rstb.royalsocietypublishing.org Review Cite this article: Jiao Y, Paterson AH. 2014 Polyploidy-associated genome modifications during land plant evolution. Phil. Trans. R. Soc. B 369: 20130355. http://dx.doi.org/10.1098/rstb.2013.0355 One contribution of 14 to a Theme Issue ‘Contemporary and future studies in plant speciation, morphological/floral evolution and polyploidy: honouring the scientific contributions of Leslie D. Gottlieb to plant evolutionary biology’. Subject Areas: evolution, genomics, plant science Keywords: genome modification, ancestral gene content, polyploidy, gene family gain and loss Author for correspondence: Andrew H. Paterson e-mail: [email protected]Electronic supplementary material is available at http://dx.doi.org/10.1098/rstb.2013.0355 or via http://rstb.royalsocietypublishing.org. Polyploidy-associated genome modifications during land plant evolution Yuannian Jiao and Andrew H. Paterson Plant Genome Mapping Laboratory, University of Georgia, 111 Riverbend Road, Athens, GA 30606, USA The occurrence of polyploidy in land plant evolution has led to an acceleration of genome modifications relative to other crown eukaryotes and is correlated with key innovations in plant evolution. Extensive genome resources provide for relating genomic changes to the origins of novel morphological and phys- iological features of plants. Ancestral gene contents for key nodes of the plant family tree are inferred. Pervasive polyploidy in angiosperms appears likely to be the major factor generating novel angiosperm genes and expanding some gene families. However, most gene families lose most duplicated copies in a quasi-neutral process, and a few families are actively selected for single- copy status. One of the great challenges of evolutionary genomics is to link genome modifications to speciation, diversification and the morphological and/or physiological innovations that collectively compose biodiversity. Rapid accumulation of genomic data and its ongoing investigation may greatly improve the resolution at which evolutionary approaches can contrib- ute to the identification of specific genes responsible for particular innovations. The resulting, more ‘particulate’ understanding of plant evolution, may elev- ate to a new level fundamental knowledge of botanical diversity, including economically important traits in the crop plants that sustain humanity. 1. Introduction Genome duplication is a punctuational event in the evolution of a lineage, with permanent consequences for all descendants—if the lineage survives. Most crown eukaryotes pass through different ploidy levels at different stages of development [1,2] and continuously produce aberrant unreduced gametes at low rates. However, the extreme rarity of genome duplications in the evolution- ary history of extant lineages, usually surviving only once in many millions of years, shows that the vast majority quickly go extinct [3]. Classical views suggest that genome duplication is potentially advan- tageous as a source of genes with new functions [4,5]. Some polyploids appear to realize these and other benefits [6], with genome duplication thought to be central to the evolution of morphological complexity [7]. Polyploids have long been suggested to enjoy a variety of capabilities that transgress those of their diploid progenitors, such as adaptation to environmental extremes [8– 11]. Angiosperms are an outstanding model in which to elucidate consequences of genome duplication in crown eukaryotes. It has long been suspected that many angiosperms were palaeopolyploids [10,12]. Indeed, recent analyses of genome sequences [13,14] show that all angiosperms are palaeopolyploids. Seminal find- ings from yeast [15–17] and Paramecium [18] are shedding valuable light on consequences of genome duplication in single-celled organisms. However, these consequences are expected to be very different in higher eukaryotes with small effective population sizes, such as angiosperms and mammals [19,20]. Herein, we describe some representative features of major land plant groups and associated genomic modifications and variations throughout the history of plant evolution. We circumscribe the ancestral gene content for key nodes of the evolutionary series, as well as adaptational genomic changes occurring along the branches leading to these nodes. We also review current approaches for genome structure comparison to unravel ancient polyploidy and discuss the consequences of these polyploidy events, particularly the biased pattern of gene gains and losses following genome duplication. & 2014 The Author(s) Published by the Royal Society. All rights reserved. on May 19, 2018 http://rstb.royalsocietypublishing.org/ Downloaded from
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ReviewCite this article: Jiao Y, Paterson AH. 2014
Figure 1. Global gene family loss and gain in plant genomes. Eleven sequenced plant genomes were selected for phylogenetic representation of major plant groups. Genefamilies were identified using OrthoMCL, and the Count program was used to determine the minimum gene set for ancestral nodes of the phylogenetic tree using aWagner parsimony framework. Numbers after each node indicate the estimated ancestral gene numbers, while the numbers above each branch show the number of genefamily gains (þ) and losses ( – ). The extra bar under the internal branches means one or more rounds of ancient polyploidy suggested along that time period.
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abies, lacks flowering locus T (FT)-like genes (that promote flow-
ering in other taxa), instead containing a group of FT/TFL1-like
genes which probably act as flowering repressors [28,46,47]. The
FT-like genes are exclusively found in angiosperms, including
early diverging and eudicot lineages, supporting the hypothesis
that the evolution of flowering plants coincided with the evol-
ution of a flower-promoting function for an FT/TFL1-like
gene. In plants, MADS-box genes encode transcription factors,
which are important regulators of plant development, particu-
larly as regulators of floral organ identity [48]. A total of 278
MADS-box homologies were identified in P. abies, most of
which are type II MADS-box genes (MIKC-type proteins, with
structure of MADS (M) domain followed by an Intervening (I),
a Keratin-like (K) and a C-terminal domain). The VASCULAR
NAC DOMAIN (VND) gene family controls the formation of
multi-cellular vessels, which has been considered to be one
of the key innovations that contribute to the success of the
flowering plants [49]. The VND gene family has been expanded
with only two VND genes found in P. abies [28] and seven in
Arabidopsis thaliana [50].
Another large wave of gene family gains (figure 1, node 4,
1492 new gene families) was inferred along the branch leading
to angiosperms, suggesting that a diverse set of novel gene
functions originated before the emergence of angiosperms.
Angiosperms have seeds contained within a fruit, unlike gym-
nosperms that have naked seeds (no fruit). The flowers, fruits
and other characters of angiosperms are likely to have contrib-
uted to their emergence as the most species-rich group of land
plants [51–53]. However, because this exemplar analysis does
not include genome sequences from basal angiosperms, it
cannot distinguish gene families originating before or soon
after the earliest diversification of angiosperms. Amborella is
thought to be the single living sister species to other extant
flowering plants, and the Amborella trichopoda genome, which
is finished but not yet available for large-scale analysis, will
provide a valuable reference for reconstructing ancestral
Figure 2. Impact of divergence time and consecutive rounds of genome duplication on synteny signals. Syntenic blocks were identified using MCscanX [61]. Thecomparisons of Oryza-Sorghum and Vitis-Carica were used to show synteny when no genome duplication occurred after the divergence. One genome duplicationoccurred after the divergence of Oryza-Zea and Vitis-Populus respectively, and multiple WGDs occurred after the split of Oryza-Musa and Vitis-Musa. The signal ofsynteny was eroded following the increasing divergence time and additional number of WGDs after the separation. (Online version in colour.)
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total orthologue pairs, versus 30–50% in intra-species compari-
son in eudicots or monocots (see table 1 in [61]). Inter-genome
synteny blocks can be substantially affected by the number of
genome duplications after species divergence, as well as the
timing of species divergence (figure 2).
Many algorithms and software have been developed to find
syntenic blocks within or among genomes. In general, hom-
ology matrices are built using all-against-all BLAST searches,
and then synteny is detected through clustering neighbouring
matches within a matrix, such as the methods implemented in
Figure 3. Different gene loss patterns affect the reconstructed phylogeny using single-copy genes. If the single-copy gene was duplicated in the common ancestorof species A, B and C, different gene silencing timing and patterns will impact the final reconstructed evolutionary relationships. The most hypothesized case is thatthe duplicates in the ancestor are quickly restored to single-copy status. However, several single-copy genes in soya bean have retained the duplicated copy for about13 Myr. Many speciation events could occur during such a long time. Here, we proposed four different gene loss patterns, and all could restore single-copy genestatus. (a) All three genes in one big clade went through gene deletion, and the remaining three genes can be used to reconstruct the phylogeny correctly. However,if gene loss patterns were as in (b) and (c), the constructed phylogeny will not truly reflect the relationships among species. (d ) Although gene c 2 is not theorthologue of a1 and b1, the final tree is correct by chance. (Online version in colour.)
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genes are more likely to be retained after WGD than after
tandem duplications, with losses of such genes resulting in
a sort of haploinsufficiency relative to the remainder of the
genome. It has also been argued that balanced gene drive
should tend to drive up morphological complexity [7],
which is potentiated by duplicated functional models (gene
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networks). An important need for further investigation
of many of these ideas is a much greater knowledge of
the various forms of interactions among genes, including
physical, regulatory and feedback-mediated.
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369:20130355
7. Palaeopolyploidy and gene lossesPolyploidy has made a significant contribution to gene family
expansion and novel gene content as discussed above; how-
ever, non-random patterns of loss of duplicated genes are less
studied. As noted above, the vast majority of gene duplicates
tend to be silenced in a relatively short period of time, and
this process is not random [81,103,104]. Specific genes and genefunctional groups show more extensive loss of duplicate copies thanthe genome-wide average, and this loss is often convergent followingindependent duplications separated by hundreds of millions of years[100,105,106]. Investigations of single-copy genes in sequenced
flowering plants has statistically ruled out the possibility of
random gene loss (e.g. [58,106]). Single-copy genes are overre-
presented in some essential functional categories, such as DNA
repair, recombination, enzyme activity and organelle-related
functions, and underrepresented in GO categories in which
WGD survivors are usually significantly enriched (e.g. tran-
scription factor activity, kinase activity, transport, signal
transduction) [105,106]. Furthermore, single-copy genes show
more sequence conservation, higher gene expression level,
and expression in more tissues than multiple-copy genes
[106]. Conserved nuclear single-copy genes have been used
as markers for reconstructing angiosperm phylogeny, even
eukaryotic relationships, and for improving resolution of the
evolutionary history of organisms [107,108]. However, it
might be problematic to use some specific single-copy gene
families as phylogenetic markers if speciation precedes their
restoration to single-copy status. For example, two recent
studies [106,107] each show that genes that are single-copy in
other organisms are still duplicated in soya bean after its
most recent polyploidization event at approximately 13 Ma,
and tetraploid cotton appears likewise to experience relatively
slow gene loss [109]. If a speciation event occurred before
duplicated genes experienced reciprocal gene silencing, a
reconstructed phylogeny may not reflect the true evolutionary
relationship (figure 3).
It has been suggested that reciprocal gene loss after
polyploidy could contribute directly to speciation and repro-
ductive isolation [17,90,110–112]. By investigating gene losses
following a WGD in a common ancestor of three yeast species
(S. cerevisiae, Saccharomyces castellii and Candida glabrata), it has
been shown that 20% of the loci experienced differential gene
loss patterns [17]. The speciations were shortly after the WGD
event, during a period of precipitous gene loss. Therefore, it is
hypothesized that reciprocal gene loss at many ancestrally
duplicated genes could be the main factor leading to speciation
[17]. However, two recent genome-wide studies of syntenic
gene losses in Poaceae found very little evidence supporting
reciprocal loss of homologous genes among the grass species
[33,113]. While evidence from additional plant groups needs
to be explored, substantially different effective population
sizes in microbes (very large) and crown eukaryotes (very
small) may contribute to differences in the fates of duplicated
genes [19,20] and associated evolutionary patterns.
8. Conclusion and future studiesOne of the great challenges of evolutionary genomics is linking
genome modifications that are evident in the burgeoning sets
of angiosperm (and other) genome sequences now available
to speciation, diversification and the morphological and/or
physiological innovations that collectively constitute biodiver-
sity. Polyploidy events are prevalent throughout angiosperm
evolution. While the timing of many ancient WGD events
can be circumscribed to specific branches of angiosperm phy-
logeny, much better resolution is needed to link genomic
changes to their biological consequences. Soon, genome
sequences will be available for virtually all branches of land
plant phylogeny, which will help to improve resolution.
Enriched knowledge of botanical diversity may permit us to
circumscribe not merely thousands or even hundreds of impor-
tant functional changes to a branch, but much smaller
numbers, approaching a more ‘particulate’ model for evol-
utionary history in much the same manner that Mendelian
genetics transitioned science away from ‘blending’ models of
inheritance. Dosage balance could explain some biases in
gene retention after different modes of duplication. Detailed
analysis of evolutionary history of all members of functional
protein complexes might provide stronger support for this
hypothesis. More effort is needed in reconstructing, decoding
and analysing the inferred ancestral genomes prior to diversi-
fication of major angiosperm groups. With reconstructed
ancestral genomes, we could thoroughly assess genome modi-
fications such as gene gain and loss through evolution, and
associate such changes with diversification and novel inno-
vation and function. In addition, genome resequencing data
could provide more insights into genome variation following
evolution and adaptation at the population level. Genome
modifications, including duplication, fractionation, rearrange-
ments and changes in expression, have the potential to
facilitate the origin of new functional variation in organisms,
including economically important traits in the crop plants
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