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Vegetative and Reproductive Innovations of Early Land Plants K.S.Renzaglia and Others 771

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Vegetative and Reproductive Innovations of Early Land Plants K.S.Renzaglia and Others 771 Vegetative andreproductiveinnovations of earlylandplants: implicationsfor a uniedphylogeny KarenSue Renzaglia 1, R. Joel Du¡1{,DanielL. Nickrent 1 and David J.Garbary 2 1Department of PlantBiology and Center for Systematic Biology,Southern Illinois University,Carbondale, IL6 2901-6509,USA ([email protected] ) 2Department of Biology,StFrancis Xavier University,Antigonish, Nova Scotia,Canada B2G 2W5 Asthe oldest extantlineages of land plants, bryophytes provide a livinglaboratory in which to evaluate morphologicaladaptations associated with early land existence. Inthis paperwe examine reproductive and structural innovationsin the gametophyteand sporophyte generations of hornworts, liverworts, mosses andbasal pteridophytes. Reproductive features relatingto spermatogenesis andthe architecture ofmotile malegametes areoverviewed and evaluated from anevolutionaryperspective. Phylogeneticanalyses of a dataset derivedfrom spermatogenesis andone derived from comprehensive morphogenetic data are comparedwith a molecularanalysis of nuclearand mitochondrialsmall subunitrDNA sequences. Althoughrelatively small becauseof arelianceon waterfor sexual reproduction, gametophytes of bryo- phytesare the most elaborateof those producedby any land plant. Phenotypic variability in gametophytichabit ranges from leafy to thalloid forms withthe greatest diversityexhibited by hepatics. Appendages,including leaves, slime papillaeand hairs, predominate in liverworts and mosses, while hornwortgametophytes are strictly thalloidwith no organized external structures. Internalizationof reproductiveand vegetative structures withinmucilage-¢ lled spaces is anadaptive strategy exhibited by hornworts.The formative stages ofgametangial development are similar inthe three bryophytegroups, withthe exceptionthat inmosses apicalgrowth is intercalatedinto early organogenesis, a feature echoed inmoss sporophyteontogeny . Amonosporangiate,unbranched sporophyte typi¢ es bryophytes,but developmentaland structural innovationssuggest the three bryophytegroups diverged prior to elaboration of this generation.Sporo - phytemorphogenesis in hornworts involves non-synchronized sporogenesis and the continuedelongation ofthe singlesporangium, features uniqueamong archegoniates. In hepatics, elongation of the sporophyte seta andarchegoniophore is rapidand requires instantaneouswall expandability and hydrostatic support. Unicellular,spiralledelaters andcapsule dehiscence throughthe formationof four regular valves are autapomorphiesof liverworts. Sporophytic sophistications in the moss cladeinclude conducting tissue, stomata,an assimilative layer and an elaborate peristome forextended spore dispersal. Characterssuch asstomata and conducting cells that areshared among sporophytes of mosses, hornwortsand pterido - phytesare interpreted asparallelismsand not homologies. Our phylogeneticanalysis of three di¡erent datasets isthe most comprehensiveto date and points to a singlephylogenetic solution for the evolutionof basal embryophytes. Hornworts are supported as the earliest divergentembryophyte clade with a moss/liverwortclade sister totracheophytes. Among pterido - phytes,lycophytes are monophyletic and an assemblage containing ferns, Equisetum andpsilophytes is sister toseed plants.Congruence between morphological and molecular hypotheses indicates that these datasets aretracking the same phylogeneticsignal and reinforces ourphylogenetic conclusions. I t appearsthat totalevidence approaches are valuable in resolving ancient radiations such asthose charac- terizingthe evolutionof earlyembryophytes. More informationon landplant phylogeny can be foundat: http://www.science.siu.edu/landplants/index.html. Keywords: bryophytes;embryophytes; gametophyte ;landplant phylogeny ;morphogenesis; spermatogenesis that werefuelled by stochastic geneticchanges and culled 1.INTRODUCTION bynatural selection (Niklas1 997;Bateman et al. 1998). Theearly evolution of land plants was characterized by Poisedat the extremity ofan uninhabited landscape, highrates ofmorphological and reproductive innovations transitionalstreptophytes (greenplants) experienced a burst ofdiversi¢ cation that resulted inradiation into and {Present address:Department of Biology ,The Universityof Akron, Akron,OH 44325-3908, USA. exploitationof avarietyof new terrestrial sites. Repeated Phil. Trans.R. Soc.Lond. B (2000) 355, 769^793 769 © 2000The RoyalSociety 770K. S.Renzagliaand others Vegetative and reproductive innovations ofearly land plants andsimultaneous patterns ofextensive morphological wereview and update two previously published morpho- diversi¢cation followed by widespread decimation logicaldata sets (Garbary et al. 1993;Garbary & Renza- presumablycharacterized these earlystages ofland colon- glia1 998)and a moleculardata set that combines ization(Gould 1989; Kenrick & Crane1 997 a). Of the sequences ofboth nuclear and mitochondrial small magnitudeof morphological experiments that were subunit(SSU) rDNA. attempted, onlylimited fragments havepersisted through the millennia,including the three lineagesof bryophytes 2.CELL STRUCTURE (Stewart &Rothwell1993; T aylor& Taylor1 993). Giventhe time since divergence,the depauperatefossil Amongembryophytes, there is remarkableconsistency recordand the vastness ofthe newlyinhabited landscape, inthe ultrastructure ofparenchyma cells. The`typical’ it is notsurprising that the earlyphylogenetic history of livingphotosynthetic cell containsa largecentral vacuole, landplants remains oneof the majorunresolved problems aperipheralnucleus, mitochondria, endoplasmic reti- inevolutionary biology .Axiomaticto current evolu- culumand lenticular chloroplasts equipped with grana tionarythought is the conceptthat embryophytesare andscattered starch (Gunning& Steer 1996).Thebryo- monophyletic,that bryophytesrepresent the basalclades phytesand lycophytes exhibit the greatest diversityin andthat Charophyceae,especially Coleochaetales and organellarcomplement and¢ nestructure, andthese Charales,are the closest livingalgal relatives of arche- cellularfeatures provideimportant clues asto evolu- goniates(McCourt 1995).Beyondthese acceptedmaxims tionaryrelationships (Duckett &Renzaglia1 988;Brown there isnoconsensus astointerrelationships amongbryo- &Lemmon 1993).Solitaryplastids (monoplastidy)are phytesand basal pteridophytes. Indeed, virtually every foundin most vegetativecells ofhornworts and charac- conceivablehypothesis regarding bryophyte phylogeny terize mitotic cells ofrepresentative taxaand/ ortissues hasbeen proposed: from paraphyleticin a varietyof (especiallyspermatogenous tissue) ofall bryophytes and branchingorders, tohornworts basal and mosses and lycophytes(Brown & Lemmon 1990 a,1993).Likewise, liverwortsmonophyletic, to a completelymonophyletic monoplastidicmeiosis (discussed below)is distributed bryophyteassemblage (Bopp & Capesius1 996;Capesius amongrepresentatives ofall these clades.Based on the &Bopp1 997;Bremer et al.1987;Garbary et al. 1993; widespreadoccurrence ofmonoplastidy in charophycean Garbary& Renzaglia1 998;Hedderson et al. 1998; Lewis algaeand the exclusivedistribution of this conditionamong et al. 1997;Kenrick & Crane1997 a; Malek et al. 1996; basalembryophytes, it is safeto conclude that monoplastidy Mishler &Churchill1 984,1 985;Mishler et al. 1994; Du¡ is plesiomorphic(Brown & Lemmon 1990 a; Graham &Nickrent 1999;Nishiyama & Kato1 999).Clearly,new 1993).Toensure distributionof a plastidinto daughter dataor perhaps new insights onanalysing existing data cells, the divisioncycle of plastids must betightly linked arerequired toresolve this phylogeneticdilemma. tonuclear division in monoplastidic cell lineages.Plastids Bynature of their antiquity,liverworts,hornworts, areintimately associated with microtubule-organizing mosses andbasal pteridophytes represent relics ofa once centres (MTOCs) andthe twoform the focalpoints for more diverse £ora,and, as the oldest livingremnants of productionof spindlemicrotubules. earlyland colonization, these organismsprovide a living Inliverworts, only spermatogenous cells aremonoplas- laboratoryin which to examine early morphological tidic andvegetative cells arepolyplastidic. During the adaptationsto existence onland. In this paper,we mitotic cycle,well-de¢ ned, electron-dense aggregations, exploremorphological and developmental features ofbryo- the so-calledpolar organizers, organize the spindles. phytesand basal pteridophytes at the cell,tissue, organ Thesestructures alsocharacterize the monoplastidic andwhole organism levels. Whenever possible,evidence is dividingcells inspermatogenous tissue ofliverworts. presented from more informativebasal representatives of Endoplasmicreticulum withinthe polarorganizer is the majorclades. This comparative approach is designed connectedto the nuclearenvelope and in this regard toidentify successful phenotypicinnovations of both the resembles the nuclearenvelope-based centrosome of gametophyteand sporophyte, which enabled these plants mosses andtracheophytes (V aughn& Harper 1998).Late tooptimize vegetativeand reproductive activities ina spermatogenouscells ofall archegoniates have centriolar terrestrial setting. Inaddition to illuminating phyloge- centrosomes andthis enablesdirect comparisonwith netic a¤nities, contemplationof morphological and similar algalMTOCs (see below). morphogeneticstrategies providesvaluable insight into Examinationof the internalstructure ofhornwortplas- the directionand sequence ofcharactertransformation. tids providesevidence of further retention ofalgal Thisreview
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