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The Origin of Alternation of Generations in Land Plants

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The Origin of Alternation of Generations in Land Plants Theoriginof alternation of generations inlandplants: afocuson matrotrophy andhexose transport Linda K.E.Graham and LeeW .Wilcox Department of Botany,University of Wisconsin, 430Lincoln Drive, Madison,WI 53706, USA (lkgraham@facsta¡.wisc .edu ) Alifehistory involving alternation of two developmentally associated, multicellular generations (sporophyteand gametophyte) is anautapomorphy of embryophytes (bryophytes + vascularplants) . Microfossil dataindicate that Mid ^Late Ordovicianland plants possessed such alifecycle, and that the originof alternationof generationspreceded this date.Molecular phylogenetic data unambiguously relate charophyceangreen algae to the ancestryof monophyletic embryophytes, and identify bryophytes as early-divergentland plants. Comparison of reproduction in charophyceans and bryophytes suggests that the followingstages occurredduring evolutionary origin of embryophytic alternation of generations: (i) originof oogamy;(ii) retention ofeggsand zygotes on the parentalthallus; (iii) originof matrotrophy (regulatedtransfer ofnutritional and morphogenetic solutes fromparental cells tothe nextgeneration); (iv)origin of a multicellularsporophyte generation ;and(v) origin of non-£ agellate, walled spores. Oogamy,egg/zygoteretention andmatrotrophy characterize at least some moderncharophyceans, and arepostulated to represent pre-adaptativefeatures inherited byembryophytes from ancestral charophyceans.Matrotrophy is hypothesizedto have preceded originof the multicellularsporophytes of plants,and to represent acritical innovation.Molecular approaches to the studyof the originsof matrotrophyinclude assessment ofhexose transporter genesand protein family members andtheir expressionpatterns. Theoccurrence inmodern charophyceans and bryophytes of chemically resistant tissues that exhibitdistinctive morphologycorrelated with matrotrophy suggests that Early ^Mid Ordovicianor older microfossils relevantto the originof land plant alternation of generations may be found. Keywords: alternationof generations;embryophytes; bryophytes; charophycean green algae ; hexosetransporter genesand proteins phyceans(brown algae) independently acquired alterna- 1.INTRODUCTION tionof two multicellular generations; so far as is known, Alternationof generations in autotrophs is generally their closest extantrelatives (tribophyceans and other de¢ned as the occurrence ofa lifehistory in which there ochrophyte/chromophyte/heterokontalgae) lack such a areat least twomulticellular generations, the gameto- lifehistory .Amongmodern green algae, alternation of phyteand the sporophyte,linked by unicellular repro- twomulticellular generations occurs onlyin certain ductivestages, namelygametes andspores (¢gure 1 ). orders ofthe class Ulvophyceae,and is lackingin the Sporesare generated by sporic meiosis, whichis the type three other greenalgal classes that includemulticellular ofmeiosis associatedwith alternation of generations forms (namelyT rebouxiophyceae,Chlorophyceae and (Raven et al.1999).Thisarticle doesnot address `alterna- Charophyceaesensu Graham& Wilcox(20 00)).Evidence tionof generations’that mayoccur in various autotrophic forindependent evolution of alternation of generations in protists that occurprimarily as unicells (e.g.certain red, brownand green algae suggests that it is highly haptophytealgae) ,orin heterotrophs (such asforamini- adaptive.Hypothetical adaptive aspects oflife history feraand fungi) . variationin autotrophs are discussed byBell & Koufo- panou( 1991),Otto &Goldstein (1992),Baillard( 1997) (a) The occurrence ofalternation ofgenerations andBell ( 1997).Areviewof alternation of generations in inautotrophs landplants, with an emphasis onfossil branchedgameto- Life histories involvingtwo or more alternatingmulti- phytesthat arethought to be linkedto the lifehistories of cellulargenerations have evolved several times among protracheophytesand early vascular plants, is provided photosyntheticprotists (algae)(Graham &Wilcox20 00). byKenrick ( 1994). Forexample, various bangiophycean red algaehave a life historywith two multicellular stages, anda three-stage (b) Ploidy change andalternation ofgenerations lifehistory appears to be a basic(plesiomorphic) feature Itshouldbe noted that whiletextbook depictions of for£ orideophyceanred algae.Ancestors ofphaeo- alternationof generations in algae and land plants Phil. Trans.R. Soc.Lond. B (2000) 355, 757^767 757 © 2000The RoyalSociety 758L. K. E. Grahamand L. W.Wilcox Alternation ofgenerations s e t a l R! l s e n g a a e l l meiospores f a - r s n a n o h a s s n C e n n c t s a n + s a y e t e h n e n a c a e 2n c p g t a e y r e l n y o m e s s h i c h a t t p g v r p x y p i i h r r t o o u h o d c o s a p n s - e l r o i o w w o o o y e r s u l b s s l l n s c e v a e r e r o h r l r o v s a i o a C T U P M e C l h m v sporophyte gametophyte * * * gametes Figure1. Diagram of alternationof multicellulargenerations. R!indicatesthe occurrence of meiosis.A lifehistory involving spatiallyand temporally separate generations is characteristi c ofseveralgroups of algae. typicallydescribe the gametophyticgeneration as being Figure2. Diagrammatic representation of phylogenetic haploid,and the sporophyticgeneration as diploid, there relationshipsamong various groups of thegreen algae and aremany examples among the algaeof life history phase embryophytes.Asterisks indicate cases of presumed changethat arenot correlated with change in chromo- independentorigin of alifehistory involving alternation of some number (Graham &Wilcox20 00).Forexample, twomulticellular generations. The barindicates the only the nucleiof sporophytes and gametophytes of the brown knowncase among green autotrophs of theoccurrence of a seaweed Haplospora globosa (Tilopteridales)possess the dependent,multicellular sporophyte (alternation of same number ofchromosomes. However, the DNA level generationsthat are not separated temporally or spatially). ofsporophytic nuclei is twice that ofgametophytic nuclei (Kuhlenkamp et al.1993).Inother algae,environmental Table 1. Matrotrophy and associated life history change have factorsare thought to be as, or perhaps more, important led tothe origin ofthree high-diversity, long-lived clades thanchromosomal level in determining the directionof lifehistory phase change. Environmental e¡ ects are reproductive regardedas possible explanations for cases ofapogamy clade innovation mechanism (transition tothe sporophytephase in the absenceof gameteproduction and syngamy) and apospory (transi- £orideophycean carposporophyte n/2n cellfusions tionto the gametophyticphase in the absenceof meiosis red algae andspore production).Inseedless plants,apogamy and embryophytes dependentembryo placental transfer aposporyare also observed, but genedosage e¡ ects are cells important.Maintenance of sporophytic growth depends eutherianmammals viviparity complexplacenta onthe presence ofat least twosets ofchromosomes, whereasgametophytic growth in culture doesnot continuewhen four or more sets ofchromosomes are andlater-divergent tracheophytes (Kenrick &Crane present (Bell1991 ). 1997).Itis importantto recognize that alternationof Inhigher plants, there aremany examples of produc- generationsin the KingdomPlantae is distinctive inthat tionof young sporophytes (embryos) fromcells other embryonicsporophytes occur in close spatialand thanzygotes (e.g. microspore embryogenesis,somatic temporalassociation with female (or bisexual) gameto- embryogenesisand apomixis) (Harada et al. 1998), and phytes.Plant embryos, including those ofthe simplest the geneticbasis forsuch variantsfrom the expectedlife liverwortsas wellas derived angiosperms, seem generally historycycling is becomingclearer. Forexample, the tobe nutritionally and developmentally dependent on Arabidopsis gene LEAFYCOTYLEDON1 (LEC1), which parentalgametophyte tissues forat least some periodof encodesa transcriptionfactor ,is su¤cient toinduce time inearly development. The presence ofa dependent embryo-likedevelopment from vegetative cells (Lotan embryonicstage is the basis forthe term embryophytes, et al. 1998). commonlyused asasynonymfor Kingdom Plantae. The occurrence ofalternation of multicellular generations (c) Importance ofsporophyte/ gametophyte coupledwith dependent embryos in all groups of land interactions plantssuggests that these features areautapomorphic Theabove variations having been noted, a lifehistory (uniqueand de¢ ning) features ofembryophytes(¢ gure 2) . involvingalternation of multicellular gametophyte and Multicellularsporophytes do not occur in the charophy- sporophytegenerations characterizes allgroups of extant ceans,the greenalgal lineage most closelyrelated to landplants, which comprise the KingdomPlantae, as embryophytes(Graham 1993),anddependence of the de¢ned by Raven et al.(1999).Members ofthe extant embryonicsporophyte is lackingin most other algaethat plantkingdom constitute amonophyleticgroup that havealternation of generations. An exception to this includesmultiple lineagesof early-divergent bryophytes generalityis the £oridophyceanred algae,whose Phil.Trans.R. Soc.Lond. B (2000) Alternation ofgenerations L. K. E.Grahamand L. W.Wilcox759 benoted,however, that fewactual measurements offertil- izationrates havebeen made for red algae.)Asimilar adaptivebene¢ t hasbeen hypothesized to accrue to seed- less landplants, whose fertilization rates maybe limited byavailability of liquid water for transport of£ agellate sperm (Searles 1980).Therest ofthis paperfocuses on palaeontological,neontological and combined approaches
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