicellular plants invade the land?American Naturalist 115: 342353.

Steemans O, Le Herisse A, Melvin J, Miller MA, Paris F, Verniers J,

Wellman CH. 2009. Origin and radiation of the earliest vascular land

plants. Science 324: 353.Strother PK, Al-Hajri S, Traverse A. 1996. New evidence for land

plants from the lower Middle Ordovician of Saudi Arabia. Geology24: 5558.

Suda S, Watanabe MM, Inouye I. 1989. Evidence for sexual reproduction

in the primitive green alga Nephroselmis olivacea (Prasinophyceae).Journal of Phycology 25: 596600.

Sym SD, Pienaar RN. 1993. The class Prasinophyceae. In: Round FE,

Chapman DJ, eds. Progress in phycological research. London, UK: Bio-Press Ltd., 281376.

Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K,

Munster T, Theien G, Nozaki H, Ito M. 2005. Characterization of

MADS-box genes in charophycean green algae and its implications for

the evolution of MADS-box genes. Proceedings of the National Academyof Sciences, USA 102: 24362441.

Tanahashi T, Sumikawa N, Kato M, Hasebe M. 2005. Diversification of

gene function: homologs of the floral regulator FLO LFY control the

first zygotic division in the moss Physcomitrella patens. Development 132:17271736.

Taylor TN, Kerp H, Hass H. 2005. Life history biology of early land

plants: Deciphering the gametophyte phase. Proceedings of the NationalAcademy of Sciences, USA 102: 58925897.

Taylor TN, Taylor EL, Krings M. 2009. Paleobotany. The biology and evo-lution of fossil plants, 2nd edn. New York, NY, USA: Academic Press.

Walbot V, Evans MMS. 2003. Unique features of the plant life cycle and

their consequences. Nature Reviews Genetics 4: 369379.Wellman CH, Osterloff PL, Mohiuddin U. 2003. Fragments of the earli-

est land plants. Nature 425: 282285.Willis KJ, McElwain JC. 2002. The evolution of plants. Oxford, UK:

Oxford University Press.

Worden AZ, Lee J-H, Mock T et al. 2009. Green evolution and dynamicadaptations revealed by the genomes of the marine picoeukaryote Micro-monas. Science 324: 268272.

Yoshii Y, Takaichi S, Maoka T, Inouye I. 2003. Photosynthetic pigment

composition in the primitive green alga Mesostigma viride (Prasinophy-ceae): phylogenetic and evolutionary implications. Journal of Phycology39: 570576.

Zignone A, Borra M, Brunet C, Forlani C, Kooistra WHCF, Procaccini

G. 2002. Phylogenetic position of Crustomastix stigmatica sp. nov. andDolichomastix tenuilepis in relation to the Mamiellales (Prasinophyceae,Chlorophyta). Journal of Phycology 38: 10241039.




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