Journal of Heredity 2005:96(3):197–204
doi:10.1093/jhered/esi032
Advance Access publication February 4, 2005
ª 2005 The American Genetic Association
Phytochrome Evolution in Green and
Nongreen Plants
S. MATHEWS
From the Arnold Arboretum, 22 Divinity Avenue, Harvard University, Cambridge, MA 02138
Address correspondence to Sarah Mathews at the address above, or e-mail: [email protected].
Abstract
Photoreceptors are critical molecules that function at the interface between organism and environment. Plants use specific
light signals to determine their place in time and space, allowing them to synchronize their growth, metabolism, and
development to the environments in which they occur. Thus, innovation in light sensing mechanisms is expected to
coincide with adaptation and diversification. Three studies involving the well-characterized phytochrome photoreceptor
system in plants indicate that much work is yet needed to test this expectation. In early diverging flowering plants, episodic
positive selection influenced the evolution of phytochrome A, but little of the functional data needed to link molecular
adaptation with a change in gene function are available. In the model plant Arabidopsis thaliana, known functional differences
between a recently duplicated gene pair remain difficult to characterize at the sequence level. In parasitic plants, patterns of
development that in autotrophs are under the control of light signals are highly modified, suggesting that phytochromes and
other photoreceptors function differently in nonphotosynthetic plants. Analyses of phytochrome A coding sequences
indicate that they are evolving under relaxed constraints in nonphotosynthetic Orobanchaceae, consistent with the
expectation of functional change. Further work is needed to determine which of the processes mediated by phyA may have
been altered, a line of investigation that may improve our understanding of divergence points in downstream signaling
pathways.
Photoreceptors, Plants, and the
Environment
Photoreceptors are critical molecules that function at the
interface between organism and environment. Variable
responses to light indicate that plants use specific light
signals to determine their place in time and space, allowing
them to synchronize their growth, metabolism, and developmental transitions to the environments in which they
occur. In autotrophic plants, light cues provide circadian and
seasonal information, used to mediate the induction and
inhibition of flowering, the induction and breaking of bud
dormancy, the opening and closing of stomata and flowers,
and the cycling between sleep and waking movements. Light
cues also provide positional information, used to induce and
inhibit germination, control the pattern of seedling development, induce directional growth, determine adult architecture, and detect and avoid neighbors (Figure 1).
Based on characterization of the known photoreceptor
systems, plants use only a subset of the pigments harbored in
their cells to monitor the light environment, relying heavily
on pigments that absorb maximally in the blue (400–500 nm)
and in the red and far-red (600–800 nm) regions of the visible
spectrum. This may reflect the utility of these particular
pigments to serve as reliable indicators of ecologically
significant fluctuations in the light environment. Shorter
wavelengths in the visible spectrum are less attenuated by
nonselective diffusing filters, such as clouds, than are longer
wavelengths (Smith 1982, Figure 1a). Light scattering by
clouds may in fact lead to a slight increase in blue light (Smith
1982). Thus, blue light receptors might have particular utility
for fundamental processes, such as early seedling development and the perception of time and season. In Arabidopsis
thaliana, the blue light receptors, cryptochromes and phototropins, have significant or unique roles in these processes
(Casal 2000; Sullivan and Deng 2003). Conversely, light
scattering within a stem will be greater for short wavelengths,
and there will be steeper gradients of blue than of red light in
a stem irradiated with unilateral light (Hart 1988). Phototropism relies on light gradients as well as light absorption
(Iino 1990), and this may be one reason why blue light
receptors have been employed to mediate phototropic
responses. In Arabidopsis, and perhaps in most angiosperms,
the sensitivity of the cryptochrome and phototropin systems
is enhanced by the possession of at least two copies of each
pigment, one that is sensitive to weak light signals and one
that is sensitive to strong light signals (Briggs and Huala
1999; Galen et al. 2004). This could ensure that processes
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Journal of Heredity 2005:96(3)
R or FR
PHY
Germination
R, FR or B
PHY, CRY
Seedling development
De-etiolation
R, FR or B
Vegetative Growth
Gravitropism (PHY)
Phototropism (PHOT)
Shade avoidance (PHY)
Stomatal opening (PHOT)
Chloroplast movement (PHOT)
Circadian timing (CRY, PHOT, PHY)
PHY, CRY
Flowering
Figure 1. The roles of different photoreceptors in the development of Arabidopsis (Sullivan and Deng 2003). R, red light;
FR, far-red light; B, blue light; PHY, phytochromes; CRY, cryptochromes; PHOT, phototropins.
mediated by blue light signals would be relatively robust to
the variation in light quantity between open and dimly lit
environments, between clear and overcast skies, and below
and above the soil surface. However, blue light receptors are
inadequate for neighbor detection, for which a dual sensing
system is needed.
The Phytochrome System
Among the most critical light cues used by plants are those
that indicate where they are in relation to neighbors that
might impinge on their access to photosynthetically active
radiation. Because the pigments in stems and leaves absorb
wavelengths below about 700 nm, reflected light and shade
are enriched for wavelengths in the far-red region but
depleted for wavelengths in the blue to red regions of the
spectrum (Smith 1982, Figure 1e). This suggests that a pair of
photoreceptors with contrasting absorption maxima above
and below about 700 nm would serve as a useful indicator of
changes in the relative proportions of short and long
wavelengths that accompany the encroachment by neighbors. What plants actually have is an elegant system relying
on a single type of pigment, phytochrome, with two
photointerconvertible forms, one absorbing maximally in
the red (660 nm) and the other absorbing maximally in the
far-red (730 nm). Absorption of red light (R) by the redabsorbing form (Pr) induces conversion of the protein to the
far-red-absorbing form (Pfr); likewise, absorption of far-red
198
light (FR) by Pfr induces conversion to Pr. Thus at any one
time, Pr and Pfr are in a dynamic equilibrium that reflects
the relative proportions of R and FR in ambient light.
Furthermore, phytochromes are very sensitive indicators of
increasing or decreasing shade because small changes in the
R:FR ratio of ambient light lead to large changes in the ratio
of Pfr to Ptotal (Smith 1982). Thus, even very small changes
are detectable, such as those that occur in the light reflected
from stems of small neighbors (Ballaré et al. 1990). In
response to the detection of neighbors, shade-intolerant
plants increase extension growth, suppress branches, make
thinner leaves with less chlorophyll, flower early, and
increase allocation to storage organs—a set of processes
collectively referred to as the shade avoidance syndrome
(Smith and Whitelam 1997). In similar conditions, an animal
might fight or take flight.
Shade avoidance is adaptive in flowering plants (Aphalo
et al. 1999; Schmitt et al. 1995) and it is clear that one critical
function of phytochrome is to detect changes in R:FR (Smith
1982). In A. thaliana, phytochrome B (phyB) is the principal
mediator of shade avoidance (Aukerman et al. 1997; Devlin
et al. 1998, 1999; Franklin et al. 2003b; Sharrock et al. 2003a;
Smith and Whitelam 1997). PhyB also is the primary
mediator of developmental responses to saturating pulses
of R that are reversible with pulses of FR (Whitelam and
Devlin 1997). These responses are important for the control
in open habitats of light-regulated seed germination and early
seedling development, a critical stage of life when the young
Mathews Phytochrome Evolution in Plants
Figure 2. The relationships of phytochrome genes of A. thaliana, where phyA and phyB have been demonstrated to be
the principal mediators of responses to far-red and red light, respectively.
seedling must make the transition from dependence on
maternal resources stored in the seed to photosynthetic
independence (Figure 1). An emerging seedling may enter
one of two alternative pathways of development: skotomorphogenesis or photomorphogenesis. Germinating seedlings
that receive a light signal switch from skotomorphogenetic to
photomorphogenetic development, a process known as deetiolation, inhibit extension growth and develop leaves and
a photosynthetic apparatus (Figure 1). Germinating seedlings
that do not receive a light signal remain skotomorphogenetic;
they delay the production of leaves and photosynthetic
development and use their capacity for elongation to seek
light.
In the event that the seedling fails to reach the light, it
may outgrow its resources and die. During this stage of
development, when greening and the inhibition of extension
growth are critical, shade avoidance reactions could be
counterproductive to seedling survival (Smith et al. 1997).
Thus, a potential cost of shade avoidance may be a decrease
in seedling establishment in shady habitats or in dense
stands. If so, seedling mortality in dense stands would be
avoided because phyB inhibits germination in these
conditions. Only when a canopy gap of sufficient size is
detected will the activity of phyB promote germination
(Smith 1995). This inhibitory influence on germination is
important for shade-intolerant species, but if present in
shade-tolerant species, could limit their ability to establish
under canopies.
Together the potential cost of early shade avoidance and
the inhibitory actions of phyB on germination in shaded
environments could limit the ability of plants to establish
under canopies, decreasing their ecological amplitude. These
costs could be a general factor affecting the capacity of seed
plants to colonize shady habitats because both gymnosperms
and angiosperms have shade avoidance responses and FRinhibition of germination (e.g., Toole et al. 1961; Warrington
et al. 1988). However, the degree to which any group of
species is limited by these costs would be influenced by other
factors. For example, counterproductive early shade avoidance is most likely to affect angiosperms because of their
rapid growth rates, especially when combined with the
possession of small seeds. Conversely, cycads, an anciently
derived group of seed plants, would be less affected because
they have relatively large seeds and their seedlings grow very
slowly; they can exist for very long periods without light
(Mathews S and Tremonte D unpublished data). Ginkgo also
has large seeds and relatively slow growth. Many conifers
have small seeds and growth rates intermediate between
cycads and angiosperms. However, in many conifers,
seedling de-etiolation is uncoupled from light signals so
that they are constitutively photomorphogenic, or green in
the dark (e.g., Bogorad 1950; Mukai et al. 1992). For these
species, early shade avoidance would less likely be
counterproductive.
As noted, angiosperms are particularly at risk because they
evolved rapid growth rates. This characteristic is coupled with
the widespread occurrence of small seeds, including in the
earliest diverging lineages (Feild et al. 2004) and skotomorphogenetic seedling development. Angiosperms then may
have a special need for a mechanism to counteract early
shade avoidance, and also the inhibitory actions of phyB
on germination and seedling development in deep shade.
A candidate for such a mechanism is one of the other
angiosperm phytochromes, phyA (Smith et al. 1997), which
functions to promote germination and seedling photomorphogenesis in continuous FR and in deep shade (Casal et al.
1997; Yanovsky et al. 1995). Additionally, phyA induces
germination in response to millisecond pulses of broad
spectrum light, promoting germination after brief soil
disturbances (Casal et al. 1997) and possibly after exposure
to sunflecks.
In flowering plants, phyA and phyB represent the
principal mediators, respectively, of FR- and R-mediated
development (Whitelam and Devlin 1997), and null mutants
of each have severe phenotypes. Three additional phytochromes occur in A. thaliana, phyC, phyD, and phyE. Each
of these apparently has a lesser role in photomorphogenesis
(Figure 2), and phenotypes of the nulls are most apparent in
mutants with lesions in multiple phytochromes (Aukerman
et al. 1997; Devlin et al. 1998; Franklin et al. 2003a,b; Hennig
et al. 2002; Monte et al. 2003; Sharrock et al. 2003a,b). PhyC
is widely distributed in flowering plants, diverging from
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Journal of Heredity 2005:96(3)
phyA prior to their origin (Mathews and Sharrock 1997;
Sharrock and Quail 1989). PhyE also is widely distributed in
flowering plants, diverging from phyB very early in their
history (Mathews S unpublished data), although sporadic
losses of phyE have occurred (Mathews and Sharrock 1997).
PhyD is restricted in distribution to Arabidopsis and its
relatives, diverging from phyB near the origin of the mustard
family (Brassicaceae; McBreen K and Mathews S unpublished data).
The Evolution of phyA in Early
Angiosperms
The possibilities that the some or all of the functions of
phyA might help plants establish in shady habitats and that
the origin of one or more of these functions might have
coincided with the origin of flowering plants suggest that
they might have provided an adaptive advantage to early
angiosperms during their colonization of the forest dominated by ferns and gymnosperms. The radiation of the
angiosperms is one of the more spectacular events in the
history of land plants. They number ; 260,000 species,
about six times more than all other land plants combined
(; 38,000 species), and they far outnumber other seed plants
(; 1,000 species). Although these numbers represent current
diversity, no other group of land plants previously achieved
comparable levels of diversity, and the rise of flowering
plants to ecological dominance was similarly remarkable
(Bond 1989; Crane et al. 1995; Wing and Boucher 1998).
Multiple factors likely account for the success of flowering
plants, but in the attempt simply to gain a foothold,
photoreceptor evolution may have played a role.
If the origin of any of the functions of phyA provided an
adaptive advantage for early diverging angiosperms, we
might expect (1) to find evidence of episodic selection in the
sequences of species belonging to the remnants of these
lineages, (2) to find that phyA functions occur in these
species, and (3) that these functions are not found outside
angiosperms. PhyA may be unique to flowering plants
because it arose by gene duplication prior to their origin
(Mathews and Sharrock 1997; Sharrock and Quail 1989).
However, its relationships with phytochromes in gymnosperms remain ambiguous in the absence of data that can
resolve whether separate gene duplications occurred in
angiosperms and gymnosperms or whether a single duplication occurred prior to the divergence of angiosperms from
gymnosperms (Sharrock and Mathews in press). Whether the
protein is ancient or was more recently derived, phyA
sequences provide unambiguous evidence that innovation at
the molecular level occurred very early in the history of
angiosperms. An apparent episode of positive selection and
a high proportion of radical amino acids map to the branch
leading to the angiosperm phyA clade (Mathews et al. 2003;
Mathews 2004), consistent with an adaptive role for phyA.
However, linking this episode of molecular adaptation with
changes in photoreceptor function requires characterization
of responses to continuous FR (FRc) in gymnosperms and in
200
the representatives of the earliest diverging angiosperm
lineages. If the capacity to establish successfully in FRc or
deep shade is not unique to angiosperms, or if it arose late in
their history, it is unlikely that it is a special feature that aided
early angiosperms.
Previous studies have suggested that the seedlings of
Ginkgo and conifers have a limited ability to de-etiolate in FRc;
seedlings of both groups exhibited greater cotyledon or leaf
development in FRc than in the dark, but extension growth
was similar in both treatments, suggesting that FRc and
perhaps deep shade cannot fully induce early seedling
development (Burgin et al. 1999; Christensen et al. 2002).
This work needs to be extended. There are no data from
Gnetales, a distinctive group of seed plants (Gnetum, Ephedra,
and Welwitschia) that are related to conifers, or from most
conifers, where only shade-intolerant members of the pine
family have been examined. No previous studies have
examined cycads, but preliminary data suggest that they lack
even the rudimentary phyA-like responses observed in
Pinaceae and Ginkgo (Mathews S and Tremonte D unpublished data). There are also no data from most groups of
flowering plants, and none at all from species that diverged
early in their history. However, similar responses to FRc in
rice (a monocot; Takano et al. 2000), Arabidopsis (a eudicot),
and Calycanthus (Mathews S and Tremonte D unpublished
data) (a woody shrub that diverged before the eudicot
radiation) suggest that phyA responses were established
relatively early. It also will be important to establish the
ecological relevance of seedling responses to FRc. The
mortality of Arabidopsis phyA-null mutants in shade suggests
that this function of phyA is critical to seedling establishment
under canopies (Yanovsky et al. 1995), but this remains to
tested in a wider range of species.
Finding that molecular adaptation and the origin of
FRc-mediated seedling development are correlated would be
consistent with the hypothesis that innovation in phyA
function was adaptive in early angiosperms. An important
further test of the link between molecular adaptation and
functional innovation is under way. It relies on mutagenesis
experiments to determine the phenotypic effects of changing
to their ancestral states the amino acid residues that changed
along the branch to all phyA sequences and were then fixed.
If the spectral activity of the resulting photoreceptor
molecule is changed and/or if expression of the sequences
in phyA-null mutants of Arabidopsis cannot fully restore phyA
function, it would be consistent with a role for these sites in
the evolution of angiosperm phyA function.
The Evolution of phyB and phyD in
Arabidopsis
Although it is clear that the divergence of phyA from phyC
involved functional divergence, evolution in the phyB lineage
has resulted in additional phytochromes that apparently
make only minor contributions to processes principally
mediated by phyB, at least in Arabidopsis (Figure 2). Neither
phyD, which is restricted to Arabidopsis and its relatives, nor
Mathews Phytochrome Evolution in Plants
host signal
Germination
?
Seedling development
?
Vegetative Growth
Flowering
Gravitropism (?)
Phototropism (absent?)
Shade avoidance (absent?)
Stomatal opening (?)
Chloroplast movement (absent)
Circadian timing (?)
Figure 3. Development in a nonphotosynthetic member of the parasitic Orobanchaceae, where aspects of development that
are light-mediated in autotrophs (compare Figure 1) are modified or possibly absent.
phyE, which is found widely in angiosperms, can rescue the
phyB-null mutant phenotype of Arabidopsis (Sharrock et al.
2003a), and both photoreceptors have phenotypes that are
difficult to discern in single mutants (Aukerman et al. 1997;
Devlin et al. 1998). Thus it is possible that these two
additional phytochromes are evolving under relaxed constraints and are likely to be silenced. Consistent with this
suggestion, phyE has been lost from monocots and from
some dicot families (Mathews and Sharrock 1997; Sharrock
and Mathews in press), and the phyD of the Ws
(Wassilewskija) ecotype of A. thaliana is a pseudogene
(Aukerman et al. 1997). However, the loci encoding both
these phytochromes have been retained longer than the
average half-life of duplicate genes of around 4 million years
(Lynch and Connery 2000), and the Arabidopsis ecotypes
commonly used in the lab retain a functional phyD
(Aukerman et al. 1997). Moreover, in the case of phyD,
there is evidence that purifying selection constrains its
evolution (McBreen K and Mathews S unpublished data).
This suggests that despite its apparently minor phenotype,
phyD is important. The phyD coding sequence driven by the
phyB promoter can fully complement the early flowering
phenotype of the phyB null mutant (Sharrock et al. 2003a). It
is possible that redundancy for flowering time is important
enough for the retention of phyD, despite its disappearance
from the Ws ecotype. It also is possible that subtle
neofunctionalization or subfunctionalization may have
occurred.
Experiments with chimeric proteins demonstrate that
amino acids in the central regions of the phyB and phyD
coding sequences are critical to their respective activities and
that these two photoreceptors differ significantly in their
abilities to activate signaling pathways (Sharrock et al. 2003b).
This is consistent with either the origin of a new function,
perhaps one that is not obvious in typical genetic screens, or
with subdivision of ancestral phyB function at the level of
downstream signaling pathways. A suggestion that may be
worth exploring is that the role of phyD in some natural
populations is more important than has been indicated by lab
phenotypes. For example, Halliday and Whitelam (2003)
have shown that both temperature and photoperiod affect
the prominence of the role of phyD in control of flowering
and leaf expansion. The natural light environment is
considerably more complex than the laboratory environment,
and it is becoming more apparent that temperature effects,
photoperiod, and potentially other environmental factors
influence phytochrome activity and the roles of specific
phytochromes (Franklin and Whitelam 2004; Halliday and
Whitelam 2003; Heschel MS and Donohue K personal
communication).
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Journal of Heredity 2005:96(3)
The Evolution of Phytochromes in a
Family of Parasitic Plants
Studies of phytochrome evolution in parasitic plants offer
the opportunity to address the question of how photoreceptors evolve in plants in which development and light
cues are to some extent unlinked (compare Figures 1 and 3).
Several studies have provided insight into the evolution of
plastid genomes in parasites, finding in many cases that
photosynthetic genes are lost or nonfunctional (dePamphilis
1995). The plant family Orobanchaceae provides a useful
system for characterization of phytochrome evolution in
parasites because it comprises a single autotrophic lineage
that is sister to the remaining family, which in turn is made up
of sister pairs of lineages that either are photosynthetic root
parasites (hemiparasites) or nonphotosynthetic root parasites
(holoparasites). Germination in the holoparasites is promoted by signals from host plants, and both holoparasites
and hemiparasites may have prolonged underground stages
of skotomorphogenetic development during which they rely
completely on the host plant. This developmental pathway
contrasts markedly with development in the light-seeking
seedlings of autotrophic plants (Figures 1, 3). On emergence,
holoparasites produce only a nonphotosynthetic inflorescence (Figure 3), whereas hemiparasites develop a photosynthetic shoot system before flowering. The degree to which
photoreceptors mediate gravitropism, phototropism, shade
avoidance, stomatal opening, chloroplast movement, and
flowering in hemiparasites remains unknown, but presumably the expression of these processes remains to
a greater or lesser extent under the control of light signals.
In contrast, some of these processes, such as phototropism
and shade avoidance, are probably absent from holoparasites, and it remains unknown what controls stomatal
opening and flowering (Figure 3). In at least one case,
flowering of Orobanche minor appeared dependent on the
flowering of the host in response to long days (Kuijt 1969).
The mechanisms that underlie novel processes in the
parasites, such as the inhibition of seedling emergence and
of photosynthetic shoot development during emergence of
the holoparasites, also remain unknown.
These developmental differences between autotrophs
and parasites suggest that the functions of photoreceptors
differ among autotrophs, hemiparasites, and holoparasites.
Changes in photoreceptor function may be required to
maintain the differences in developmental pathways that
characterize the three lifestyles. In some cases, origin of
a novel function may be important. In others, aspects of
photoreceptor function may become superfluous during the
transition from autotrophic to parasitic habit. Functional
changes may occur through gene loss, through altered
expression patterns, by sequence-specific changes in coding
regions of the genes, or through a combination of these
factors. The holoparasite O. minor retains and expresses at
least one cryptochrome gene (Okazawa et al. 2004), but other
data regarding the distribution of cryptochromes and phototropins in the family are lacking. In contrast, there is evidence
that the two major phytochromes, phyA and phyB, are widely
202
retained in the family, as is phyE; fewer data are available
about the distribution of phyC, but it has been detected in at
least some species (Bennett JR and Mathews S unpublished
data). PhyA is expressed in the holoparasite O. minor
(Okazawa et al. 2004), but other expression data are lacking.
Because phytochromes participate directly in the transition from skotomorphogenetic to photomorphogenetic
developmental pathways, it will be critical to compare
patterns of gene expression among autotrophs and parasites
during the transition from underground to above-ground
phases. Characterization of changes in coding sequences also
may provide insight. For example, if any one of the
phytochromes is directly implicated in the transition to
parasitism, convergent amino acid substitutions might be
observed in multiple holoparasitic lineages, and there might
be evidence that these positions have been influenced by
positive selection (or more generally, that selective constraints
have been altered at these sites). Conversely, if the function of
any one of the phytochromes is less important in parasites,
there should be evidence of relaxation in selective constraints.
Preliminary analyses of phyA sequences provide no evidence
of convergent change that would directly implicate changes in
this photoreceptor in the transition to the parasitic habit.
However, there is evidence that phyA is evolving under
relaxed selective constraints in the holoparasites relative to
both the hemiparasites and autotrophic species (Bennett JR
and Mathews S unpublished data). These observations are
consistent with a scenario in which at least some of the
functions of phyA are less critical in holoparasites than they
are in photosynthetic taxa. Ultimately, studies in this system
may lead to the discrimination of divergence points in the
downstream signaling pathways because some aspects of
development differ between autotrophs and holoparasites
whereas others do not (Figures 1, 3).
Concluding Remarks
These studies of the phytochrome system highlight the limits
of our understanding of how plant photoreceptors might
function in natural environments and outside model species.
In Arabidopsis, the factors responsible for the functional
differences between phyB and phyD remain elusive. Intriguing new data suggest that temperature has a profound
effect on processes mediated by specific phytochromes
(Halliday and Whitelam 2003; Heschel MS and Donohue K
personal communication), a phenomenon certain to come
into play outside the lab. In nonmodel systems, functional
information generally is lacking. Nevertheless, it is clear that
phytochrome-mediated processes differ in parasitic plants
and outside angiosperms from those characterized in model
systems. Limited knowledge of these systems hinders efforts
to understand the roles that photoreceptor evolution might
have in enhancing the capacity of plants to adapt to new
environments during diversification events. It is important
to develop strategies to take advantage of both natural
environments and nonmodel species to increase understanding of how photoreceptor function evolves. Specifically,
Mathews Phytochrome Evolution in Plants
functional models inferred from model systems should be
tested in a wide variety of natural environments and in
species with a wide range of morphologies and ecologies.
Studies of Arabidopsis already are being extended to evaluate
amounts of natural variation and to exploit natural variants
(e.g., Borevitz et al. 2002; Botto and Smith 2002; Maloof
et al. 2000, 2001; Mitchell-Olds 2001). A complimentary
effort to exploit the rich resources of nonmodel systems,
a more challenging task, is also needed.
Acknowledgments
This paper is based on a presentation given at the symposium entitled
‘‘Genomes and Evolution 2004,’’ cosponsored by the American Genetic
Association and the International Society of Molecular Biology, and
Evolution, at the Pennsylvania State University, State College, PA, USA,
June 17–20, 2004.
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Corresponding Editor: Shozo Yokoyama