Table Of ContentTHE 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
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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-
