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com

Ancient whole genome duplications, novelty and diversication: the WGD Radiation Lag-Time Model
M Eric Schranz1, Setareh Mohammadin1 and Patrick P Edger2
Many large and economically important plant groups (e.g. Brassicaceae, Poaceae, Asteraceae, Fabaceae and Solanaceae) have had ancient whole genome duplications (WGDs) occurring near or at the time of their origins, suggesting that WGD contributed to the origin of novel key traits and drove species diversication. However, these large clades show phylogenetic asymmetries with a species-rich crown group and a species-poor sister clade, suggesting signicant lag-times between WGDs and radiations. The species-poor sister groups share many key traits, but are often restricted to the hypothesized center of origin for the larger clade. Thus, the ultimate success of the crown group does not only involve the WGD and novel key traits, but largely subsequent evolutionary phenomena including later migration events, changing environmental conditions and/or differential extinction rates.
Addresses 1 Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, PO Box 94240, 1090 GE Amsterdam, The Netherlands 2 Division of Biological Sciences, University of Missouri, 1201 Rollins Street, Columbia, MO 6521, USA Corresponding author: Eric Schranz, M (M.E.Schranz@uva.nl)

origin of novelties and radiations across the tree of life [2]. For example, all vertebrates underwent two rounds of WGD in their early evolutionary history [3], the Saccharomyces yeast clade is polyploid [4], and the origin and diversication of the ray-nned sh lineage is correlated with a polyploidy event [5]. Pathways and genes preserved in duplicate after a WGD often seem to contribute to evolutionary innovations [6]. For example, anaerobic glucose fermentation in yeast [7] and pigmentation of sh [8] are both associated with duplicate regulatory and biosynthetic pathways derived from WGDs, in which one ancestral pathway evolves a novel function (i.e. neofunctionalization, [9]) while the second pathway retains the ancestral function. Based on the phylogenetic placement of WGDs near the base of speciose clades, it has been argued that these events must have largely contributed to such massive radiations [5,10]. Several genetic mechanisms, including reciprocal gene loss (RGL), have been proposed to explain such patterns, including in yeast [4] and raynned shes [11]. In plants and other organisms, RGL is less often seen then biased fractionation [12,13]. However, more thorough analyses have revealed a signicant lag-time between the WGDs and the ultimate radiation, for example in ray-nned shes (29 000 species) [14]. Santini et al. [14] determined that 10% of the diversity was directly due to the whole genome duplication. The remainder of ray-nned sh diversity (88%) derives from secondary diversication events not associated with the WGD, likely due to later migration events into new habitats following global movements of continents. It has not been tested whether this is a unique scenario, or whether other eukaryotes, including angiosperms, exhibit similar diversication patterns. The evolution of a novel key-trait, millions of years before a lineage radiates, is not an uncommon feature in evolution. For example, most children are now aware that mammals evolved in the shadow of the dinosaurs, with placental mammals even appearing in the Jurassic [15]. In addition, a new study shows lineages involved in the great Cambrian explosion likely evolved tens of millions of years before the radiation [16]. These species were present in such small numbers, thus leaving a currently non-existing fossil record (the Cambrian Conundrum). In this review, we rst discuss recent developments in genomics, phylogenetics, and biogeography highlighting other processes that possible contribute to documented
Current Opinion in Plant Biology 2012, 15:147153

Current Opinion in Plant Biology 2012, 15:147153 This review comes from a themed issue on Genome studies and molecular genetics Edited by Yves Van de Peer and J. Chris Pires Available online 3rd April 2012 1369-5266/$ see front matter # 2012 Elsevier Ltd. All rights reserved. DOI 10.1016/j.pbi.2012.03.011

Radiations and novelty

The origin of novel traits and the associated radiations of large groups of plants have long fascinated scientists, including Darwin in his The Origin of Species. Key traits that dene major radiations vary from the seed and seed plants, the ower and angiosperms, and specialized oral organs and secondary defense compounds for many of our major agriculturally important plant families. For nearly a century [1], whole genome duplications (WGDs) or polyploidy has been hypothesized to be a major mechanism for generating key innovations, novelty and the organismal diversity we see today. The recent ood of genomic data has indeed revealed the ubiquity of WGDs and its apparent association with the
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148 Genome studies and molecular genetics

species radiations in angiosperms. We also state two outstanding questions to be answered: What are the exact phylogenetic placements of WGDs and when did species radiations occur relative to the WGD? We illustrate six examples in the angiosperms where there may be signicant lag-times between WGD and latter radiations. Finally, we discuss the need for future targeted phylogenomic efforts of key sister-group taxa to fully test our WGD Radiation Lag-Time Model (WGD-RLT Model).

be due to the random stochasticity of branching and/or attributable to unequal extinction rates, and that the species-poor sister clade does not represent the ancestral state [28] (see excellent review in this issue [29] discussing extinction rates following WGDs). This observation is consistent with the ray-nned shes data, particularly that there is a signicant delay in species diversication following WGDs [14]. These data are the basis of the WGD-RLT Model.

WGD, plant evolution and diversication

Nowhere is the prevalence of WGD more striking than among the owering plants. All angiosperms share at least two polyploid events in their evolutionary history, with many species being also recently derived polyploids such as cotton, tobacco, wheat and canola [17]. Genome data provides mounting evidence for the occurrence of several ancient WGDs, including one near the origin of the seed plants, one near the origin of the angiosperms and one near the origin of the eudicots [18,19,20]. The rate of molecular evolution can vary widely among lineages and life-history strategies [21] thus, assigning absolute ages to WGDs events can be difcult. The absolute ages are not a necessary component of the WGD-RLT Model. Many of the most important agricultural families are associated with independent WGD(s) such as Brassicaceae (Brassica vegetables and oil-crops), Poaceae (grasses), Fabaceae (legumes), Asteraceae (sunower and lettuce) and Solanaceae (potato and tomato) [22,23]. Each family also has a suite of dening key traits [24] whose origin appears to be correlated with WGD events. The genetic regulation of many dening traits is controlled by duplicated gene networks derived from WGDs [6]. The WGDs that characterize these clades likely occurred at or near the time of their origin [25]. A recent analysis supports that these lineages have greater diversication rates and a higher biodiversity than other lineages without WGDs [22]. Thus, it is tempting to infer that these WGD events drove the evolution of novel traits and species diversication, leading to the global success of these lineages. However, a recent study assessing plant species diversication using 55 000 seed plant species, including many of the large clades sharing a WGD, came to a striking and important conclusion: that major shifts in diversication are not directly associated with entire major named clades (e.g. entire plant family), but rather with slightly nested subclades [26]. In other words: the evolution of a novel key-trait, often evolved substantially before the major radiation of a subset of the newly evolved plant family. In a phylogeny, this would be represented by an asymmetry: a species-rich clade with short divergence times near the origin of the radiation that is sister to a species-poor clade [27]. We acknowledge that such a tree might alternatively
Current Opinion in Plant Biology 2012, 15:147153

Genomics, phylogenetics and biogeography of six major clades

Each group below is dened by a suite of novel traits putatively derived due to independent WGDs, and has an asymmetric phylogeny (i.e. large crown-groups and smaller sister-groups). A major outstanding issue is whether the precise phylogenetic placement of each WGD event cooccurs with the origin of novel traits and/or the major species radiations [22,24], http://www.mobot.org/ mobot/research/apweb. Specically, four inter-related questions must be considered: when did the WGD event occur relative to the lineage splitting? When did a key-trait (or traits) arise relative to the WGD event? When did the apparent radiation occur relative to the WGD (again, with the caveat of past extinction as an alternative [24,28])? What and when were there historical climatic, geological, and dispersion events? We propose these six major plant groups as ideal candidates to test the WGD-RLT Model.
Brassicaceae

The Brassicaceae can easily be recognized by their cruciform-owers with tetradynamous stamens and their mustard-oils [38,39]. There are a number completed genome projects including Arabidopsis thaliana, Arabidopsis lyrata, Brassica rapa and Thellungiella (Schrenkiella) parvula, as well as many new projects underway, such as the BMAP project aimed at generating sequence data for twenty new taxa. A key nding is that likely all Brassicaceae species share a common polyploidy event in their history (Atalpha) [30]). Also, there is a genome triplication (Br-alpha) specic to the lineage containing the Brassica vegetables. Recent phylogenetic analysis shows a major crown-group radiation with a poorly resolved phylogeny [31]. This species-rich crown-group (3700 species) has a worldwide distribution, mostly in temperate regions of the globe but with hypothesized center of origin from the Irano-Turanian region [32,33]. Phylogenetic results also strongly support the small tribe Aethionemeae (41 species), endemic to the Irano-Turanian region, as the sister clade of the family (i.e. species-poor sister group). Current efforts are ongoing to sequence the Ae. arabicum genome. Couvreur et al. [31] found that the radiation of the crown-group Brassicaceae occurred after the split from the Aethionemeae. Interestingly, Aethionemeae contain the novel Met-derived mustard oil glucosinolates, which are unique to the family, are found throughout the crown-group [34]. Both the development of telltale
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WGD Radiation Lag-Time Model Eric Schranz, Mohammadin and Edger 149

cross-shaped ower [35] and mustard-oils of a crucifer [36] are regulated by duplicated pathways from the At-alpha WGD. This suggests that the entire family shares the Atalpha event. Phylogenetic results also show that the Cleomaceae is the out-group to the Brassicaceae, which also has its own unique WGD (Cs-alpha) [37] and there are several ongoing genome projects for this family including Cleome spinosa and Cleome violacea.
Poaceae

Fabaceae

The grass family, with more than 10 000 globally distributed species, are the basis of much of the human diet. A WGD event, rho, has been suggested at the base of the Poaceae [45,46] supported by gene family duplication histories [47], with the Joinvillaceae and Ecdeiocoleaceae as the potentially non-duplicated outgroups. Duplicate gene pairs contribute to key-traits such as the oral spikelet [40] and starchy endosperm seeds [41]. It has been suggested that the Poaceae originated from former Gondwana, what we call now South America and Western Africa in the late Cretaceous [42,43] and occur in a variety of habitats, ranging from dry and arid places to swamp like biotopes. A spread throughout the Gondwanan continent before the split of India could have been the opening window for their global distribution by the end of the Eocene [43]. The small basal clade of the Poaceae, with only 4 species, is Anomochlooideae with two genera Streptochaeta and Anomochloa restricted to South America [42,44]. Though the numbers and arrangement of oral structures in species of Streptochaeta and Anomochloa are different there are conserved patterns in the expression of duplicated MADS box genes [40]. Ongoing projects in this family include the genetics and genomics of Oryza sativa, Zea mays, Brachypodium distachyon and Sorghum bicolor among others.
Asteraceae

The legumes are a large family of 19 500 species, with most contained in the subfamily Faboideae (13 800 species). The Faboideae mostly have typical zygomorphic pea-like (papilionoid) owers [54] legume seedpods and nitrogen-xing nodules. The out-group to the palpinioids is the Mimosoidae, including Acacia. The complete sequencing of several species, including Lotus japonicus, Medicago truncatula, Cajanus cajan and Glycine max show that the Faboideae contain a shared WGD, while G. max also has it own more recent WGD. Genetic mapping data show that peanut (Arachis hypogaea) of the tribe Aeschynomeneae shares the Faboideae WGD [73]. Nodulation has evolved at least three independent times in the Fabaceae [55]. While the two non-Faboideae origins of nodulation do not seem to be associated with a WGD [55], the basal genus Swartzia (180 species) as well as most crown-group species sharing the WGD do have nodules [56,57]. The Tethys Seaway is the center of origin of the Fabaceae in the early Tertiary [58,59,60]. After the continental breaking and the climate cooling the tropical Swartzia was pushed downwards to its current distribution of the neotropics [17]. However due to a lack of research in this basal genus it is not known whether the Faboideae radiated before or after this migration.
Solanaceae

The Asteraceae originated from Patagonia (South America) during the Eocene [48]. With more than 23 600 species the Asteraceae cover 10% of all Angiosperm species [24]. A WGD event occurred near the base of the Asteraceae and at least two within the crown-group: one at in the Mutisieae and one in the Heliantheae [37]. Duplicate regulatory pathways are known to contribute to control of key-traits, such as the daisy-like composite ower (capitulum) [49] and components of the milky white latex [50]. These traits are conserved among all the Asteraceae lineages, including its basal-clade Barnasesioideae. The 91 Barnasesioideae species are endemic to the Asteraceaes center of origin [51]. Although Asteraceaes center of origin is known, there is still ongoing debate about the historical events that contributed to such an extensive global radiation [52]. With 440 and 60 species Goodeniaceae and Calyceraceae, respectively, are the outgroups of the Asteraceae. Full genome projects are underway for sunower (Helianthus) and lettuce (Lactuca sativa), and transcriptome analyses of many other species [53].
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The Solanaceae is known for its edible fruits such as tomato, eggplant, and pepper [61] and their highly poisonous relatives [62]. There are several genome projects completed or underway including for Solanum tuberosum, S. lycopersicum and Petunia inata. The entire family contains 2460 species, with most of these found in the x = 12 clade of the Solanoideae (1940 species) and the smaller sister-group Nicotianoideae (125 species) [63,65]. There is a WGD in the Solanoideae that is shared with the Nicotianoideae based on the extensive genome co-linearity between the two lineages [64]. The WGD may also be shared with the Petuniodeae, the sister-group to this x = 12 clade [63]. The center of diversity of the family is in South America [63], with later migrations world-wide.
Angiosperms

The angiosperms are the most diverse group of land plants with an estimated 225 000 to 425 000 species partitioned into over 400 families, which are characterized by a set of novel characters including the ower, fruits, and seed endosperm [66,67]. There are currently over 20 publicly available angiosperm genomes distributed among several major eudicot and monocot clades. Genomic plant resources can be found at Phytozome (http:// www.phytozome.net/). Amborellaceae, which is a monotypic family containing only Amborella trichopoda, is sister to all other Angiosperms (i.e. species-poor sister-group) [68,69]. The rst draft of this phylogenetically valuable genome was recently released via the Amborella Genome Database (http://www.amborella.org/). The estimated
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150 Genome studies and molecular genetics

Ae ~4 thio 1 s ne pp me a .

The WGD radiation lag-time hypothesis

Each of the aforementioned angiosperm radiations has a species-poor sister-group (Figure 1). This is seen at the family scale (Aethionemeae of the Brassicaceae, Anomochlooideae of the Poaceae, Barnadesioideae of the Asteraceae, Swartzia of the Faboideae, the Nicotianoideae of the Solanaceae), as well on the larger of the phylum of Angiosperms. Based on our earlier brief review of genomics, WGDs, phylogenetics, phylogeography and trait evolution, we outline the WGD-RLM model to potentially explain the observed patterns. In the model (1) a WGD occurs; (2) the WGD contributes to the evolution of key dening trait(s) [2,6]; (3) lineage splitting occurs and persists in the region thought to be the center of origin; (4) after millions of years, a major dispersal event (or events) involving one of the two lineages occurs; (5) the dispersion triggers the now observed crown-group radiation across the globe, while the sister group does not disperse, and may only undergo modest degrees of radiation later. These major dispersion events are likely not driven by the WGDs, but rather by secondary dispersal events triggered by later changing environmental conditions (climate, geological, etc.), evolutionary arms races (e.g. herbivore and plant host), co-radiations (e.g. specialized pollinator and plant host), and migration events into new environments. We acknowledge that it is often difcult to determine which key traits are novel, plus many traits may have evolved convergently (e.g. Fabaceae origins of nodulation). Although, it is interesting to note that several key traits seem to be completely canalized in the species-rich crown groups, but more variable in the speciespoor sister clades [72]. There are certainly going to be examples where WGD does correlate with species diversication and ecological radiation, but as the examples here show (Figure 1), WGD alone may not be sufcient. Instead, the data from the six groups above support Santini et al. [14]. We highlight this model to stimulate targeted phylogenomic projects, specically for genomic projects aimed at the species poor sister-groups. In addition, future analyses need to contrast results to specious groups that lack independent WGDs or are not restricted to the center of origin of the groups. The support for the WGD-RLT is strongest for Brassicaceae, Asteraceae and Poaceae and less so for Faboideae, Solanoideae and Angiosperms.

Brassicaceae Crown group ~3720 spp.

Poaceae Crown group ~11,160 spp.

Ks=0.80

Ks=0.90
Ba ~9 rnad 4 s es pp ioi de . ae

Fabaceae Faboideae ~13,600 spp.

Sw ~1 artz 80 ia sp p.

Asteraceae Crown group ~23,500 spp.

Ks=0.60

Ni ~1 cotia 25 no sp ide p. ae

Solanaceae Solanoideae ~1940spp.

Angiosperms ~225,000 425,000 spp.

Ks=0.60

Ks>3
Current Opinion in Plant Biology

Whole genome duplications and asymmetrical phylogenetic trees: Adaptive radiation crown-groups and species-poor sister groups of six lineages. Each phylogenetic tree is a simplification of the known phylogenies for six major plant groups showing the species-rich crowngroup radiations and species-poor sister-groups (Aethionemeae of the Brassicaceae, Anomochlooideae of the Poaceae, Barnadesioideae of the Asteraceae, Swartzia of the Faboideae, the Nicotianoideae of the Solanaceae and Amborella of the Angiosperms) and the number of species in each clade. Also shown is the potential placement of whole genome duplications (WGDs) represented by circles and the divergence is presented as the mean reported Ks value of duplicate gene pairs.

Phylogenomics of crown-sister-outgroups needed

Evolutionary, ecological and genomic comparisons of species-rich crown groups with their species-poor sister-groups that share a common WGD history could be
Current Opinion in Plant Biology 2012, 15:147153

used to shed light on the radiation lag-time paradox. Ideally this should be done not just for one major plant radiation, but several such as the six discussed and others such as the eudicots. Towards this end, we argue for the need for strategic crown-sister group comparative genome analysis, including out-groups that lack the WGD, to identify important changes in a phylogenomic context. With such analyses, emerging hypotheses about unequal genome fractionation [12], reciprocal gene loss [4], and the contribution of lineage-specic genes [34] could be tested. The success of the crown group, dened by
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Am ~1 bor sp ella p.

An ~4 omo sp ch p. loo i

center of origin for all angiosperms is the supercontinent Gondwana, with Amborella being endemic to the island of New Caledonia in the southwest Pacic Ocean that may not have ever experienced submergence after continental breakup [70]. The Gymnosperms are strongly supported as the sister group with 700900 species [71].

Figure 1

Ks=0.75

de ae

WGD Radiation Lag-Time Model Eric Schranz, Mohammadin and Edger 151

number of species, does not only involve the WGD and novel key traits, but also subsequent evolutionary phenomena including later migration events, changing environmental conditions and/or differential extinction rates. As stated in another review in this issue, polyploid plants are rarely successful [29], and we add that when success does come, it may come late.

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Acknowledgements
We thank Chris Pires, Mike Barker, Stephen Wright, Mike Freeling, and Claude Depamphilis for fruitful discussions on this topic.

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WGD Radiation Lag-Time Model Eric Schranz, Mohammadin and Edger 153

69. Soltis DE, Albert VA, Leebens-Mack J, Palmer JD, Wing RA, dePamphilis CW, Ma H, Carlson JE, Altman N, Kim S et al.: The Amborella genome: an evolutionary reference for plant biology. Genome Biol 2008, 9:402. 70. Jolivet P, Verma KK: Good morning Gondwana. Ann Soc  Entomol Fr 2010, 46:53-61. An interesting paper arguing that areas thought to be submerged after the breakup of Gondwana, like New Caledonia, may in fact not have been completely ooded. This would have important implications for the biogeography and distribution patterns during angiosperm evolution. For example, it would suggest that Amborella as the sister-group to the rest of the angiosperms did not necessarily undergo a long-distance dispersal event in its recent evolution. 71. Lee EK, Cibrian-Jaramillo A, Kolokotronis S, Katari MS, Stamatakis A, Ott M, Chiu JC, Little DP, Stevenson DW,

McCombie WR et al.: A functional phylogenomic view of the seed plants. PLoS Genet 2011, 7:e1002411. 72. Chanderbali AS, Yoo M, Zahn LM, Brockington SF, Wall PK,  Gitzendanner MA, Albert VA, Leebens-Mack J, Altman NS, Ma H et al.: Conservation and canalization of gene expression during angiosperm diversication accompany the origin and evolution of the ower. Proc Natl Acad Sci U S A 2010, 107:22570-22575. The authors describe an important trend in oral evolution in angiosperms, the eventual canalization of gene expression patterns. 73. Bertioli DJ, Moretzsohn MC, Madsen LH, Sandal N, LealBertioli SCM, Guimaraes PM, Hougaard BK, Fredslund J, Schauser L, Nielsen AM et al.: An analysis of synteny of Arachis with Lotus and Medicago sheds new light on the structure, stability and evolution of legume genomes. BMC Genomics 2009, 10:45.

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Current Opinion in Plant Biology 2012, 15:147153