Perspective: The Origin of Flowering Plants and Their Reproductive Biology- A Tale of TwoPhylogeniesAuthor(s): William E. Friedman and Sandra K. FloydReviewed work(s):Source: Evolution, Vol. 55, No. 2 (Feb., 2001), pp. 217-231Published by: Society for the Study of EvolutionStable URL: http://www.jstor.org/stable/2640745 .Accessed: 17/02/2012 02:23Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jspJSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact firstname.lastname@example.org. Society for the Study of Evolution is collaborating with JSTOR to digitize, preserve and extend access to Evolution.http://www.jstor.org
ESVO)LUTlI ON INTERNATIONAL JOURNAL OF ORGANIC EVOLUTION PUBLISHED BY THE SOCIETY FOR THE STUDY OF EVOLUTIONVol. 55 February 2001 No. 2Evolution, 55(2), 2001, pp. 217-231 PERSPECTIVE: THE ORIGIN OF FLOWERING PLANTS AND THEIR REPRODUCTIVE BIOLOGY-A TALE OF TWO PHYLOGENIES WILLIAM E. FRIEDMAN1 AND SANDRA K. FLOYD Population and OrganismicBiology, University Colorado, Boulder, Colorado 80309 Department Environmental, of of 1E-mail:ned@ colorado.edit Abstract.-Recently, areas of plantphylogeny two have developedin waysthatcould nothave been anticipated, even a fewyearsago. Amongextant seed plants,newphylogenetic hypotheses that a of suggest Gnetales, group nonflowering seed plantswidelyhypothesized be the closest extantrelativesof angiosperms, to may be less closely relatedto angiosperms thanwas believed. In addition, recentphylogenetic analyses of angiosperms have, forthe first time, clearlyidentified earliest the lineagesofflowering plants:Amborella, and Nymphaeales, a lade that includes Illiciales/ Trimeniaceae/Austrobaileyaceae. Together, new seed plantand angiosperm the phylogenetichypotheses have major implications interpretation homologyand character for of evolutionassociatedwiththe originand earlyhistory of flowering plants.As an exampleof the complexand oftenunpredictable of and interplay phylogenetic comparative biology, analyzetheevolution doublefertilization, we of a processthat forms diploidembryo a triploid a and endosperm, the embryo-nourishing tissueuniqueto flowering plants.We demonstrate thenew phylogenetic how hypotheses for seed plantsand angiosperms can significantly alterpreviousinterpretations evolutionary of homologyand firmly entrenched assumptions aboutwhatis synapomorphic flowering of plants.In thecase of endosperm, solution the a to century-old questionof its potential homology withan embryo a femalegametophyte haploidegg-producing or (the generation within lifecycle of a seed plant)remains the complexand elusive. Too little knownof thecomparative is reproductive biologyofextant seed nonflowering plants(Gnetales, conifers, cycads,and Ginkgo) analyzedefinitively to thepotential of homology endosperm withantecedent structures. Remarkably, new angiosperm the phylogenies reveal thata second fertilizationeventto yield a biparental endosperm, long assumedto be an important synapomorphy of flowering plants,cannotbe conclusively for resolvedas ancestral flowering plants.Although substantiveprogress has been made in theanalysisof phylogenetic relationships seed plantsand angiosperms, of theseefforts have notbeen matched comparable by levels of activity comparative in biology.The consequenceof inadequatecomparative bio- logical information an age of phylogenetic in biology is a severe limitation the potentialto reconstruct on key evolutionary historicalevents. Key words.-Amborella, double fertilization, angiosperms, endosperm, seed plants. Gnetales,phylogeny, Received June21, 2000. AcceptedOctober9, 2000. Along with the origins of vascular plants and seed plants, There have been threemajor obstacles to thereconstructionthe origin of angiosperms representsone of the three most of historical events associated with the origin and early di-significantevents in the 475 million-year evolutionaryhis- versificationof angiosperms. First,the macrofossil record oftory of land plants. With more than 250,000 extant species early floweringplants has shed littlelight on the question of(Crane et al. 1995), angiosperms are the largest and most which angiosperm lineages are truly most ancient. Fossilsdiverse group of extantplants. Althoughubiquitous and dom- with affinitiesto diverse floweringplant lineages, includinginant in nearly every terrestrialecosystem, angiosperms are monocots (Crane et al. 1995), Platanaceae (Friis et al. 1994b),also one of the most recent major groups of land plants to Ceratophyllaceae (Dilcher 1989), Nelumbonaceae (Upchurchhave evolved, with a fossil record extendingback only to the et al. 1994), Laurales (Upchurch et al. 1994), Winteraceaeearly Cretaceous, more than 130 million years ago (Crane et (Walker et al. 1983), and Chloranthaceae (Friis et al. 1986,al. 1995). Paradoxically, we know less about the origin and 1994a) are all found in early Cretaceous floras. Second, forearly evolutionaryhistoryof angiosperms than we do about more than a centurytherehas been considerable uncertaintymany considerably older groups of land plants. Darwins about the identityof the closest seed plant relatives of an-"abominable mystery" of the origin and early evolution of giosperms (Doyle 1998). Difficulty in establishing angio-flowering plantscontinuesto challengeevolutionary biologists. sperm outgroups (or immediate ancestors) has made assess- 217 C 2001 The Society for the Study of Evolution. All rightsreserved.
218 W. E. FRIEDMAN AND S. K. FLOYDmentof the homologies of important flowering plant features, Anthophytesfromthe carpel to the second integumentof the ovule, prob-lematic. Third, a numberof conflicting hypotheses about the Gnetales lidentity of the most basal (and potentially plesiomorphic) Eo 0extant angiosperms competed formuch of the twentieth cen- 0 -~~~~~~ 0) sQ)~~~~~~~~~~~~~~~. )tury. During the last 25 years alone, everythingfrom the O0 -_1 -> O, -C X ~ O - 0 Q 3 0Magnoliaceae (and allies), the traditionalfavorite(Takhtajan1969; Dahlgren 1980; Cronquist 1981; Walker and Walker1984; Donoghue and Doyle 1989a; Thorne 1992), to Cera-tophyllum(Les 1988; Chase et al. 1993), Chloranthaceae/Piperaceae (Taylor and Hickey 1992; Nixon et al. 1994),Schisandraceae (Martin and Dowd 1986), monocots (Burger1977, 1981), and Nymphaeaceae (Hamby and Zimmer 1992;Doyle et al. 1994) have been proposed as the earliest diver-gent lineage of angiosperms. To decipher the origin and early evolutionary historyof commonancestorangiosperms, a clear formulationof the phylogenetic rela- ~~of Gnetalesandtionships of angiosperms to other groups of seed plants and / ~~angiospermsthe phylogenetic interrelationships basal angiosperms is ofabsolutely necessary (Friedman and Carmichael 1996). Once FIG.1. Hypothesis relationships extant of of seed plantsbased onrobust phylogenetic hypotheses have been established, crit- morphological phylogenetic analyses (see textforcitations).Theical interpretation the comparative biological featuresof of anthophyte hypothesis expressedin thisphylogeny suggeststhatbasal angiosperms and angiosperm outgroups can be used to and Gnetales(along withBennettitales several otherextinct Me-inferand reconstruct evolutionaryhistoryof a broad range the sozoic seed plantlineages) are the closest relativesof flowering plants.Because Gnetalesare the mostclosely relatedextantseedof biological characters (Floyd et al. 1999). Thus, study of plantsto angiosperms,theysharea relatively morerecent common the origin of floweringplants, like the origin of any group ancestor.This phylogenetic hypothesis was favoredfrom1985 to of organisms, relies on the interplay of phylogenetic and 1999 (Donoghue and Doyle 2000). comparative biology. The past two years have been a time of unprecedented turmoil,surprise,and advancement in our understandingof with additional molecular phylogenetic analyses of extant the phylogenetic relationships of plants. In particular, two seed plants consistentlysupportedthe status of the Gnetales areas of plant phylogeny have developed in ways thatcould as the most closely related extantseed plants to angiosperms not have been anticipated, even a few years ago: the phy- (Fig. 1). By the mid-1990s, the issue of the relationship of logenetic relationshipsof extantseed plants (and specifically angiosperms and Gnetales was widely perceived as resolved. hypotheses for the closest extant relatives of angiosperms) Although the hypothesisthatGnetales is closely related to and the identificationof the most basal extant angiosperm angiosperms was consistently supported in phylogenetic lineages. analyses of the last 15 years, almost every molecular phy- logenetic analysis of extant seed plants since 1996 (Gore- THE NEW PHYLOGENIES AND THEIR IMPACT ON ANALYSIS mykinet al. 1996; Chaw et al. 1997; Hansen et al. 1999; Qiu OF CHARACTER EVOLUTION et al. 1999; Samigullin et al. 1999; Bowe et al. 2000; Chaw et al. 2000; Frohlich and Parker 2000; Sanderson et al. 2000) Seed Plant Phylogeny.A Radical Change in Favored has failed to detect an affinitybetween the Gnetales and Hypotheses angiosperms. Instead, these recent molecular phylogenetic During the last century,many seed plant lineages were analyses reportthat Gnetales are most closely related to, orproposed as the closest relatives of angiosperms. These in- even nested within, conifers (Fig. 2). There may be goodclude Gnetales, Bennettitales,Caytoniales, Pentoxylales, and reason to suspect that the findingthat Gnetales are nestedGlossopteridales (Doyle 1998). Beginning with the morpho- within (paraphyletic) conifers is spurious (Donoghue andlogical cladistic studies of extant and extinct seed plants by Doyle 2000; Sanderson et al. 2000) based on an unusualCrane (1985) and Doyle and Donoghue (1986), a consensus chloroplast DNA structural mutation(loss of one copy of theemerged that angiosperms may be phylogenetically nested inverted repeat) shared by all conifers to the exclusion ofwithin a clade that contains several extinct lineages (Ben- other seed plants (including Gnetales; Raubeson and Jansennettitales,Pentoxylales, Caytoniales) and extant monophy- 1992). However, the hypothesisthatGnetales are closely re-letic Gnetales (Ephedra, Gnetum, and Welwitschia; Crane lated to conifers (among extant seed plants) appears to be1985; Doyle and Donoghue 1986, 1992; Martin and Dowd supported by DNA sequence data and the discovery of two1986, 1991; Zimmer et al. 1989; Loconte and Stevenson derived gene duplications in the chloroplast that are shared1990; Hamby and Zimmer 1992; Chase et al. 1993; Doyle by Gnetales and conifers (Raubeson 1998, pers. comm.).et al. 1994; Rothwell and Serbet 1994; Doyle 1996, 1998; In itself,the close alliance between conifers and GnetalesStefanovic et al. 1998). Although the phylogenetic position mightnot have representeda radical change fromearlier seedof the Gnetales had been viewed as uncertain for much of plant phylogenies, had conifersplus Gnetales been shown tothe 20th century, morphological cladistic analyses, along be closely related to angiosperms (as originallysuggested by
FLOWERING PLANTS-REPRODUCTIVE BIOLOGY 219 monophyletic gymnosperms EvolutionaryImplications of the New Seed Plant Phylogenies Gnetales-conifer lade The newest seed plant phylogenetic hypotheses (Fig. 2) Gnetales reveal that the paradigm of the late 20th century-that Gne- _ , ,, (I) tales are the closest living relatives of angiosperms-may well be incorrect. Gnetales may be most closely related to ~ ~ ~ 0 (1) -~ 0 I conifers, and the concept of a monophyletic extant gymno- ~~) Q ~~~~ 0) sperm lade that is the sister group to angiosperms is, for 6 L Q CD C) < the timebeing, supportedby a significant body of data (Bowe et al. 2000; Chaw et al. 2000; Frohlich and Parker 2000; Sanderson et al. 2000). There are several aspects of the new seed plantphylogenies that bear directly upon the interpretation character evo- of lution associated with the origin of floweringplants. First, the close relationship of Gnetales and conifers suggests that it is appropriate to more critically examine the comparative biology of these two major seed plant lineages to determine whethersome of theirsimilar featuresreflectunderlyingho- mologies that,in thepast, were notrecognized. These features might range from aspects of wood anatomy to embryogeny (e.g., suspensor and proembryoorganization,which are quite similar in Gnetales and Araucariaceae; Martens 1971) to commonancestor sperm cell organization (Gnetales and some conifers are the of Gnetales and only seed plants withbinucleate spermcells; Friedman 1991), angiosperms female gametophyteontogeny (conifers and Gnetales are the only seed plants in which substantial development of theFIG.2. Current hypothesis relationships extantseed plants of ofbased on recent molecular female gametophyteoccurs afterfertilization;Friedman and phylogenetic analyses(Goremykin al. et1996; Chaw et al. 1997; Hansen et al. 1999; Qiu et al. 1999; Sa- Carmichael 1998), and the process of fertilizationitself (asmigullin al. 1999; Bowe et al. 2000; Chaw et al. 2000; M. San- et will be discussed).derson, are pers.comm.).Extantgymnosperms monophyletic, and Within the contextof earlier anthophyte hypotheses (Gne-Gnetalesare nestedwithin paraphyletic a conifergroup.The most tales most closely related to angiosperms among extantseedrecentcommonancestor Gnetalesand angiosperms morean- of iscientthanis the case withthe anthophyte hypothesis and is the plants), homologous features of angiosperms and Gnetalescommonancestor all extantseed plants. of must have been present in the common ancestor of a mono- phyletic subset of seed plants thatincluded Gnetales, angio- sperms, and extinctlineages such as Bennettitales. If extant gymnospermsare monophyletic,any featureof Gnetales andWettstein  and hypothesized thefirst in cladisticanal- angiosperms that is presumed to be evolutionarily homolo-ysis of seed plantsby Hill and Crane ). However,an gous must have been present in the common ancestor of alladditional and unanticipated finding manyrecentmolec- of extant seed plants: cycads, Ginkgo, conifers, Gnetales, andular phylogenetic studiesis thatextantnonflowering seed angiosperms (Figs. 1, 2). The clear implication of the mono-plants(cycads,Ginkgo, conifers,Gnetales)comprise mono- a phyletic extantgymnospermhypothesis(or even of the morephyletic groupthatis the sisterlineage to flowering plants restricted of finding Gnetales sisterto conifers) is thatsimilar(but foranalysesthatyield gymnosperms paraphyletic, see biological featuresof Gnetales and angiosperms eithermustBowe et al. 2000; Chaw et al. 2000; Sanderson al. 2000). et have a deeper (more ancient) origin within the evolutionaryIf thishypothesis correct, mostrecent is the common ancestor historyof seed plants (if homologous) than had previouslyof Gnetalesand angiosperms also thecommon is ancestor of been assumed or they must representhomoplasies.all extant seed plants(Fig. 2). Giventhereality thatmostseed plantlineagesare extinct The Search for the Earliest Lineages of Extant Angiosperms(onlyfivemajorclades are extant) and thecomplexities and Yields a Surprise Consensusconflicting resultsof recentmolecularsequence analyses Within the last few years, there have been significantad-(Bowe et al. 2000; Chaw et al. 2000; Sanderson al. 2000), vances in the analysis of large-scale phylogenetic relation- et isit may yetbe some timebeforethe finalchapter written ships among floweringplants (Dahlgren and Bremer 1985;on the interrelationships cycads, Ginkgo, of conifers, Gne- Cronquist 1988; Donoghue and Doyle 1989a,b; Zimmer ettalesandangiosperms. However, evenifextant gymnosperms al. 1989; Loconte and Stevenson 1990; Les et al. 1991; Martinshouldultimately shownto be paraphyletic, hypoth- and Dowd, 1991; Hamby and Zimmer 1992; Taylor and Hick- be theesized sistergroupstatusof conifers Gnetalesindicates ey 1992; Chase et al. 1993; Qiu et al. 1993, 1999, 2000; andthatthe mostrestrictive lade thatGnetalescould possibly Doyle et al. 1994; Nixon et al. 1994; Soltis et al. 1997, 1998,sharewithangiosperms mustalso includetherelatively an- 1999; Nandi et al. 1998; Hoot et al. 1999; Mathews andcientconifers. Donoghue 1999; Graham et al. 2000). A central findingof
220 W. E. FRIEDMAN AND S. K. FLOYD Basal angiosperm grade logenetic analyses indicate thatmonotypicAmborella is sister a) to all other angiosperms; thatNymphaeales (Nymphaeaceae a) a) 0 plus Cabombaceae) is sister to all angiosperms exclusive of Amborella; and a lade thatincludes Illiciales (Illiciaceae plus CZ al) 0) 0) 00) C Schisandraceae) plus Trimeniaceae plus Austrobaileyaceae is C c- () C: o ~ CZ 0CZ sister to the remaining angiosperms (Fig. 3). Together,Am- o a- a) U borella, Nymphaeales, and the Illiciales/Trimeniaceae/Aus- E < Z *- F- <.9 0 , - E > E L c 3: W trobaileyaceae lade representa grade at the base of angio- sperms (the "ANITA grade" of Qiu et al. 1999; hereafter, the "basal angiosperm grade" of Fig. 3). Taken altogether, current the phylogeneticanalyses strong- ly support the hypotheses (Fig. 3) that monocots are mono- phyletic, but dicots are paraphyletic; magnoliids are a par- aphyletic basal assemblage of angiosperms in which mono- phyletic monocot and eudicot (having tricolpate pollen) clades are nested; and Anmborella, Nymphaeales, and the Il- liciales/Trimeniaceae/Austrobaileyaceae lade are basal to commonancestor the common ancestor of monocots and eudicots. Although of monocotsand not formallynoted in the literature, these phylogeneticanal- eudicots yses demonstratethatthe common ancestor of monocots andFIG. 3. Current of hypothesis relationships extant of basal angio- eudicots is notthe common ancestorof all extantangiospermssperms based on recent molecular phylogenetic analyses(Mathews (Fig. 3). This simple fact, as will be seen, has major impli-and Donoghue 1999; Parkinson al. 1999; Qiu et al. 1999, 2000; etSoltiset al. 1999; Graham Olmstead and 2000; Graham al. 2000). cations for assumptions about what is actually known about etThree clades (Amborellaceae,Nymphaeales,Illiciales/Trimeni- definingand synapomorphicfeaturesof floweringplants.aceae/Austrobaileyaceae) basal to the common ancestorof aremonocots and eudicots.A monophyletic "eumagnoliid" lade that EvolutionaryInmplications the New Angiosperm ofis sisterto the eudicotshas been recovered withweak support inrecentanalyses(Qiu et al. 2000). There is strong support the for Phylogenies ofmonophyly bothmonocots and eudicots. For more than a century,biological features common to both monocots and "dicots" were assumed to be generalrecent analyses of angiosperm relationships is that whereas (synapomorphic) features of all angiosperms. A key impli-monocotyledonous flowering plants comprise a monophyletic cation of the new angiosperm phylogenies (Fig. 3) is thatgroup (monocots), the dicotyledonous floweringplants (di- those featuresof angiosperms assumed to be synapomorphiccots) are a paraphyleticassemblage thatincludes magnoliids of angiosperms,but known only frommonocots and eudicotsand a large, nested monophyletic group, the eudicots (Fig. (the vast majority of dicots), may not be flowering plant3). Magnoliid lineages include diverse clades such as Aris- synapomorphies if they are absent from some or all of thetolochiales, Chloranthaceae, Nymphaeales, Piperales, Illi- most basal floweringplant lineages. The common ancestorciales, Winterales, Laurales, and Magnoliales. of monocots and eudicots is not the common ancestor of all Recent phylogenetic analyses of basal angiosperm inter- extant angiosperms (Fig. 3); in all recent phylogeneticanal-relationships also call into question longstanding assump- yses, three lineages of floweringplants (Amborella, Nym-tions about which lineages constitutethe earliest divergent phaeales and Illiciales/Trimeniaceae/Austrobaileyaceae)are(and potentiallyplesiomorphic) angiosperms. Although tra- basal to the common ancestor of monocots and eudicots.ditional views focused on the Magnoliaceae and close rela- Although flowers,carpets, microsporophyllswith four spo-tives (Takhtajan 1969; Dahlgren 1980, 1983; Cronquist 1981, rangia (stamens), bitegmic ovules, a highly reduced female 1988; Walker et al. 1983; Donoghue and Doyle 1989a,b; gametophyte(embryo sac), a three-celledmale gametophyte,Thorne 1992), several alternativeextant angiosperm groups and endosperm have been documented in all major lineageshave been favored in more recent phylogenetic analyses. of floweringplants and are known synapomorphies of an-These include the reduced aquatic Ceratophyllunt (Les 1988; giosperms, there are some biological features whose repre-Les et al. 1991; Chase et al. 1993; Nixon et al. 1994), Chlor- sentation in basal lineages of floweringplants remains un- anthaceae/Piperaceae (Taylor and Hickey 1992; Nixon et al. documented. 1994), Nymphaeaceae (Hamby and Zimmer 1992; Doyle et The renlainderof this paper will be devoted to a case study al. 1994), Schisandraceae (Martin and Dowd 1991), Schis- of the impact of the new seed plant and basal angiosperm andraceae/Illiciaceae/Austrobaileyaceae (Soltis et al. 1997), phylogenetic hypotheses on the reconstructionof the evo- monocots (Burger 1977, 1981), and Amborella (Soltis et al. lutionaryhistoryof two of the most definingfeaturesof an- 1997). giosperm biology: the process of double fertilization and the Beginning in 1999, a series of independentanalyses (Ma- formationof an endosperm that nourishes the embryo. As thews and Donoghue 1999; Parkinson et al. 1999; Qiu et al. will be seen, the continuous interplayof phylogenetic sys- 1999, 2000; Soltis et al. 1999; Graham and Olmstead 2000; tematics and comparative biology can sometimes yield sur- Graham et al. 2000) produced an unanticipatedconsensus on prising insights into what is known and, perhaps even more the most basal extant lineages of angiosperms. These phy- importantly, what is unknown.
FLOWERING PLANTS-REPRODUCTIVE BIOLOGY 221A CASE STUDY: THE EVOLUTION OF DOUBLE FERTILIZATION donous orchids and diverse dicotyledonous taxa such as Ran- AND ENDOSPERM unculaceae, Asteraceae, and Monotropaceae; by 1903, 16 an- giosperm families were known to have a second fertilization Although determinationof character distributionand its event (Coulter and Chamberlain 1903). The determinationdevelopmental underpinnings basal angiosperms is critical in thatdouble fertilization could be found in both major groupsto understanding the diversification of flowering plants of floweringplants, the monocots and the dicots, led Sargant(Doyle and Donoghue 1993; Friedman 1994), therehave been (1900) to conclude thatthis unique reproductiveprocess wasfew recentinvestigationsof the reproductivebiology of basal likely to be a feature of all floweringplants. Less than twoangiosperms. Except for importantcontributionson floral years afterits discovery, the race to determinethe extentofmorphology among basal extant taxa (e.g., Endress 1987, double fertilization among flowering plants was over, and the1994, 1995, 1997; Friis and Endress 1990; Tucker and Bour-land 1994; Williamson and Schneider 1994; Friis 1996; Tuck- inferencethatdouble fertilization was a synapomorphy (usinger and Douglas 1996; Endress and Igersheim 1997, 2000; modern terminology)of angiosperms, was firmly establishedIgersheim and Endress 1997), a few studies of embryology in the fields of comparative and evolutionaryplant biology.in basal taxa (Prakash et al. 1992; Chitralekha and Bhandari Modern research (mostly transmission electron micros-1993; Tobe et al. 1993; Heo and Tobe 1995; Rudall and copy) on double fertilization(specifically the second fertil-Furness 1997; Xuhan and Van Lammeren 1997; Floyd et al. ization event) in angiosperms has involved the study of a 1999; Floyd and Friedman 2000; Tobe et al. 2000), and re- very limited number of phylogeneticallyhighly derived eu-cently described early Cretaceous angiosperms (Taylor and dicot taxa that include Gossypium (Malvaceae) (Jensen andHickey 1990; Crane et al. 1994; Friis et al. 1994a,b, 1999, Fisher 1967), Linurn (Linaceae; dAlascio 1974), Spinacia2000; Crane et al. 1995; Sun et al. 1998; Mohr and Friis (Chenopodiaceae; Wilms 1981), Plumbago (Plumbaginaceae;2000), the origin and diversificationof many of the defining Russell and Cass 1981; Russell 1982), Populus (Salicaceae;reproductivefeatures of floweringplants remain unstudied. Russell et al. 1990), Glycine (Fabaceae; Folsom and CassMost importantly, the purposes of this paper, definitive for 1992), and Nicotiana (Solanaceae; Yu et al. 1994) and theinformation about double fertilizationand endosperm devel- highly derived monocot taxa Zea, Hordeurn, Triticurn, andopment in basal angiosperms, two features of angiosperm Triticale (all members of Poaceae; Cass and Jensen 1970;biology long thoughtto have been central to the radiation of You and Jensen 1985; Hause and Schr6der 1987; Mogensen floweringplants (Stebbins 1976; Tiffney 1981), is virtually 1988; Gao et al. 1992; M61 et al. 1994). Although the second nonexistent. fertilization process to initiatea triploidendospermmay vary among floweringplants (polar nuclei may fuse prior to or Double Fertilization: A Synapornorphy Angiosperms? of concurrentwith the second fertilizationevent), descriptions are fundamentallysimilar in monosporic monocots and eu- For a century,a double fertilizationprocess that yields a dicots. This stronglysuggests that the common ancestor ofdiploid embryoand a triploidendospermhas been considered these two large angiosperm clades expressed a pattern ofa definingfeature of angiosperms. Although endosperm is double fertilizationin which a second sperm nucleus fusedknown to be a ubiquitous feature of angiosperms, except with the polar nuclei of the central cell of the embryo sacwhere it has been secondarily lost (as in the Podostemaceae;Johriet al. 1992), the participationof two spermfroma single (Fig. 4). In contrast with the study of derived angiosperms, therepollen tube in an act of double fertilizationin angiospermshas been carefully documented in only a relatively small are just three reports of the fusion of a second sperm withnumber of mostly derived monocot and eudicot taxa. The the two polar nuclei (or theirfusion product) of the embryointellectual history of how double fertilization(to yield an sac in angiosperm lineages that are not withinthe clade de-embryo and a sexual endosperm) came to be thoughtof as fined by the common ancestor of eudicots and monocots:a general and definingfeatureof floweringplants (Friedman Brasenia (Khanna 1965), Nymphaea (Khanna 1967), and II-2001a) is fascinating. licium (Hayashi 1963). A single drawing,but no micrograph, The process of double fertilization floweringplants was in of a second fertilization event accompanied each publicationindependently discovered in Liliurn and Fritillaria by Na- and each of the original figuresis reproduced in Figure 5.vashin (1898) and Guignard (1899). Prior to this,it had been These drawings (Hayashi 1963; Khanna 1965, 1967) mayassumed that endosperm, the embryo-nourishing tissue of accurately depict the initiationof a second fertilization eventfloweringplants, was a developmental product of the fused (i.e., proximityof a putative sperm nucleus and the fusedpolar nuclei of the female gametophyte(embryo sac; Fig. 4). polar nuclei) in angiosperms basal to the common ancestorGuignard and Navashin documented that the endosperm of of monocots and eudicots, however, they cannot be consid-Lilium and Fritillaria originates from a fertilizationof the ered strong proof of double fertilization.This is especiallytwo polar nuclei of the embryo sac by the second sperm of so in light of an earlier reportof reproductionforNyrnphaeaa pollen tube. that indicated that "endosperm tissue [can form] without Within months of the announced discoveries of double triplefusion" (Cook 1909). Equally intriguing a suggestion isfertilizationin Lilium and Fritillaria (both members of the forthe basal monocot Acorus thata second fertilization eventLiliaceae), a massive effort was underway to determine does not occur prior to the development of an embryo-nour-whethera second fertilization eventto initiateendospermwas ishing endosperm (Buell 1938). In Acorus, the two polar nu-widespread among floweringplants. By 1900, double fertil- clei were reported to fuse (in the absence of a sperm) andization had been additionally documented in monocotyle- divide transverselyto initiate a diploid endosperm. Unfor-
222 W. E. FRIEDMAN AND S. K. FLOYD tube pollen twosperm Vj egg zygote synergid cells sngcesuegg nucleus diploid and ~~~~biparental cel E 0@ polarnuclei sperm secondsperm * CL nonfunctional W 0 ; sa cell ~central i primaryendosperm CL (1) antipodal cells nucleusdiploid and maternal G)c E pollen tube twosperm V ~~~~~egzygote cells synergid nucleus biparedand + biparental cel I polarnucleiermaf"dt sf l n o CL) th Qf centralcell formation the zygote. possiprimary of It is endosperm -0 antipodal cells triploid ~~~~~~~~~~~~nucleus C- ~~~~~~~~~~~~~~~~~~and biparentalFIh. 4. Two different possible developmental mechanisms the formation endosperm. for of Endosperm maternal origin:Priorto thediscovery of double fertilizationin floweringplants at the end of the 19th century,it was assumedthatfusionof the two polar nucleiof the central cell initiated strictly a maternal endosperm thatrepresented delay in femalegametophyte a development untilafter theformation the zygote.It is possible thatendosperm basal angiosperms of in forms thismanner in because a second fertilization eventhas notbeen definitively documented any of the mostbasal angiosperms. in Endosperm biparental origin:Followingthe discovery ofdouble fertilization flowering in plants,it was assumed(untilpresently) thatall endosperms flowering in plantswere formed fromasexual fusion a sperm of withtwo (or some other of number) polarnucleiof thecentral cell. The formation endosperm of from second afertilization eventhas onlybeen carefully confirmed monocots in and eudicots.tunately,no micrographs were published in support of this with a triploid fusion, as well as DNA quantitation of theconclusion. putative fertilizationproduct,will be essential. Even if second fertilizationevents are eventually conclu- Discovery that a second fertilizationevent (triple fusion)sively documented in the Nymphaeales and the Illiciales/ does not occur in some or all key basal angiosperm taxaTrimeniaceae/Austrobaileyaceae lade, determination of would have significant, and unexpected, implications forun-whetherthis featureof endosperminitiationrepresentsa syn- derstandingthe evolutionaryorigin of endosperm. Althoughapomorphy of floweringplants may still depend on an as- a second fertilizationevent has not been definitivelydocu-sessment of the condition in Amborella. The fertilizationpro- mented in any basal angiosperm, the formationof an endo-cess in Amborella has never been studied. If a second fertil- sperm (assumed to be sexually produced) derived from theization event is to be definitivelydocumented in an angio- central cell of the embryo sac has been reportedfor all basalsperm basal to the common ancestor of monocots and angiosperms (Johriet al. 1992). Thus, if a second fertilizationeudicots, micrographs of developmental events associated event is ultimatelyproven to be absent in key basal angio-
FLOWERING PLANTS-REPRODUCTIVE BIOLOGY 223 Si E~~0 E~~~~~ ~K E PTEE / Si - ~~~~~~S2 FPN S2FIG. 5. Figures of double fertilizationin (A) Brasenia (Cabombaceae, Nymphaeales); (B) Nyinphaea (Nymphaeaceae, Nymphaeales);and (C) Illicium (Illicaceae) reproduced fromKhanna (1965), Khanna (1967), and Hayashi (1963), respectively. Labeling has been added:A, antipodals; E, egg; FPN, fused polar nuclei; PT, pollen tube; Si, firstsperm; S2, second sperm.sperms,and plesiomorphic endospermis shown to be a strict- the fusion product of the two polar nuclei in the central cellly maternaltissue derived fromthefusionof two polar nuclei, of the female gametophytedirectlyproliferatesinto a strictlya new hypothesis for the origin of endosperm will involve maternal endosperm tissue; and (2) A later stage of endo-(Figs. 4, 6): (1) An evolutionary transitionalstage in which sperm evolution in which additional participationof a sperm nucleus with the fusion of polar nuclei results in the origin of a hybrid(maternal/paternal) triploidendosperm,as occurs Basal angiosperms in monocots and eudicots. The inevitable consequence of a) CZ a) such a discovery (if it were made) would be that, because C 0X) CS 0 Eumagnoliids the evolution of endosperm did not initiallyinvolve a fusion E a) aC > between a sperm and two polar nuclei, endosperm tissue is CS CS ~ 0 evolutionarilyhomologous withthe female gametophyte. Im- 0 a)S CZ 4- portantly,even if double fertilizationis eventually docu- o OL C CZ L. L_ E -~E aa) *~E o0 > .CSZ t S mented in all extant basal angiosperms, it is still possible <C Z H <C 2: a WL that the endosperm of the ancestors of extant angiosperms (stem lineage angiosperms) was originallya diploid maternal structure and later became a triploid product of a sexual fu- U) - 0 frizatio an 0 i sion with a sperm (Friedman 2001a,b). From a theoretical perspective, if a sexually formed en- dosperm is not a synapomorphyof angiosperms, this would have a significantimpact on hypotheses concerning the pos- sible adaptive value or key innovation status (sensu Sander- of origin double son and Donoghue 1994) of a hybrid (biparental) embryo- fertilization triploid and biparentalendosperm nourishingtissue in floweringplants (see Brink and Cooper 1940; Stebbins 1976). Recent evolutionary analyses of the origin of endosperm based on the constructs of inclusive origin diploid of fitnesstheory(kin selection) have focused on potentialfitness maternalendosperm benefitsof a maternal/paternal endosperm over a strictly ma-FIG. 6. and of Hypothesis theorigin earlyevolution endosperm for ternal embryo-nourishing female gametophytetissue in non-based on the assumption thatbasal angiosperms not have a dosecondfertilization event.Basal angiosperms wouldhave a diploid flowering seed plants (Charnov 1979; Westoby and Ricematernal endosperm thatrepresents continuation femalega- a of 1982; Queller 1983, 1989; Haig and Westoby 1988, 1989;metophyte development derivedfrom fusionof the two polar the Friedman 1995, 1998). These models for the functionalre-nucleiof thecentralcell. At a laterpoint, thecommon in ancestor placement of the seed plant female gametophyteby an en- ofof monocotsand eudicots,theparticipation a spermin theini- dosperm tissue for the purposes of embryo nourishment willtiation a triploid of biparental endosperm evolves. If it shouldturnout thatbasal angiosperms lack a second fertilization event,the need to be reexamined if it should be discovered that the ofhomology flowering plantendosperm would be withthefemale earliest manifestationof endosperm was a strictlymaternal ofgametophyte thelife cycle. (and not a biparental) tissue.
224 W. E. FRIEDMAN AND S. K. FLOYD In summary,although a triploidsecond fertilization event polarity and the potential for developmental transformationhas long been considered a synapomorphy for flowering indicated that the ancestral double fertilizationprocess wasplants (and was essentially firstreportedas such by Sargant likely to have produced a normal embryo and a genetically1900), it has yet to be definitivelycharacterized in any of identical supernumeraryembryo (similar to the plesiomor-the most basal angiosperms. This unanticipated realization phic condition in Gnetales). If the second fertilization event(more than a centuryafterit was assumed that double fer- in Gnetales and angiosperms is homologous, it follows thattilization was a general feature of all angiosperms) is the endosperm is likely to represent a developmental transfor-directresult of the interplayof new phylogenetichypotheses mation of an embryo (Friedman 1995).and analysis of thecomparativebiology of criticaland diverse The hypothesisthatdouble fertilization events may be ho-angiosperm taxa. This situation representsan enormous gap mologous in Gnetales and angiosperms rests upon two keyin our knowledge of the most basic aspects of fertilization assumptions: (1) double fertilizationto produce an embryobiology thatcharacterizedthe first angiosperms.It is essential and an endosperm was a featureof the common ancestor ofthat the developmental origin of endosperm be studied in flowering plants; and (2) a process of double fertilizationwasbasal taxa to unequivocally document or refute whether a presentin the common ancestorof Gnetales and angiosperms.triploid second fertilizationevent is a synapomorphic con- Clearly, if endosperm is not formedfroma second fertiliza-dition for floweringplants. tion event in basal angiosperms, the hypothesis that double fertilizationevents in Gnetales and angiosperms are homol- Double Fertilization: A Synapomorphy Seed Plants? of ogous must be rejected. This will be the case irrespectiveof the seed plant phylogeny that is favored (Gnetales closely The new seed plant phylogenetic hypotheses have clear related to angiosperms or Gnetales distantlyrelated to an-implications thatdirectlyrelate to the potentialhomology of giosperms).endosperm to structures found in nonfloweringseed plants. If double fertilizationis eventually shown to be a featureFor much of the last century,two dramaticallydifferent hy- of thecommon ancestorof extantangiosperms,theevaluationpotheses of endosperm homology have competed (Friedman of its potential homology with the process in Gnetales is1998). One hypothesisholds thatthe endosperm of flowering complex. Ultimately,however, "homologous features... inplants is evolutionarily homologous with a supernumerary two or more organisms are those that can be traced back toembryowhose normal development was transformed into an the same feature (or state) in the common ancestor of thoseembryo-nourishing tissue (LeMonnier 1887; Sargant 1900; organisms" (Mayr 1969). Even if Gnetales were conclusivelyHaig and Westoby 1988, 1989; Queller 1989; Friedman shown to be closely related to angiosperms, this would not1992a). Others have argued (Strasburger1900; Coulter 1911) imply that all of their shared features are necessarily evo-thatthe fusion of male and female nuclei associated with the lutionarilyhomologous. For example, it has long been hy-initiation of endosperm in angiosperms is not sexual in na- pothesized thatthe vessel elements of angiosperms and Gne-ture, but instead is a "vegetative fertilization" that serves tales are homoplasious based on the evidence that pittingto stimulate "belated" development of the embryo sac. As patternsand perforationplates in these two lineages are toosuch, endospermis viewed as a phase of female gametophyte dissimilar to representdevelopmental transformations an ofdevelopment that is evolutionarilyhomologous with the fe- original vessel element in a common ancestor (Carlquistmale gametophytesof all other seed plants. 1996). Recent research on the fertilizationbiology of members of Conversely, the hypotheses that Gnetales are closely re- the Gnetales appeared to have shed light on the homology lated to conifers and thatextantgymnospermsare the mono- of endosperm. Regular double fertilizationevents were doc- phyletic sister group to angiosperms do not necessitate the umented in Ephedra and Gnetum (Friedman 1990; Carmi- conclusion thatall shared biological featuresof Gnetales and chael and Friedman 1995). The product of the second fertil- angiosperms are homoplasious, as has been asserted recently ization event in Gnetales is a diploid supernumerary embryo by Hansen et al. (1999), Chaw et al. (2000), and others (for (Friedman 1992a; Carmichael and Friedman 1996). Com- an additional critique, see Axsmith et al. 1998). The general parisons of the presumed plesiomorphic manifestationsof conclusion that "shared morphological characters [of the double fertilization angiosperms and Gnetales demonstrate in Gnetales and angiosperms] are convergent,ratherthan ho- key developmental and genetic similarities(Friedman 1995). mologous" (part of the title of Hansen et al. 1999) is incor- In both groups, two sperm froma single pollen tube engage rect. Many, if not most, shared featuresof the Gnetales and in separate fertilizationevents with an egg and its mitotic angiosperms are evolutionarilyhomologous and representei- sisternucleus. The productsof double fertilization Ephedra in ther symplesiomorphic or synapomorphic features of seed (two embryos) are genetically identical (coefficientof relat- plants. Gnetales and angiosperms share homologous roots, edness = 1.0), as is the case with the two products of double homologous leaves, homologous ovules, and homologous fertilization (monosporic) angiosperms (an embryoand an in chloroplasts to name but a few obvious structures that were endosperm). inheritedfrom a common ancestor. Explicit analyses of comparative developmental patterns Within the context of the currentphylogenetichypotheses and genetic constructsassociated with double fertilization in for extant seed plants (conifers sister to Gnetales and mono- Gnetales and angiosperms are congruentwith the hypothesis phyletic extant gymnosperms sister to angiosperms), any thatdouble fertilization each of these lineages was derived in structure process hypothesized as homologous in Gnetales or froma common ancestor and is therefore homologous (Fried- and angiosperms must eitherbe a synapomorphyor symple- man 1994, 1995, 1998). Moreover, determination character of siomorphyof extantseed plants. For double fertilization, the
FLOWERING PLANTS-REPRODUCTIVE BIOLOGY 225fundamentalquestion is whetherthis process was (or could cess. Although double fertilizationmay occur in both thehave been) present in the common ancestor of extant seed Pinaceae and Cupressaceae (see above), there are no reportsplants. To evaluate this question, detailed and accurate in- of double fertilizationevents in cycads or Ginkgo. However,formationon the comparative fertilization biology of all ex- several studies have documented developmental events thattant seed plant lineages is essential. As will be seen, for all are consistent with the potential for double fertilizationof the recent activityin systematics,thereis currently much events in cycads and Ginkgo (reviewed in Friedman 1992b).that remains unknown about even the most basic aspects of In cycads and Ginkgo,anomalous egglike developmentof thethe reproductive biology in extant lineages of seed plants; sister nucleus of the egg (this nucleus participates in theand for now, therecan be no definitiveanswers to questions second fertilizationevent in Gnetales, angiosperms, and co-associated with the origin and evolution of double fertiliza- nifers) has been reported (Ikeno 1901; Chamberlain 1906,tion in seed plants. 1912; Sedgewick 1924; Bryan and Evans 1957). This sug- gests that the developmental conditions for a second fertil- Double Fertilization and Close Relationships of Gnetales ization event may well be presentin these much understudied and Conifers seed plants (Friedman 1992b). Given the hypothesisthatGnetales and conifersare closely Future documentation of a regular or occasional secondrelated (among extant seed plants), featuresof the reproduc- fertilizationevent in all major lineages of extant seed plantstive biology of Gnetales, such as double fertilization, might would be congruent with the hypothesis that double fertil-be expected to occur among conifers. Although largely ig- ization evolved in a common ancestor of extant seed plantsnored for most of the 20th century,reportsof double fertil- and is homologous throughout seed plants (Fig. 7). How- theization events in conifers do exist (reviewed in Friedman ever, if double fertilizationis ultimatelyshown to be absent1992b). These double fertilizationevents (although not well in cycads and Ginkgo and futurephylogenetic analyses up-documented) appear to be fundamentallysimilar to what oc- hold the hypothesis of monophyletic extant gymnosperms,curs in Ephedra. In Thuja (Cupressaceae), a second fertil- this would suggest that double fertilizationin Gnetales andization event, in addition to the fusion of an egg and sperm, angiosperms is homoplasious.may occur and appears to yield a supernumeraryembryo One importantpossibility that has been overlooked in re-(Land 1902). In Abies (Pinaceae), in addition to the regular cent discussions of seed plant phylogeny (given some of thefusion of an egg and sperm,a fusion between a second sperm currentuncertaintiesover the monophyly of extant gymno-and the sister nucleus of the egg nucleus has been reported sperms) is the hypothesisthatGnetales, conifers,and angio-(Hutchinson 1915). This extra fertilizationproduct also ap- sperms may comprise a monophyleticgroup to the exclusionpears to initiate embryogenesis. Others have suggested that of cycads and Ginkgo. Interestingly,if a conifer/Gnetalesfertilizationevents involving the sister nucleus of the egg lade was ultimately shown to be sister to angiospermsmightoccur in Pseudotsuga (Allen 1946) and Pinus (Cham- (among extant seed plants), double fertilizationand siphon-berlain 1899), both of which are members of the Pinaceae. ogamy (the use of a pollen tube to conduct nonmotile sperm Clearly, much remainsto be discovered about putativedou- to an egg) might prove to be key synapomorphies of thisble fertilizationevents in conifers. However, if futureanal- lade (Fig. 7).yses should firmlydocument that some conifers express adouble fertilizationprocess (occasionally or regularly), the Double Fertilization: An ApornorphicTendencyof Seedclose relationshipof conifersand Gnetales, and theputatively Plants ?identical patternof double fertilization(in termsof the pro-cess and the plesiomorphic production of two genetically An alternativeapproach to understandingthe evolution ofidentical embryos) would favor the hypothesis that double double fertilizationin seed plants may be in order. Irrespec-fertilizationin these two lineages is evolutionarilyhomolo- tive of the distributionof double fertilizationamong seed gous and was inheritedfroma common ancestor (Fig. 7). If plants and of the favored phylogenetic hypothesis for seed this was so, double fertilization yield two geneticallyiden- to plants, all extant lineages of seed plants exhibit three key tical embryos would almost certainly represent a synapo- developmental preconditions for a process of double fertil- morphy or symplesiomorphyof the lade that includes co- ization: (1) all extant seed plants produce two (or more) ge- nifersand Gnetales. neticallyidentical spermper pollen tube; (2) all (monosporic) extant seed plants differentiate genetically identical sister a Double Fertilization and MonophyleticExtant nucleus to the egg (one of the polar nuclei in angiosperms Gymnosperms and the ventralcanal nucleus in gymnosperms)thatmay per- The issue of whetherdouble fertilizationin the Gnetales sist throughthe time of normal fertilization and acquire egg-is evolutionarilyhomologous withtheprocess in angiosperms like characteristicsor be fertilized(Friedman 1992b); and (3)requires careful analysis of the interplayof phylogeny and occasional or regular entryof two functional sperm into athe often very limited knowledge of comparative biology. If single archegonium or embryo sac has been documented inextant gymnospermsare monophyletic,a findingof homol- conifers,cycads, Ginkgo,Gnetales, and angiosperms (Fried-ogy requires that double fertilizationbe a synapomorphyof man 1992b). Thus, it would not be surprisingif double fer-extant seed plants; and barring any loss of this character in tilization,per se, representsan "apomorphic tendency" (sen-extantseed plant lineages, it would be predictedthatconifers, su Cantino 1985; Sanderson 1991) of seed plants thatevolvedcycads, and Ginkgo would display this developmental pro- several times, predicated upon the fact that all seed plants
226 W. E. FRIEDMAN AND S. K. FLOYD monophyleticgymnosperms monophyleticgymnosperms paraphyleticgymnospermsI i I I I I Gnetales-coniferclade Gnetales-coniferLade Gnetales-coniferclade Gnetales Gnetales Gnetales ~ a a) a a a, a) a) a) a) ~ M c- w z 0 .2 0)~~~~~~~~~~~~~~~ - ) C) ZM -O_ 0 2 q 0 0 q00 ; - ADDS X~~~~~~~~~double fertilization Add/~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ y doubl fertilization double ertilIization (A) double (developmental developmental fertilization preconditionsfor C preconditionsfor double fertilization double fertilization a- - * double fertilizationunknown , double fertilizationdefinitely or possibly present double fertilizationabsentFIG. 7. Alternative for hypotheses theorigin of and earlyevolution doublefertilization based on theassumption basal angiosperms, thatGnetales, and some conifers have a secondfertilizationevent.(A) Underthisscenario, double fertilization assumedto have evolved isin thecommonancestor extantseed plantsand is homologous Gnetales,conifers, angiosperms. of in and Although doublefertilizationeventshave notbeen reported Ginkgo or cycads,thepotential double fertilization in for eventsexistsin thesegroupsand will requirefurther study. Underthisscenario, (B) doublefertilization assumedto have evolvedin thecommon is ancestor Gnetalesand conifers ofand separately the commonancestorof angiosperms. in Although is double fertilization homoplasious(and represents apomorphic antendency amongseed plants)underthisscenario, underlying the developmental preconditions enablethehomoplasious that evolutionofdouble fertilizationevents(the production pairs of male and femalenuclei thatare capable of engagingin fusionprocesses) are a ofdefining feature("underlying synapomorphy," textfordiscussion)of seed plants.(C) This scenarioassumesthatgymnosperms see areparaphyletic, monophyletic conifers sisterto Gnetales(supported sequence and indel data; L. Raubeson,pers. comm.),cycads are byare sisterto Ginkgo (supported some sequence data and indel data), and the conifer/Gnetales by clade is sisterto angiosperms. This ofhypothesis relationship was originally recoveredin the cladisticanalysisof Hill and Crane (1982), but has not been supported inmolecularanalysesto date. A sistergrouprelationship a conifer/Gnetales of clade to angiosperms (among extantseed plants)would thesupport hypothesis doublefertilization siphonogamy important that and are synapomorphies a conifer/Gnetales/angiosperm of clade.formpairs of both male and female nuclei thatmay participate lution of double fertilizationevents (involving pairs of spermin separate fertilizationevents (Fig. 7). and pairs of female nuclei that can behave as gametes) in If the evolution of double fertilizationis homoplasious various seed plant lineages may be the end result of a systemamong seed plant lineages, this phenomenon would stand as of fertilizationbiology that was established with the origina premier example of an apomorphic tendency predicated of the seed plant lade more than 360 million years ago.upon what has been referredto as an "underlying synapo-morphy" (Tuomikoski 1967; Swether 1983; Brooks 1996), in The Search for the Homologue of Endospernmessence, a case of parallelism thatresultsfroman underlyingdevelopmental constraintor bias (sensu Maynard Smith et If the process of double fertilization angiosperms should inal. 1985; Schwenk 1995; Wake 1996). The concept of an ultimatelyprove to be homoplasious with all other manifes-underlying synapomorphycan be broadly viewed as a de- tations of double fertilizationin seed plants, the issue stillvelopmental and evolutionarycapacity to produce a specific remains that endosperm must have an evolutionaryanteced-apomorphic trait repeatedly within a lade. This develop- ent or homologue. For more than a century,only two hy-mental and evolutionary capacity (the underlying synapo- potheses have been proposed for the origin of endosperm: itmorphy) to produce the apomorphic and homoplasious trait is either a homologue of the female gametophyteor a de-will have evolved once in the common ancestor of the lade velopmentally transformed embryo (Friedman 1998).that contains the various lineages exhibiting the homopla- If the endosperms of basal angiosperms are not the productsious trait.In the case of seed plants, a systemof fertilization of a second fertilizationevent, it must be concluded thatbiology thatinvolves the productionof two genetically iden- endosperm is homologous with the female gametophyteandtical sperm per pollen tube (a synapomorphyof seed plants) became a hybrid(biparental) structure subsequent to the or-that are broughtthrougha pollination process (another syn- igin of floweringplants (Friedman 2001a). However, if basalapomorphy of seed plants) into proximityto an egg and its angiosperms are ultimatelyshown to have a sexually formedgenetically identical sister nucleus representthe underlying endosperm, double fertilizationprocesses in nonfloweringsynapomorphy. The potentiallyiterative(homoplasious) evo- seed plants may yet provide critical insights into the origin
FLOWERING PLANTS-REPRODUCTIVE BIOLOGY 227of the endosperm of floweringplants-even if double fertil- female gametophytes could be interpretedas the result ofization arose independentlyin angiosperms, Gnetales, and functionalconstraints;the embryo-nourishingprogramof en-perhaps conifers.When double fertilization been reported has dosperm was likely to have been borrowed fromthe femalein nonfloweringseed plants, the product has always been gametophyteof the ancestors of angiosperms,irrespectiveofshown to be an embryo(Friedman 1992b). Indeed, it is hardly the morphological homology of endosperm (with an embryosurprising thattheproductof a novel fertilizationeventwould or a female gametophyte).Ultimately,at the molecular levelbe a manifestationof the plesiomorphic product of a normal endosperm may have hybrid origins: a functional (physio-fertilization event (i.e., an embryo). This may well have been logical) program coopted from the previous embryo-nour-the startingpoint for the evolution of a second fertilization ishing component of the seed plant life cycle (the femaleproduct in the angiosperms and their immediate ancestors. gametophyte) and a structural(pattern level) program thatAnalyses of the origin of endosperm based on the constructs was inheritedfromthe antecedentmorphological or life cycleof inclusive fitnesstheory(kin selection) have demonstrated homologue (either an embryo or a female gametophyte).that it is theoreticallypossible for a supernumerary embryoin the life cycle of a seed plant to acquire altruistic(nour- Conclusionsishing) behavior throughincreases in the inclusive fitnessof The questions of whetherconifers are paraphyletic,gym-a compatriot embryo (Charnov 1979; Westoby and Rice nosperms are monophyletic,or even whetherAmborella is, 1982; Queller 1983, 1989; Haig and Westoby 1988, 1989; in fact, the sister taxon to all other flowering plants (seeFriedman 1995, 1998). Barkman et al. 2000; Graham et al. 2000) will likely find In addition to theoreticalconstructs,there are new empir- definitiveresolution in the coming years. Perhaps what isical developmental data thatmay shed lighton the homology most importantabout the new, and in many ways, radicallyof endosperm. In vitro formed endosperm in Zea has been different hypotheses of seed plant and angiosperm relation- ofreported to exhibit a marked differentiation two poles ships is that these hypotheses have the importanteffectof(Kranz et al. 1998). These endosperms (formed outside of challenging old (and often static) concepts about characterthe physical constraints an ovule) typicallyforma globular of evolution and homology. Regardless of whethersome or allregion of densely cytoplasmic cells and a filamentousregion of the new phylogenetic hypotheses for plants are shown toof larger,more vacuolate cells. Kranz noted the embryo-like be robust or ephemeral, these hypotheses can and shoulddevelopmental propertiesof these endosperms. Additionally, directly stimulate new ways of thinkingabout the transfor-recent studies of endosperm development in diverse basal mation of characters,as well as focused studies of thebiology angiosperm taxa (Floyd et al. 1999; Floyd and Friedman of phylogeneticallycritical and often overlooked lineages. 2000) have revealed that plesiomorphic endosperm devel- Clearly, substantiveprogress has been made in the deter- opment in floweringplants is remarkablysimilar to the basic mination of phylogenetic relationships of seed plants and developmental patternsexpressed by embryos. The early on- angiosperms. Regrettably, these efforts have not been togenies of both embryos and endosperms in basal angio- matched by coordinate levels of activityin comparative bi- spermsinvolve unequal partitioning the first of cell, followed ology. Far too little is known about the most basic repro- by differential patternsof development in chalazal and mi- ductive features of extant basal angiosperms and nonflow- cropylar regions, or "domains." In fact, those principles ering seed plants; even less is known of thebiology of critical thoughtto govern embryo development in angiosperms (re- extinctlineages. In the absence of a rich and detailed knowl- viewed by Kaplan and Cooke 1997) appear to be equally edge of the comparative biology of key lineages of plants, applicable to the endosperms of basal angiosperms (Floyd the utility of new insights into phylogenetic relationships and Friedman 2000). remains limited. A commitment comparativebiology in all to Definitive resolution of the evolutionary origin and ho- of its manifestations now needed, fromdevelopmental mor- is mology of endosperm remains, as it has always been, com- phology to cellular and molecular biology. Only when knowl- plex and difficultat best. Nevertheless, there is reason to edge of phylogeneticrelationshipsis joined withthepowerful believe that a solution may someday be at hand. The recent insights of comparative informationwill it be possible to evidence of embryo-likefeaturesof endosperms in basal an- make significantprogress in reconstructing evolutionary the giosperms suggests that comparative studies of molecular and developmental historyof plants. expression in the endosperms and embryos of basal angio- sperms and the female gametophytesof nonfloweringseed ACKNOWLEDGMENTS plants could prove quite valuable. If it could be shown that gene expression patterns associated with early patternfor- We thank P. Diggle, L. Hufford,P. Stevens, and R. Rob- mation and morphogenesis in basal angiosperm endosperms ichaux for suggestions of ways to improve the manuscript and embryoswere similar,these data could supporta finding and L. Raubeson, P. Crane, and C. DePamphilis for most of homology of these two critical components of the angio- helpful discussions. This research was supported by a re- sperm life cycle. search grant from the National Science Foundation (BSR A comparative molecular developmental approach might 9816107) to WEF. also be fraught withpitfalls.Comparisons of gene expression patternsin endosperms of basal angiosperms and the female LITERATURE CITED gametophytesof nonfloweringseed plants mightalso reveal Allen,G. S. 1946. Embryogeny development theapical mer- and of much in common. However, similarities in molecular ex- istemsof Pseudotsuga.I. Fertilization and early embryogeny. pression patternsin endosperms and nonflowering seed plant Am. J.Bot. 33:666-677.
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