The evolutionary dynamics of plant duplicate genes
Richard C Moore and Michael D Purugganan
Given the prevalence of duplicate genes and genomes in plant
species, the study of their evolutionary dynamics has
been a focus of study in plant evolutionary genetics over
the past two decades. The past few years have been a
particularly exciting time because recent theoretical and
experimental investigations have led to a rethinking of the
classic paradigm of duplicate gene evolution. By combining
recent advances in genomic analysis with a new conceptual
framework, researchers are determining the contributions
of single-gene and whole-genome duplications to the
diversification of plant species. This research provides
insights into the roles that gene and genome duplications
play in plant evolution.
Addresses
Department of Genetics, Box 7614, North Carolina State University,
Raleigh, NC 27695, USA
Corresponding authors: Moore, Richard C (remoore@unity.ncsu.edu)
and Purugganan, Michael D (michaelp@unity.ncsu.edu)
Current Opinion in Plant Biology 2005, 8:122–128
This review comes from a themed issue on
Genome studies and molecular genetics
Edited by Susan Wessler and James C Carrington
Available online 29th January 2005
1369-5266/$ – see front matter
# 2005 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2004.12.001
Introduction
The evolutionary diversification of genomes and genetic
systems is driven in part by duplication events [1
,2].
Gene duplications contribute to the establishment of new
gene functions [3] and underlie the origins of evolutionary
novelty [4]. Plants are exceptional among eukaryotic
organisms in that duplicate loci compose a large fraction
of their genomes, partly because of the frequent occurrence
of genomic segmental duplications and polyploidization
events in plants. For example, in the Arabidopsis
thaliana and rice genomes up to 90% and 62% of loci are
duplicated, respectively, and it is estimated that 70–80%
of angiosperm species have undergone polyploidization at
some point in their evolutionary history [5–7,8
,9
].
The high proportion of duplicate genes in plant genomes
reflects the rate of retention of duplicate copies among
plant species [10,11]. The birth rate of genes in A. thaliana
(0.002 duplicates per gene per million years) is in the
same order of magnitude as that observed for yeast and
Drosophila, although ten-fold slower than that found in
Caenorhabditis elegans. The half-life to silencing and loss of
a gene duplicate in A. thaliana, however, is estimated at
23.4 million years, which is 3–7-fold higher than for
animal genomes [11]. It is not clear why duplicate genes
persist for longer periods in A. thaliana than in animal
genomes, nor is it known whether this is a general
characteristic of plant genomes. Understanding the
mechanisms underlying the retention of duplicate genes
in plant genomes continues to remain a topic of intense
interest [8
,9
,12,13
,14,15].
Theoretical and experimental studies in the past few
years have advanced our understanding of the evolutionary
dynamics of duplicate loci in plant genomes, and have
led to a rethinking of the paradigm that provided the
conceptual foundations of studies on duplicate gene
evolution [10,13
,16,17
]. The confluence of a new
conceptual framework for gene duplication with new
genomic technologies has allowed investigators to study
gene duplications on a genome-wide scale [8
,9
,12,
14,18
]. This, in turn, has reshaped our understanding
of the evolution of duplicate genes and genomes.
The fates of duplicate genes: a new
paradigm emerges
In the thirty years since the publication of Ohno’s landmark
book entitled ‘Evolution by Gene Duplication’ [2], the
reigning paradigm regarding the fate of duplicated genes
predicts that one of the duplicates is either lost (pseudogenization)
or gains a new function (neofunctionalization)
(Figure 1a). Because deleterious mutations are more
probable than advantageous mutations, it has been presumed
that most duplicate copies are lost and only a few
neofunctional loci are maintained by selection.
It has since become apparent that positive selection does
play a key role in preserving some gene copies, and
indeed can act at a very early stage of the gene duplication
process. For example, a population genetic analysis of
three unlinked duplicate gene pairs in A. thaliana that
originated less than 1.2 million years ago (mya) revealed
significantly reduced levels of nucleotide polymorphism
in the progenitor locus, the duplicate locus or both. This
reduced nucleotide variation, which is associated with a
recent selective sweep, is evidence that positive selection
plays a prominent role in the establishment of duplicate
loci [17
]. Although the action of positive selection is
consistent with the process of neofunctionalization, the
precise targets of selection in these duplicate genes are
unclear in the absence of functional data [19]. It will also
be of interest to determine whether selection acts to
Current Opinion in Plant Biology 2005, 8:122–128 www.sciencedirect.com
preserve tandem-linked duplicate loci, which are prevalent
in plant genomes [14,17
] and for which neofunctionalization
is theoretically unlikely [20].
Although Ohno’s classic paradigm provides key insights
into duplicate gene evolution, it fails to account for the
preponderance of retained duplicates in whole genomes
[21]. The duplication-degeneration-complementation
(DDC) model [16,22], which harkens to the ‘gene sharing’
concept proposed by Hughes [23], suggests an additional
evolutionary fate for duplicate loci. This model,
also referred to as subfunctionalization, suggests that
duplicate genes acquire debilitating yet complementary
mutations that alter one or more subfunctions of the
single gene progenitor (Figure 1b). The strength of this
model is that it does not rely on the sparse occurrence of
beneficial mutations, but on more frequently occurring
loss-of-function mutations in regulatory regions [16].
Subsequent empirical studies on expression divergence
between duplicate genes suggest that changes in expression
regimes occur both frequently and rapidly, consistent
with the predictions of this model [13
,24,25].
The plant MADS-box gene family: a case study
of the fate of duplicate genes
The diversification of the MADS-box transcription factor
family, whose members control key aspects of plant
vegetative and reproductive development, is a clear
example of the role that subfunctionalization plays in
shaping genetic systems. Indeed, one of the earliestdocumented
examples of subfunctionalization in plants
is the lineage-specific duplication of an AGAMOUS (AG)like
MADS-box gene in maize [26]. In maize, the ancestral
function of AG (which is expressed in stamens and
carpels) is partitioned between the duplicated genes
ZMM2 (expressed primarily in stamens) and ZAG1
(expressed primarily in carpels) [26]. A more recent
example of subfunctionalization involving MADS genes
The evolutionary dynamics of plant duplicate genes Moore and Purugganan 123
Figure 1
-
+
Redundancy
Neofunctionalization
Pseudogenization
–
Pseudogenization
+
+
–
Redundancy
Neofunctionalization
–
–
+
+
–
Neofunctionalization
and/or
subfunctionalization
Subfunctionalization
(complete)
Neofunctionalization
and/or
subfunctionalization
Regulatory subfunction
+ Gain-of-function mutation
Loss-of-function mutation–
Coding function
Gain of coding function
Loss of coding function
Gain of regulatory subfunction
Loss of regulatory subfunction
(a)
(b)
Current Opinion in Plant Biology
Segm
ental or
genom
ic
duplication
Transposition
or
sm
all-scale
duplication
+ Neofunctionalization
(coding)
Neofunctionalization
(regulatory)
Subfunctionalization
(partial redundancy)
(a) Classic Ohno model of duplicate gene fates. Mechanisms of duplication and fates of genes are indicated. Thickness of arrows indicate
relative frequency of possible fates. (b) Recent theoretical work supports a much more complex model for the fates of duplicate genes.
www.sciencedirect.com Current Opinion in Plant Biology 2005, 8:122–128
comes from the dioecious plant Silene latifolia, in which
the male sex is determined by the presence of a morphologically
distinct Y chromosome. In this species, an
autosomal homolog of the MADS gene APETALA3 (AP3),
which is involved in petal and stamen identity, was
duplicatively transferred to the Y chromosome, and subsequently
underwent divergence in gene expression [27].
On a larger evolutionary time-scale, the evolutionary
forces that govern the fates of duplicate genes are responsible
for the incredible diversity of MADS-box genes
found in present-day flowering plants. MADS-box genes
are found ubiquitously in eukaryotes as type I and II gene
subfamilies [28]. The proliferation of type II MADS-box
genes, known as the MIKC-class genes, is unique to
plants [29]. A comparative genomic survey indicates that
although the birth rate of type II MADS-box genes in
plants is lower than that of type I genes, the former are
preferentially retained in the genome [30
]. This pattern
suggests that the loss of type II MADS genes is more
deleterious than the loss of type I loci, a prediction
supported by the observation that type II genes tend
to be subject to stronger purifying selection. The lower
death rate of type II MADS genes might be due to
subfunctionalization if the divergence in function that
is observed across this subfamily necessitates the retention
of family members in the genome [31
,32]. The
selective retention of type II MADS genes also creates
a certain degree of redundancy between closely related
paralogs [33], however, suggesting that only partial subfunctionalization
occurs in certain clades.
An examination of the AG subfamily of MADS-box genes,
which controls key aspects of inner whorl floral development
in flowering plants [34
], reveals evidence of both
subfunctionalization and overlapping redundancy. The
AG subfamily is subdivided via an ancient duplication at
the base of the angiosperms into the C-class and D-class
lineages. The D-class genes are almost all expressed in
the ovules, where they specify ovule identity, whereas the
C-class lineage is primarily involved in carpel and stamen
identity [35]. By contrast, an AG-like gene in gymnosperms
is expressed in both the female reproductive
structure (megasporophyll) and the ovule [36–39], suggesting
that the genetic function of the ancestral gene in
this group was partitioned into two distinct lineages
within the angiosperms.
Another issue raised by this study is whether the partitioning
of subfunctions is equally shared between
lineages. The Antirhinnum majus PLENA (PLE) gene
was presumed to be an ortholog of the A. thaliana AG
gene because mutant analysis indicated that both genes
provide the primary C-class function in their respective
species [40,41]. However, the true ortholog of AG in
A. majus is FARINELLI (FAR), which functions redundantly
in specifying stamen identity [34
,42]. By contrast,
the orthologs of PLE in A. thaliana are the SHATTERPROOF
(SHP) genes, which primarily control differentiation
of the seed valve margin while sharing overlapping
redundancy with AG [33,43]. Thus, subfunctions of
the progenitor gene were asymmetrically partitioned
between AG/SHP paralogs in the A. thaliana lineage
relative to the PLE/FAR paralogs in the A. majus lineage.
This functional asymmetry also underscores the possible
difficulties in using functional similarity as evidence for
evolutionary orthology because the latter does not necessarily
lead to the former.
All is not lost: redundancy remains
One of the predictions of the subfunctionalization model
is that duplicate genes will share overlapping redundant
functions early in the process of functional divergence,
and phylogenetic and functional analyses clearly support
this prediction [16,33,34
,43,44]. Within A. thaliana, the
C-class genes AG and SHP1/SHP2, along with the D-class
gene SEEDSTICK (STK), share overlapping functions in
carpel identity, a remnant of their shared ancestral role
[33]. Given that these paralogs diverged at the base of the
angiosperm lineage, it is clear that duplicate genes can
exist stably in at a partially redundant state over a protracted
evolutionary period. Although subfunctionalization
can occur rapidly, it is not clear when the transition to
complete functional partitioning occurs. Indeed, theoretical
considerations of redundancy predict that duplicate
genes will reach an evolutionarily stable equilibrium of
partial redundancy, potentially delaying the transition to
complete subfunctionalization [45].
Although complete functional redundancy is difficult to
confirm, numerous examples of paralogous genes in
plants for which the deletion of one copy yields no
observable phenotype do exist [46–52], including the
three SEPALLATA1/2/3 (SEP1/2/3) and two SHP1/
SHP2 MADS-box paralogs [43,44,53]. The protein
changes in these paralogous redundant genes show no
evidence of functional divergence, suggesting that aminoacid
replacements are functionally constrained [54].
Although purifying selection apparently constrains divergence
between paralogs, population genetic analyses
indicate that significant heterogeneity in nucleotide
diversity, suggestive of positive selection, occurs within
the transcriptional unit of SHP1 and the promoter of
SHP2. By contrast, SEP2 and SEP1 appear to be evolving
neutrally [55]. These differences in evolutionary
dynamics between paralogs might be a consequence of
the position of these genes in the floral developmental
pathway. The SEP loci are involved in the highly conserved
function of floral patterning, whereas the SHP loci
control the more variable trait of seed shattering.
Duplicate and defend
The duplication of genes within or between closely
related species might lead to phenotypic variation in
124 Genome studies and molecular genetics
Current Opinion in Plant Biology 2005, 8:122–128 www.sciencedirect.com
specific traits, and manifest itself as functionally relevant,
ecologically significant polymorphisms. Gene duplication,
for example, contributes to the ability of plants to
mount a defense response against disease and herbivory
by allowing the functional diversifcation of genes that are
involved in pathogen recognition and herbivory defense.
This diversification is most evident in the large family of
disease resistance (R) genes that encode the nucleotidebinding
site plus leucine-rich repeat (NBS–LRR) proteins.
The Arabidopsis genome contains more than 150
NBS–LRR genes found as isolated genes or in tandemly
arrayed clusters that are dispersed throughout the genome.
Gene duplication of NBS–LRRs followed by positive
selection for diverse amino acids in the LRR proteinrecognition
domain might provide the means by which
the plant’s recognition of novel pathogens evolves [56].
Interestingly, a genomic analysis of the history and chromosomal
locations of NBS–LRR gene duplications
revealed that tandem duplications have contributed to
the birth of the majority of NBS–LRRs in the Arabidopsis
genome, whereas the duplicative transfer of NBS–LRRs
to dispersed chromosomal locations is largely the result of
segmental duplication [55]. Because tandemly arrayed
NBS–LRRs are subject to frequent intergenic exchange,
it is believed that those genes found in different chromosomal
regions have a greater chance of evolving new
pathogen recognition functions [56]. Moreover, a recent
study of the NBS–LRR Cf-2 pathogen-resistance gene
family in the wild species Solanum pimpinellifolium suggests
that complex evolutionary dynamics surround
duplicate Cf-2 genes, including the differential selection
of gene copies [57].
Gene duplication also plays a significant role in the
evolutionary dynamics of anti-herbivory genes. In A.
thaliana, resistance to generalist insect herbivores is conferred
in part by glucosinolates, a class of plant secondary
metabolites. The composition and quality of glucosinlate
production varies between Arabidopsis accessions. This
variation is due, in part, to the tandemly duplicated
methylthioalkylmalate synthase (MAM) genes, MAM1
and MAM2, that are involved in glucosinolate biosynthesis
[58]. MAM1 and MAM2 are functionally divergent
duplicates: the MAM2 locus is a stronger deterrent against
generalist herbivores than the MAM1 locus [59
]. A population
genetic analysis of the MAM genes found evidence
of differential gene loss and differential selection
between the MAM loci within A. thaliana accessions
(Figure 2; [59
]). These data support the action of balancing
selection on the MAM2 locus but not on MAM1.
Because glucosinolates can also stimulate feeding in
specialist herbivores, selection at the MAM2 locus might
be caused by the ecological trade-off between protection
against generalist insect herbivores and increased susceptibility
to specialists.
Variable patterns of evolution exist in another class of antiherbivory
genes, the tandemly arrayed family of six A.
thaliana trypsin inhibitor (ATTI) genes. The expression of
these six genes varies significantly between loci, among
allelic classes within A. thaliana, and in response to herbivory
[60]. These data suggest that subfunctionalization is
acting to maintain divergent functions between duplicate
loci. Despite their close proximity to each other (within
10 kb), population genetic analyses suggest that evolutionary
history also varies between ATTI loci, although
the flanking loci, ATTI1 and ATTI6, which are separated
from the core loci by recombination, have the greatest
opportunity to be acted upon by natural selection [60,61].
Polyploids: ancient and new
Polyploidization is a major mechanism by which duplicate
genes are introduced into plant genomes, and this is
reviewed elsewhere in this issue (see review by Adams
and Wendel). Several aspects of polyploidization do, however,
highlight several interesting facets that surround the
evolutionary dynamics of duplicate genes in plants. In a
recent genomic analysis of 14 model plant species, nine
species were documented to have one or more wholegenome
duplication events in their evolutionary past
[18
]. Up to four whole-genome duplication eventsappear
to have occurred in A. thaliana [6,7,8
,62,63]. Genomics
technologies might now provide a systematic explanation
of the fates of duplicate genes on a whole-genome level.
As predicted by theory [20,64,65], the majority of duplicated
genes resulting from polyploidization events are
lost in the transition to diploidy, although the percentage
of retained duplicates varies between species [10,11].
The type of duplicate genes lost or retained after
The evolutionary dynamics of plant duplicate genes Moore and Purugganan 125
Figure 2
MAM2 MAM1
Frequency Phenotype
Current Opinion in Plant Biology
7 (CH2)4
6 (CH2)3
4 (CH2)3
3 (CH2)3
3 (CH2)4
1 (CH2)4
1 (CH2)4
The genotypic frequencies and structural organization of the MAM
duplicate loci from a survey of 25 A. thaliana ecotypes. The MAM loci
modify the carbon length of the glucosinolate basic side chain; MAM2
adds three methylene groups ([CH2]3), whereas MAM1 adds four
methylene groups ([CH2]4). Slanted lines indicate the loss of particular
duplicate copies. (Based on Figure 1 of [59
].)
www.sciencedirect.com Current Opinion in Plant Biology 2005, 8:122–128
polyploidization is correlated with function. Among the
retained duplicates from the last whole-genome duplication
event in A. thaliana, genes involved in signal
transduction and transcriptional regulation are over represented,
whereas DNA-repair genes have been preferentially
lost [13
,15]. The majority of duplicates retained
(57%) tend to have divergent expression patterns as
predicted by the DDC model, whereas over 20% have
asymmetric rates of protein evolution; both are suggestive
of functional divergence [13
].
Functional divergence can occur rapidly after polyploidization,
perhaps even within a generation, and this
phenomenon has been studied in both naturally occurring
recent polyploids and in synthetic polyploids. For
example, among 40 homeologous gene pairs in natural
tetraploid cotton (which was the result of a wholegenome
duplication event that occurred 1–2 mya), nine
gene pairs exhibited biased expression, with the homeolog
from one parental genome contributing more to the
transcriptome than the other [66
]. Interestingly, 11 of
these 18 homeologs showed tissue-specific silencing or
biased expression in at least one of 10 organs tested,
indicating that they were at an early phase of subfunctionalization.
Similar patterns of biased expression were
observed in synthetic Gossypium polyploids, demonstrating
that functional divergence could occur within one
generation of polyploidization [66
]. Similar conclusions
were reached in a study of synthetic Arabidopsis allotetraploids
produced in a cross between A. thaliana and
Arabidopsis arenosa [67,68
].
Conclusions
A new conceptual framework for gene duplication combined
with emerging genomic data and technologies has
advanced our understanding of the contributions of gene
and genome duplication to the evolution of plants. Care
must be taken, however, in interpreting the influx of
genomic data in a proper functional and phylogenetic
context. For instance, although gene expression can
diverge rapidly between duplicate genes, expression data
alone cannot reveal whether the combined expression
domains of the duplicates reflect that of the progenitor
gene or whether one or both of the duplicates have gained
a novel expression regime. Indeed, in a comparative study
of lineage-specific duplicates in humans and mice, changes
in expression were more often associated with the gain of
novel expression domains, consistent with neofunctionalization
[69
]. Similarly, inferring patterns of plant genome
evolution requires a ‘phlyogenomics’ approach; genomic
data on the structural arrangements of extant genes must
be compared to that from related taxa to determine the
extent and timing of genome duplication events [9
]. Only
when such comparative approaches are used will we be
able to truly understand the contribution of single-gene
and whole-genome duplications to the emergence and
diversification of plant species.
Acknowledgements
The authors thank members of the Purugganan laboratory for a critical
reading of the manuscript. This work was supported in part by
grants from the Integrated Research Challenges in Environmental
Biology (IRCEB), Frontiers in Integrative Biological Research (FIBR)
and Plant Genome Research Programs of the US National Science
Foundation.
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