THE USE OF PHYLOGENETIC Monson- Russell K. PERSPECTIVE IN COMPARATIVE PLANT AND PHYSIOLOGY DEVELOPMENTAL BIOLOGY^ Abstract development The use of phylogenelic reconstruction for the testing of comparative hypotheses is a recent in the fields of plant physiology and developmental biology. In this review, several u^es of phylogenetic information are discussed, indepenrlence phylogenetic choosing experimental systems, justifying the statistical including the use of trees for (1) (2) of compared taxonomic groups, identifying evolutionary direction using outgroup analysis, and (4) studying the (3) evolutionary tempo of physiological and developmental change. Difficulties are also discussed, especially with respect phylogenetic constructing to mapping continuous, physiological traits onto the discrete, binary structure of trees, (2) (1) trees from traits that are independent of the physiological and developmental characters being map[)ed, an<l (3) re- specting the statistical nature of phylogenetic trees. The bulk of the review is devoted to several examples from the power phylogenetic perspective comparative studies. Reviewed examples include literature thai illustrate the of a in elucidation of a novel pyrophosphale-dependent phosphofructokinase in the glycolytic pathway of phosphate-stressed (1) endosperm angiosperms, adaptive plants the Brassicaceae, evolutionary pattern in the origins of polyploid in (3) in (2) radiation of Hawaiian Island plants into dry habitats, and (4) evolutionary pattern in the origins of C4 photosynthesis. common merge The fields of systemalics, comparative physiology, and developmental biology will continue to as their on phylogenetic perspective increases. reliance The purpose of this review is to describe aspects Sweden with Turreson (1922) and in the United The Clausen focus of the past, present, and future relationship be- States with et al. (1940, 1948). — embedded com- was evo- tween two disparate disciplines of these studies firmly in tlu' historically parative plant systematics and comparative plant lutionaiy process: to uncover the cohesive and di- physiology and development. Researchers in plant vergent forces that maintain the structure of taxo- same systematics focus on the pattern of evolutionary di- nomir units while at the time allowing for A compo- Researchers in plant physiology and diversification and speciation. principal versification. comparisons developmental biology focus on the products nent of these early studies included plant — mccha- among plants from different geographic locations of evolutionary diversification functional common The nisms, structural attributes, and their relationships that were grown in environments. goal "common-garden" was genetic and environmental controls. The nexus pursued in these studies to to and environmental among these disciplines occurs through a need to partition the influence of genetic During understand the role of evolutionary constraint in influences on character expression. the modem and dictating patterns of adaptation, the timing and rale birth of comparative physiology, to a of phenotypic evolution, and the evolutionary in- lesser extent developmental biology, scientists dis- same common-garden approach among covered the phenotypic that teractions traits. one can recognize several connec- could be used to standardize the influence of en- Historically, between comparative systematics vironment, while observing inherited differences in tions the fields of & Mooney and comparative functional biology. As examples, the adaptive responses of plants (e.g., & Bjorkman Holmgren, Fur- numerous 1961; 1963). consider the studies that originated in Billings, comments, and unpublished material provided by Ray Huey, The author grateful for the thoughtful discussions, ' is Michael Grant, Manuel Ionian, William Bowman, Ned Friedman, Richard Olmstead, Robert Rohichaux, Bill Plaxton, and Richard Suzanne Warwick, Todd Dawson, and Paul Teese. Special thanks are due to Michael (Jrant, Brian Farrell, Olmstead for their helpful collaboration in providing the Flaveria phylogeny. Thanks are also due to the sponsors and Agenda 2000 and Organizing Conunittee of the Missouri Botanical Garden's 41st leaders of the Systematics effort the NSF BSR- Annual Systematics Symposium. The author's research discussed in this paper was supported by grants 8604960 and BSR-8911433. Colorado and Organismic University of Colorado, Boulder, Department Environmental, Population, Bioh^gy, ^ of 80:?09-0334, U.S.A. Ann. Missouri Bot. Gard. 83: 3-16. 1996. 4 Annals of the Garden Missouri Botanical ihcrmore, by choosing congeneric and confamilial witli process of natural selection (Feder, 1987)? llic groups for their comparisons, these mechanistic hi- Pattern is typically measured as tfie functional at- were ologisls using phylogenetic perspective as tributes of organisms native to different environ- common they observed the products of descent, ments. If the pattern correlates with enhancement examples identified of convergent evolution, and of growth and persistence across an environmental isolated patterns of adaptation. Thus, incep- at its gradient, {\wn the pattern ascribed to natural se- is modem tion, comparali\c plant pliysiology had de- and lection taken as adaptive. Recent is studies, fmitive links with comparative plant systematics. however, liave revealed phylogenetic history to hv. Unlike researchers comparative in systematics, as liktdy a constraint on pattt>m variation as nat- is howevcr, the focus of comparative physiologists was & ural seh^ction (Huey, 1987; Garland Carter, not the evolutionary procc^ss in relation to natural 1994; louder et al, 1995). Disentanglement of laxonomic units, but rather the nature of media- phylogeny and selection only accomplished is nistic adaptations and their relationship to envinm- through reliance on comparative systematics and mental extremes. the existence of accurate phylogenetic reconstnic- Since these pioneering studies, 'hers in tion. Th<^ integration of comparative systematics physiology atid developmental biologj' have strayed with comparative pliysiology and development is i from their phylogenetic, comparative em- mapping origins, exercise in functional onto estah- traits bracing instead the implicit assumption that func- lished phylogenetic Several methods have trees. tional resp(mses to the environment are the prod- been develo{Hul accommodate such mapping and to When ucls of natural comes selection. accompanying the it to statistical analysis (Felsenstcin, inten>reting evoIulionar> patterns in functional 1985; Harvey Pagel, 1991; Brooks McLennan, *& *S. orm 1991). and adherence to intuition to an adaptational doc- TIktc are some must potential pitfalls that l)e trine. This tendency has been criticized in past es- recognized before one can successfully engage in & says Gould The (e.g., Lt^wontin, 1979). potential the activity of phylog<*netic mapping. For examph\ contributions of phylogenetic reconstnu'tion and many comparative physiologists and developmental the comparative method formal hypothesis may to test- biologists not recognize the tentative nature of ing in physiological and developmental biology phylogen<Mic trees. Al appearance, such first trees have only been recently n^visited (e.g., Felsenstein, refled firm, dt^finitive relationships, especially from & 1985; Huey, 1987; Harvey Pagel, 1991; Garland the pt^rspective of mechanistic who biologists are & Lauder Carter, 1994; et al., 1995). There accustomed observing is little to the discrete conclusions doubt more become that as biologists aware of the of manipulative experiments. how- important, It is useful deductions that can be made using phylo- ever, to recognize the statistical nature of phylo- genetic data, a remarriagt^ be witnessed A will be- genetic trees. phylogenetic tree is essentially the tween the fitdds of comparative systematics and solution of gn^atest parsimony, given knowledge comparative physiology and development. about a particular set of measured, shared traits among an assumed many set of related taxa. In On tmk Different Natures of Comparative ^^^^^^'^ ^"^*' *^'<>"'^iructed from assumptions of max- ** imum parsimony svstkmatics and compakative will poorly reproduce the alleged & Pmysioeogy/Development phylog(uiy (Fiala Sokul, 1985; Rohlf 1990; et al., Lamboy, 1994). Phylogenetic trees have conclusive comparative In systematics, trait variation is confidence limits that should be honored when used study among to natural relationships different framing ionclusions about evolutionary patterns. groups of organisms. In comparative physiology and As second example a of dealing with phy- i* development, among natural relationships organ- logenetic mapping, comparative physiologists ant 1 isms are used study the nature and to functional Icvelopnu^ntal biologists must recognize disparities significance of traits. Thus, although researchers in in the nature of traits that are frequently studied. both draw upon same fields the puzzle pieces (van- Comparative systematics based on the use of is dis- ation in organismic traits), those in one discipline crete, binary traits, the raw material of cladistic use the pieces to assemble the puzzle, while those constniction. Comparative mapping of physiological in the other discipline use the completed puzzle and developmental to traits also requires that they study the pieces. have clearly delineated limits. There are examples In focusing on adaptation, comparative physiol- of such traits (e.g., the presence or absence of the ogists ask the question: does physiological variation C, pholosynthetic pathway), though physiolog- itiost among organisms show a pattern that consistent and is ical trails, to a lesser extent developmental Volume Number Monson 5 83, 1 1996 Phylogeny and Comparative Plant Biology max 20 I C/) CN 18 I 16 - o 14 - 12 0) 10 CO CO 8 C/) 0) 6 4 - CO o 2 o 200 400 600 800 1000 1200 1400 1600 1800 2000 2200 0. Photon m"^ density flux (lumol s"^) grown Figure Hypothetical responses of photosynthesis rate to incident photon flux density in a high-light leaf 1. (H) and a low-light grown leaif (L). The results demonstrate variability in photosynthesis rale as a function of the immediate (or instantaneous) light environment and the past (or growth) light environment. One commonly used index maximum of photosynthesis rate in studies of genotypic differences is the photosynthesis rate (A,„^J. maximum com- measured are continuous and show plasticity in their of a trait is at its for all traits, measurements responses the environment. This leads pared taxa, then variability in the to to diffi- mapping. As an example genotypic differences. In practice, difficul- culties in the process of reflect and one determining the species- -spe- consider the case for photosynthesis rate, of the ties arise in trait maximum most commonly studied characters in comparative cific conditions that foster expression of physiology. Within a plant, maximum photosynthe- a trait. For some traits (e.g., resource acquisition maximum may come rates can vary considerably (by up to a factor rates) expression with envi- sis maximize where- of 10) among leaves that develop in different parts ronmental conditions that growth, mechanisms of a plant's canopy (e.g.. Fig. By studying the as with other traits (e.g., of stress tol- 1). may come und environmen of such variation comparative physiologists erance) it tal can gain insight into interactions between the pho- conditions that minimize growth. and environment, One issue deal with in terms of phylo- tosynthetic process a plant's in final to this case the light environment. Yet this same vari- genetic mapping is the need to construct phyloge- ation creates difficulties in assigning discrete char- netic trees from traits that are not mechanistically acter values for phylogenetic mapping linked to those being mapped. This concern is min- In some way, the influence of environment on imized when trees constructed from molecular character expression must be standardized. Phylo- markers (though one can imagine gene sequences genetic reconstruction only meaningful the in which molecular variability is reflected in en- is if mapped genotypic comparisons with- zymatic variability). Trees based on morphological traits reflect Lack out environmental influence on character variabil- traits carry greater risk in this respect. of in- One way commonly accomplished dependence between used in tree construc- this in traits is ity. comparative physiology compare tion and those mappt^d onto the tree would decrease studies of to is maximum observed values some process the likelihood of reproducing the true phylogeny for for (e.g., mapped A„,^ in Fig. 1). It is reasoned that if the expression the trait. 6 Annals the of Missouri Botanical Garden On Specific Issles That Can Bk Addukssed plet.-Iy iiiilciH^ndent in terms of past history. There UsiN(, A PiiV!.()(;KNK'nc Pfmspkctivk always -oing be some degree common, is to of hi- erarehieal deseciil system hy in a i'haraeteriz(Ml a L niYl.OCKNV AND THE CHOICE OF EXPEKIMKNTALTAXA monophiylei ti-e eli adi ogram. rhyl,ogeneli• e conneeti• ons Phylogeiiies ean he used provide interfere witli stalislical assumptions of indepcn- to direction in — & dence ttie ('hoi((^ of experim(Milal systems allowing for (CIutlon-Bn»<'k Hai-vey, 1984; Felsenstein, & tlie ehoiee of taxa that are closely related or mon; 1985; Martins Garland, 1991). Basically, lliis is ^ "degrees of fn^Mlom" becomes distantly relal<'d. This allows investigators max- issu(* that es- to imize the possibility that being compared p^'cially relevant in attempts to construct correla- tht^ traits among common tions eo-occurring are the j)roducts of descent in the ease of traits or relate tin* ex- closeOy n^lated groups, or convergent evolution pression of a trait with environmental variability, in the case of distantly related groups. Through the a ^Y ignoring phylogenetic relatedness, investigators priori choice of groups with contrasting phyloge- tt^nd to indale iht^ potential for Tyi)e I errors (wrong- netic patterns, investigators ean study ^"' n*jeclion of llu* null hypothesis), reduce the relative tlu* roles of {)hylogenetic inertia versus selection p^^wer of their statistical conclusions, and increase in in- fluencing evolution of functional inaccuracies in (estimating cumulation coefficients th<* traits (Martins Garland, The Traditional choices of experimental systems 1991). only groups that in Sii imnmne comj)arativp functional biology have been (hiven by apf)ear to he from such phylogenetic influ- ^nces <'(msiderations of environment (Huey, 1987; Lauder are those characterized by early diversifica- et al., 1995). Witli respect to plants, the paradigm *'<*'' foll*»w<Ml by long periods of phylogenetic stasis of choice has staled that adaptive responses vn- (so-called '^star" phylogeuies in Felsenstein, 1985) to & Mailins Garland, vironiiH^nt an^ best observed in extreme habitats. (^*'^' 1991). Thus, adaptive responses high Sevt^ral methods have been propostu] deal with to temp<*rature are to probh'ms The best studied in hot, desert habitats, whereas adap- *''*' of {)hylogeri<etie interd<*pend<Mice. live nvsponses to cold temperatures are best studied ^iniph^st tm^hod, though not ihv most accurate, is in cold, luniha environmt^nts. This approach con- center the analysis on higher taxonomic units, ^^^ which lains a compelling dose of intuition and How- will {)resumably possess weaker phylog<uietie logic. ev(M-, also perpetuates some dang(Mous and short- interdep(Midcnee in terms of the traits they exhibit it & sighted assumptions. One principal assumption (Crook, 1965; Clutton-Brock Harvey, 1981-). This is nu'lhod does that any intuitively b(^neficial aspect of a functional not comj)letely doa] with the issue of attribute the product of sidection response phylogtMietic connections, however, since even the is in to the most eonmion, and higher levels will be inli.rdeptaidenl some de- jH>l(Mitially stressful, envi- to ^" ronnuMital extreme. A coroUar)^ assumptii>n a[)proach that deals more directly with to this S^^^- is that, with rtvspecl to inllut^iees on phenolype, phylogenetic connections was first proposed by Fi»l- selecli<»n in a plants curnMit environment has over- senslein (1985) and modified in various ways by & Huey shadowed historical events in the acquisition of (>th(Ts (t\g., Bennet, 1987; Grafen, 1989). trails from past ancestors. These assumptions I'^ essence, this approach takes advantage of ex- fecvl the adaptationist program discussed above. This {H'^'lt^d variance of character change to compute current enviromnent-oriented approach standardiz<Ml, independent contrast valu(\s from the lias little measunnl comparative Such t)rovision for phylogenetic constraint or <lata. contrast values inertia. This is where a phylogenetic perspective can con- *'^" *'**'" ^^^ subjecleil to standard statisti<'al tests Even tribut<> to adaptive analysis. By choosing groups <*f significance. with this approach, how(?ver, based on criteria of botli environment an<l the avail- uncertainties exist due to limited knowledge about ability of phylogenetic reconstructions, one can phylogenetic branch lengths and th(Mr relationship — and conduct truly synthetic analyses of the relative ^h*" ^'^^^^ pattern of evolution specifically, (1) ^'^ roles of selection versus phylog<»netic constraint, vvJiether trait divt^rsificatiim has occuit<m1 in a grad- & and (2) the relationship of traits to the curn^nt \ci- ^''^^ ^*'" pnnctuat(Ml palt<^ni (Marlins Garland, ms past environment. 1991). lMiVEO(;ENY AS A (;UinE TO STATISTICAL ANAIA'SIS PliVI.()(;ENY AND THE DETERMINATION OF EVOLUTIONARY PATTERN „, , . 1 . , , hylogenetic relationships ean be used to justify 1 among statistical patttMus experiim'utal groups be- maps Phylog(Mietic trees represent from which ing compared. an unatlainabh* goal com- one can It is for polarize patlt^ns of adaptive diversifica- parativ(^ biologists obtain groups com- to that are tion. Polarization involves determination of the se- Monson Volume Number 7 83, 1 1996 Phylogeny and Comparative Plant Biology o o I CD c5 2 3 4 5 6 1 Species 2 5 outgroup (W) outgroup (W) D Figure Hypothetical water-use efficiencies measured for six different plant species (upper panel). The lower two 2. trees demonstrate how evolutionary patterns in this physiological character can be polarized with respect to ancestral and derived traits using outgroup comparison. In both cases the outgroup is assumed to occur in wet habitats (W). Those species exhibiting lower water-use efficiencies are assumed to also occur in wet habitats, whereas those that found exhibit higher water-use efficiencies occur in dry habitats (D). In the tree on the left, a single transition is to on occur as species radiated into dry habitats and evolved higher water-use efficiencies. In the tree the right, a transition has occurred early during diversification of the group, followed by a later reversal. By quential origins of traits relative to patterns of tax- between, or among, multiple traits. simulta- onomie diversification. The origins of traits are neously mapping two or more traits, one can gain how appearance one polarized through comparison with ancestral out- insight into the evolutionary of may appearance Without outgroup impos- have influenced the of a dif- groups. polarization, trait it is appearance sible to determine whether a trait represents the ferent trait. Alternatively, the of traits phylogeny can be mapped simultaneously with major ecolog- ancestral or derived state. This use of is illustrated in Figure 2 for a hypothetical study of ical shifts (e.g., shifts in habitat type, phenology, or photosynthetic water-use efficiency. Without phy- community structure). With respect to plants, this may deducing determine approach be particularly useful in logenetic analysis, not possible to is it and whether high or low water-use efficiency represents the relationships between functional life-his- the ancestral state in this group of species. Two tory traits, as well as between functional and struc- each altemative phylogenies are presented, of lural traits. which conclusion concerning The use of phylogenetic trees for the study of leads a different to most funda- evolutionary patterns represents the the evolutionary pattern in this trait. between In addition to polarizing single traits, outgroup mental of all symbiotic connections the and and phylogenetic mapping also provide a disciplines of comparative systematics corn- analysis This the connection means studying the evolutionary interactions parative functional biology. is for 8 Annals of the Garden Missouri Botanical that is destined to draw llie most attention from eesses. It is not uncommon to find investif^ators romparative physiologists and developmental hiol- 'iiing an entire j^tMrns to determine the extt^nt As ogisls. is evident in the following sections, this of (hstrihution in some functional or trait idt^ntify approach has gnvit power to provide new insight possible comparative systems which in the trait dif- into the processes and patterns of functional ad- fers. Sucli an approach has heen taken, exam- for i»P*^**'''"- in the identification of Clilorclla species pos- I>1^, sessing the ability to utilize l)icarl)onale as an RECONSTRlCTiON AND I'JIYLOC.KNI-TIC TIIK inorganic carbon source (Miyachi 1985) and et al., DKIKKMINATION OF TIONAKY TFMPO KVOI.l the assessnu^nt of phytochelalin (heavy-metal bind- ing j>cptid(*s) distribution within various gn>ups of With appropriate* calibration, phyIog(*nies can Ix 1/ plants (Ce^keh'r et al., 1989). Re(U)ffnition of nhy- f ,• f .• usedI .to assess rat. es of evol1ution, liat. es of evol1 ution I . 1 w logenctic pattern in the distri1bution phvtochi;m- of ca,n., p. iovHtI e *insi•gl1it» *uil. o patterns ofr ad]apt.i• ve ra(1h-- 1 , r icals ihas exi. sled for many years. In phvto- fact, ,• aluin andI t.1hei' r und1erl1 yi• ng processes suchI . ^' as nat- ' 1 ,-1 m 1 • 1 i- -i . chemical distribution represents foundation for .u.r,.a,l1 sel1 ect,•ion and1 gi'uctic -n Temporal1 cal,i.,bra- llu* drift. * , , cheni((syst(^matics, a central discipline within the of phylogenies can be accomplished lion through broader comparative many fiehl of systemalics. In paleontological dating, the use of mohn^ular clocks L instances the ch(MTiicals of systematic interest also A J inn'i\ r (e.g,r., deli\e.?e..i- e.t. at., lvv»>), or t»itie appluat»i• on ofr sl. a- 1 . 1 . have roles in plant adaptation. Tcrpenes and alka- based listi<"ally trajectory moch'Is to the variance example, loids, for exhibit strong phylog<Mietic af- among rneasunul characters Lande, 1985; (e.g., ill loon '^ finities and serve an adaptive role in tlctcrring her- fLy^n.,cwl.il,? lIoVolr/^U.; lIuVta..i.li:u.i.s, IWl). tilie use ofr diat/c<i1 |)uhy-' I 1 • /r. & bivory (BaiUh, (»rpe Ch, arl, wood, 1980; Lerdau Lwr.^.w.o et logerues (leMive temjioral1 pat»t.i^rns r evol1 ut.•ion • of in t*» ^ i t\ ammonium 1994). Quat(»niaiy and '"•- tertian' sul- Al.u»n.c..'il;io..n,a.l1 It.i-a.i:.ts Il.ias notI 1been great.. T^ilure are sev- 1 1 . compounds i- fonium ,' are distributed const^'va- alonii; er,.a,l1 com„p.le1 xities ,1 , ,-11 need1 resol1 uti• on 1 r llial still bt^fore • 1 • i- ^ ^ive plivilogenclic lines and have impoilant roles in ri ¥7 s..u.,chI, u.se I• S !ik(»Ilv ,to incn\isc. For exampl1e, mol1ec- 1 responses and water (Rhodes .III . to salinity stress ,u.lia„i, ,c.lro,,c.krs. a,„r,e, \t,y„pi• cally based1 on neut.ral1 , i','^^"*..,.. trails. o & ., 1 Hanson, . Numerous examples 199.*}). other of r .. Ihuvevei, most 1 . . is likt^ly that tunctiona„l, traits it . . ' ,1 i)livtocliemicals have dual impoilance com- „ that to Iliav(% a„t. sonu^ t,-ime i• n .t1hei• r past, been t.1he subIjt• ^ct T.I ' — . . . parative systemalics and comparative ,s physiolojiiv mav hJ ot sel1 ect1;ion.. a process t1IhaiI 1have accelerated t J .» » .1 1be diescrir»ed1 flavonoids. cyano^enic (e.g., ^'t*'! ffly- ^.,.j. .' * pvolutionaiy ch1 ang<^ rel1 ative to neutral markIers. hi t • n * cosid<1's). lu all these examples t1he systematic ap- AAddI iit;»i;on.a.l,1l1y, itiliere are uncert*ai•nties i* n .t1he cl1 oc1ks * * -^ , , , , , , . |)roach lias playe<! an obvious role in ex|)andiug the themselves and their application ^•.•t•o 1j)h1yl1og<.uieti( of species possess chemical Ti ^^^^ that th(* of inter*^st ,n.^.wc.,o.n.,st*r.-u..ctfi' ou. these unceilainties include lietero- 1 • 1 i- ^"^" <*stabbshing con-elations between taxonomic k *'^ g.<..*.n.cwiolMy, ;i«n 4tln. c. l..a.t»e. olf n..ucl1eot4i- dIe base sub1 st.i*.tut.•ion and, , . ,. f, . eculogic distributions. DNA depeii(hiig on the environment (Saccoiu* et One rec<MU which knowl- cas(» in phyl()g(Mi(Mic due ah, 1989), (MTors to interactions bi^tweeii the edge lias had an obvious influence on discov- trait choice of iiuchH)tide setjuence and the method of '<"»«'''.« nnhu-.I.Ir & 7"^ llu- pyn>plH.spl,Ml.'-<l,.|u.„- Uvr ivconslnu-tio., (Zlunklkh Li, 199;?). an.l the pli-sphofructokinasr was '''*"' that recently i..fluonrc of c.-,1ain funrli..>ial traits gnu-ra- (e.j^.. ""f""""' '" ^^"''"''' "'^''" ^^ ^'"'' ^''*'"- ^^'^ '^- J" lion lin.r a.ul nu-talx.lic on rat,-) nu<l.-<,ti,le snl.sti- * Thoodorou ami '''^''"•"' ^"^"^'^^ mtioM ^'^'^^^- rates (Ma.lin&Paluml)i, 1993). If. uch com- '. "' Plaxton suggested enzyme (1994) that conft^rs tliis [)h^xities can be resolved, evolutional clocks could an adaptiv<' advantaii:e under ^pnhwo.sn|h«autitu* rs^tmrae:s^s buvv become .' ^ ^^^^^^^ 1 val1 uab1 lI e .tool1 s as comparative bI i- ol1 ogi•sts ad,- ' ^^'""- fnu^tose 6-phos- «'><-'>^>'''' l"«>---i"S <«f <lress issue of future environmental change and llu. '" ''"" "'" '^'^^^' ^vailahility. Fol- ^'''''\ evolutional its iullucMK-e patterns in the Ea.lh ().. s 'T^^"^'"^ P'^"'" lowing a protocol typical of comparative^ physiolo- j^j^jl^ gists, Plaxloirs group recently screened other plant species assess to overall distribution of the induc- On thk Use Of Systematic Infokmatu) N ibh' t^nzyme Plaxton, Queetrs (\^' Univi^rsity, pers. Systems fou Discovkhy and Inventory of riiF comm.). TluMr search reveahnl presence its at n^l- AND UNI(^)rF RlOCIIEMlCAL PHYSIOLOGICAL atively higli constitutive levels tobacco and in to- Processes mato cells, but the absence of plu)sphale-stn»ss in- Phylogenetic trees provide maps of historical ducibility. A similar pattern of constitutive among groups As linkagf^s of organisms. with any presence, without was iuducibility, f(»und other in map, i)hylogenetic trees can provide direction and lirassica species thought be to closely allied with orienlalion for searches of unitjue fuiK'tional pro- m^ra and li. (e.g., R. olcracea L. B, rapa L.). Thus, Number Monson Volume 9 83, 1 1996 Phylogeny and Comparative Plant Biology appeared that the induction mechanism was iso- merous cases of triazine resistance have been re- it lated B. nigra, being absent even from conge- ported in A, powellii S, Watson and A. hybridus L., to American ners. At this point Plaxton's group initiated discus- the two less widespread species of North sions with Suzanne Warwick, a systematist who had weedy amaranths (Hill, 1982). Triazine resistance recently constructed a phylogenetic tree of fira^^ica has only been reported in one population of the cpDNA and related taxa through the use of markers more widespread species, A. retroflexus L. Although & (Warwick Black, 1993). From the molecular phy- the data are incomplete, there is reason to hypoth- logeny was clear that 6. nigra more closely esize that the two minor species will usurp the eco- is it with three members of the genus Synapis, logical dominance of the widespread species in the allied than Brassica Plaxton's group has recently face of continued heavy herbicide use (see Gressell (Fig. 3). & surveyed the two species oi Synapis, 5. alba L. and Segal, 1982). This issue is complicated by the 5. arvensis L., which appear to share close affinities fact that European populations of A. retroflexus ap- with the re-aligned B. nigra. Both Synapis species pear more likely to develop triazine resistance com- exhibit the inducible pyrophosphate-dependent pared to North American populations, a situation common weedy themselves phosphofructokinase. to species that find out- & This example provides three important conclu- side their native ranges (Gressell Segal, 1982). sions concerning the use of phylogenetic trees in This problem begs for the inclusion of a phyloge- studies of comparative physiology and developmen- netic perspective. The question of whether one spe- tal biology. First, it is clear that phylogenetic trees cies is more or less constrained by its phylogeny to would appear be can be useful in directing the search for novel bio- evolve herbicide resistance to fun- and and developmental damental understanding predicting future chemical, physiological, pro- to cesses. Second, this example illustrates the poten- patterns In biological responses to herbicide appli- two-way exchange of information in collaborations cations, tial between systematists and functional biologists. In On THE Use OF PHYLOGENETIC ANALYSIS TO pyrophosphate-de- case the distribution of the this EVOLUTIONARY Patterns Plant independent DISCERN pendent phosphofructokinase provides in DEVELOPMENT AND FUNCTION support for the taxonomic realignment of B. nigra as suggested by the molecular phylogeny. Finally, Phylogenetic trees provide comparative biolo- should be clear that the effective use of system- it gists with an important tool to uncover and polarize information systems by comparative physiolo- atic Through an evolutionary pattern in functional traits. and developmental biologists requires that gists examination of pattern comes insight into the evo- The taxonomy phylogeny. fact that B. nigra -a reflect in l J n *u T ,lut.iouary const^ ra•mt^s that» have mnuenced,i and will \ ;. . ^^ 1 ' was with Brassica, rat1her traditionally classified n r *u ^ conti. nue ,to i• nnuence, lunct»i• onali responses .to the caused1 1 • 1bi• oc1hemi•cal1 search ^ than with Synapis, this n u ^ / envi. ronment.. tIn *tih, e rtollowi• ng paragraphs examplies . stray from the correct phylogenetic path. to are provided to illustrate the use of phylogenetic One area which a phylogenetic approach in is study evolutionary patterns in plant phys- trees to currently missing, but potentially beneficial, is the and development. iology study of herbicide resistance in weedy, agricultural In the past 25 years has become obvious pests. it EPHEDRA AND DOUBLE FERTILIZATION that the continued use of herbicides on agricultural has resulted in the evolution of several her- For many years was thought that a defining fields it weed species (Warwick, 1991; Holt of angiospenns was the process of double fer- bicide-resistant trait Friedman has 1993). Apparently, there considerable in- tilization during reproduction. (1990) et al., is dogma and interpopulation variability in the recently challenged this through definitive terspecific Hkelihood of evolving herbicide resistance. un- observations of double fertilization in Ephedra, a It is known what such due non-flowering seed plant. Phylogenetic trees con- extent variability to dif- to is from numerous including molecular ferences in selection regime, population genetic structed traits, A member Ephedra structure, or phylogenetic constraint. systematic markers, have placed as a basal approach would be of obvious benefit in partition- of the Gnetales, the group of extant non-flowering angiosperms ing the influences of selection versus phylogeny, seed plants most closely allied to the & though date no such approaches have been at- (Doyle Donohue, 1986). Using these phyloge- to tempted. An example of the potential use of com- netic relationships as a guide, Friedman (1992) was parative systematics the question of herbicide able to demonstrate that the likely homolog to an- to endosperm supernumerary-embryo resistance can be seen in the case of triazine re- giosperm is the Ephedra Amaranthus. Within North America nu- product of the second fertilization In (Fig. sistance in 10 Annals of the Garden Missouri Botanical Brassica rapa Brassica oleracea Brassica bourgeaui Brassica incana Brassica iiiiarionis montana Brassica Brassica cretica Brassica insuiaris Brassica rupestris Brassica defiexa Sinapis auciieri Brassica oxyrrtiina Brassica barreiieri Brassica repanda Brassica desnottesii Brassica gravinae Brassica e iongata Brassica nigra Sinapis anfensis Sinapis aiba Brassica fruticuiosa maurorum Brassica Brassica spinescens Sinapis pubescens Brassica tournefortii Figure among 3. Plivlogeiu'tir relationships nu-nilx'rs of suhliil..' Rras.siriiiar ((:rurif<'ra(% tribe Brassiccac) based epDNA on resUiclion mapping. The tree has been ''pruned" from the more eomjtietr analysis presented Warwick in and Hiaek (1993), sueh thai only species in Bnissica and Si/uipis are shown. The arrow marks the eurrentlv nown k distribution of (he inducible TPi-dependent phos[)horruelokiiiase as determined by ^, (Queens l^laxlon lJniv<*rsity, Ontario, pers. eoimn.). Number Monson Volume 11 83, 1 1996 Phylogeny and Comparative Plant Biology oi en c: CO CD cts CO O CD :3 c: c: CD i& CD GAMETOPHYTE REDUCTION OF FEMALE TO EMBRYO-SAC FORM OF 2ND FEMALE NUCLEUS ADDITION TO 2ND EVENT FERTILIZATION PRODUCT OF 2ND MODIFICATION FERTILIZATION NON-EMBRYO INTO TISSUE PRODUCT PROLIFERATION OF 2ND FERTILIZATION SUPERNUMERARY EMBRYO INTO DOUBLE FERTILIZATION Figure Phyiogenetic mapping of double fertilization and the evolution of polyploid endosperm in the Anlliophytes, 4. ncluding the Cnetales {Ephedra, Gnetum. Welwitschui). the fossil groups Pentoxyion and Bennett itales, and the angio- 1 sperms. Following observations by Friedman (1990, 1992) it is eoneluded that double fertilizalion oecurs [)rior to Redrawn from divergenee of the angiosperms, but the evolution of polyploid euidosperm oeeurred after divergence. Friedman (1992). Baldwin and The supernumerary embryo functions nourish preference onto the phyiogenetic tree to 4). — been the primary embryo an act of apparent ''altruism" Robichaux (1995) concluded that there have that raises questions about the role of kin selection at least five independent transitions from ancestors the evolution of developmental pathways (Fried- occurring in wet habitats to the derived species oc- in cumng man, 1992). in dry^ habitats. Adaptation to dry habitats known morphological include in this alliance is to vnoN THE HAWAIIAN ISLANDS A[)APTIVE RAD! energy IN ^nd physiological that influence leaf traits conduc- chmensions, stomatal t^^l^"^^ ^^^^ (^S- between Robert Recent collaborative studies tance, and leaf surface properties that regulate solar and Robichaux comparative physiologist ecolo- (a and physiological that influence -eflectance) traits and Bruce Baldwin comparative moleculai (a gist) leaf responses to water stress (e.g., cell wall elas- systematist) provide an example of how phyloge- ^^'^ and influence on turgor maintenance) its netic trees can direct the study of physiological ad- molec- (Robichaux Unfortunately, the 1990). et The Hawaiian silversword alliance in- al., aptation. phylogeny exhibited lowest degree of res- ular cludes 28 endemic species that represent three its A those lineages with the greatest physio- Dubautia, and olution in genera {Argyroxiphium, Wilkesia), been logical diversity, limiting the potential for molecular phylogeny has recently constructed DNA By successful reconstruction of physiological diversi- based on nuclear ribosomal sequences. on This one important constraint mapping the distribution of wet versus dry habitat fication. illustrates — 12 Annals of the Garden Missouri Botanical mapping llie process of physiology onto phyloge- sal of a pathway involving complex developmental nclic trees, namely that one must have a highly and liiocfKMnical modifications occurs with relative resolved phylog(Miy before gaining insight into ease (see also Watson et ah, 1985). This suppoils physiological divergence. lecisions of optimization during phylogenelic C^ Using a similar approach, Todd Dawson com- mapping which addition and pathway (a in loss of this teamed I)arative ecophysiologist) has up with Ste- are treated as equally likely as two ad(htions. has It phen WcIUm- (a com[)arative syslematist), Warren hcvu suggested that such labile evolutionary pal- Wagner Ann comparative and (a systematist), Sakai tenis must he founded on a genetic architcctu (a pojmlation hioh»gist) to study another group of with one, or a few, regulatory genes controlling Hawaiian plants, Schiedea and AIsin den (Iron (Car- linked sets of Cj-family structural genes (Watson i el yophyllaceae)/rhey have also ohsened the wet-to- ah, 1985; Mcmson, 1989a; & Ilatlersley V^atson, & i\vy Iransilinn in this group (Weller S. Sakai, 1990; 1992; Ehh-ringer Monson, 1993). Thus, ndative- Welleret and ah, 1900) are currently investigatiiig ly h'w nuitations, they occur in the regulator) if the physiological and ecological attributes (e.g., genes, can liave a large influence on evolution- tlie {)hotosynthctic water-use illiciency, hydraulic prop- ary expression of photosynthetic pathway type. erties of lh<» water-con<Iucting system) of these* taxa Fuilher work on the evolution of C, pliolosynlhe- hwu which permit tliem to (*xploit the drier habitats. Ul- sis has conducted in the genus Fhuvria (As- aimed liiuatcly, the study is at placing these attri- lerareae). The monograph by Powell (1978) de- butes into a phylogeui'tic context using character scribed 21 species genus. for this Piiysiologlcal mapping procedures and tlu* current [)hylogenetic cliaracterization of the component species has re- 995) veahMJ that only five or six might be classified as vide^ insight into whether those traits that permit '1ully expressed" C^ or Cj types (Monson, 1989a; cerlaln s[»ecies to thrive in dry habitats have arisen Monson Si Moore, 1989). M(»st of the sp(M*ies reflect through respons<^ to selection in their curnMit hah- some intermediate phenotype Ix^lween the C, and itals or are historical artifacts of past selection. C^ extn'uujs (the so-called Cj-C^ in1(*rmediates). Some Q-C^ work(M-s have described these species ^^ IntcrnuHliate evolutionaiy stages on the path KVOLITIONOKCJMIOTOSYNTIIKSIS from the ancestral C3 type toward derived C^ llie 0\w of tlie earliest uses of phylogeny to discern type (Monson ah, 1981; Monson, 1989a; Brown (^t & evolutionar>^ pattern in a functional plant trait in- Ilatlersley, 1989). Thus, this appears to )e a very I volves C, photosynthesis. \^'ithin five years after the active group of species in terms of photosynthetic disc(»very of C, photosynthesis researchers liad as- evolution. seml)lcd phylogenetic showing trees the distribu- Using morphological provided descrij)tions llie in tion of (;, [)lanls (Evans, 1971; Moore, 1982). From Powell (1978), have constructed a phylogenelic I was this eff(»i1 it clear that C^ photosyntliesis has tree of this genus (Fig. 5). This tree was used to and multiple origins represents a derived address whether trait, th<' qut^stion of th<wipp(»arar)ce of evolving from the ancestral Cj pholosynlheti<* path- CrQ^ iulermediate photosynthesis always precedes way pentose phosphate pathway). (tlie the ap|)earance of fully expresstMJ C, [)hoti>synthe- More and Watson recently, Ilatlersley (1992) sis. Support for such a pattern would strengthen the eonstriict(Hl an evolulIonai7 hypotlu^sis in the Po- supposition that C^-C^ intermediate photosyntluvsis aceae that n^fli-cts patterns of C4 evolution and is in lliis grouj) represents the anttn-edent to the evo- consist(*nt witli vvcll-accej)ted, higher-level laxo- lution C, pln»tosynthesis. In this reconstruction, (»f nomic affiniti(*s. Ext<Misive reticulation of liiuMges C4 sptH ies were classified as those in which the Poaceae makes in the difficult to reconstruct phy- majorit) of atmospheric CO. assimilated through it is Q Q h)geny with high levels of confidence (though mono- die C^ initlnvay, and the and cycles have phyly has been (*slablisli(Hl for s<neral subfamilies, evolved coordination where to the point leaves ex- & see Kellogg Campbell, 1987). Hattersley aiul hibit higher water- and nitrogt*n-use efficiencies Watson (1992) ma{)i)ed photosynthetic pathways hallmarks of fully expressed C^ plants. In this case, <»nlo tlu^ir tentative phylogenetic tree, revealing improvemcMits in photosynthetic water- and nitro- several possible patterns of C^ evolution. Of gen-use were assumed pailic- efficiency past gas-ex- if ular importanc(\ appears that multi])le origins of chann-e measurements have revealed reduced it in- C^ photosynthesis can occur within a single* family tercellular CO^ concentrations without reduction in and reversals of C^ photosynthesis, back to the an- {)h(>losyntlu^sis rate below average expressed by the* cestral C3 type, have occurred in several groups. all species in the genus. Such traits are presumably Such patterns suggest that tlu* evolution and revt^r- a reflection of the C^ CO^-concenlrating riKM-ha-