(Paleo)Polyploidy – When Things Get Bigger Whole-genome duplications HegartyandHiscock2008, CurrentBiology18 AUTOPOLYPLOIDY ALLOPOLYPLOIDY Hegarty and Hiscock 2008, Current Biology 18 Examples of allopolyploid speciation Leitch & Leitch (2008) Science 320 Evolutionary significance of polyploidy Whole-genome duplications of different age time paleopolyploidy mesopolyploidy neopolyploidy time 6 increasingploidylevels PALEOpolyploidy MESOpolyploidy NEOpolyploidy Multiple Whole-Genome Duplication Events, Diploidization and Extant Karyotype Structure chromosome number decrease genome diploidization • Most of the allopolyploidization events identified here occurred in the Late Miocene, simultaneous with or following the well documented expansion of the C4 grasslands. • The dominant species of modern C4 grasslands are members of Andropogoneae, and most are allopolyploid. Many of these ecological dominants whose origin is dated to about 10.5 million years ago (mya) correlates closely with the date when C4 species came to dominate grasslands in Africa and Southern Asia (Pakistan), also estimated about 10–11 mya; the expansion in North America is dated about 7 mya. • Allopolyploidy is thus correlated with ecological success. Allopolyploidy, diversification, and the Miocene grassland expansion Estep et al., PNAS (2014) T. aestivum T. turgidum Ae. tauschii    Model of the phylogenetic history of bread wheat (Triticum aestivum; AABBDD). Three rounds of hybridization/polyploidy. Marcussen et al. (2014), Science • Aury et al. (2006) analyzed the unicellular eukaryote Paramecium tetraurelia • most of 40,000 genes arose through at least 3 successive whole-genome duplications (WGDs) • most recent duplication most likely caused an explosion of speciation events that gave rise to the P. aurelia complex (15 sibling species) • some genes have been lost, some retained • many retained (duplicated) genes do not generate functional innovations but are important because of the gene dosage effect Whole-genome duplications in protozoa Whole-genome duplications in yeast • genome comparison between two yeast species, Saccharomyces cerevisiae (n=16) and Kluyveromyces waltii (n=8) • each region of K. waltii corresponding to two regions of S. cerevisiae • the S. cerevisiae genome underwent a WGD after the two yeast species diverged • in nearly every case (95%), accelerated evolution was confined to only one of the two paralogues (= one of the paralogues retained an ancestral function, the other was free to evolve more rapidly and acquired a derived function) Kellis et al. 2004, Nature 428 Whole-genome duplications in yeast a) after divergence from K. waltii, the Saccharomyces lineage underwent a genome duplication event (2 copies of every gene and chromosome) b) duplicated genes were mutated and some lost c) two copies kept for only a small minority of duplicated genes d) the conserved order of duplicated genes (nos. 3-13) across different chromosomal segments e) comparison between genomes of S. cerevisiae and K. waltii reveals the duplicated nature of the S. cerevisiae genome Kellis et al. 2004, Nature 428 Duplicated nature of the S. cerevisiae genome duplicated genome of S. cerevisiae S. cerevisiae chromosome 4 with sister regions in other chromosomes Kellis et al. 2004, Nature 428 First evidence of a WGD in plants What does the duplication in the Arabidopsis genome tell us about the ancestry of the species? As the majority of the Arabidopsis genome is represented in duplicated (but not triplicated) segments, it appears most likely that Arabidopsis, like maize, had a tetraploid ancestor. …The diploid genetics of Arabidopsis and the extensive divergence of the duplicated segments have masked its evolutionary history. AGI (2000) 14 Arabidopsis Species Are „Paleotetraploids“ with 8 or 5 Chromosomes AGI (2000) Nature, Hu et al. (2011) Nat Genet segmental duplications in the A. thaliana genome Nature 449, 2007 The formation of the palaeo-hexaploid ancestral genome occurred after divergence from monocots and before the radiation of the Eurosids. Star = a WGD (tetraploidization) event. β γ αp The γ triplication may have been an ancient auto-hexaploidy formed from fusions of three identical genomes, or allo-hexaploidy formed from fusions of three somewhat diverged genomes. Tang et al. 2008, Genome Research WGD events in seed plants and angiosperms Jiao et al. (2011) Nature Phylogenetic Tree of Sequenced Genomes with Whole Genome Duplications Marked CoGePedia (http://genomevolution.org/wiki/) Theres is evidence of ancient polyploidy throughout the major angiosperm lineages. It means that a genome-scale duplication event probably occurred PRIOR to the rapid diversification of flowering plants Charles Darwin’s abominable mystery solved? "The rapid development as far as we can judge of all the higher plants within recent geological times is an abominable mystery." (Charles Darwin in a letter to Sir Joseph Hooker, 1879) assumed ancient whole-genome duplication events De Bodt et al. 2005 Archaefructus liaoningensis (140 million year old fossil) The leaf-like structures on the stem are pods containing the seeds, a characteristic unique to flowering plants. PNAS 106 (2009) Could WGD event(s) help plants to survive the mass extinction (one or more catastrophic events such as a massive asteroid impact) at the Cretaceous– Tertiary boundary ? Genome Res (2014) Phylogenetic tree of flowering plants with assumed WGD events Fawcett et al., PNAS (2009), Vanneste et al., Genome Res (2014)  WGDs clustered around the Cretaceous–Tertiary (KT) boundary  the KT extinction event - the most recent mass extinction (one or more catastrophic events such as a massive asteroid impact and/or increased volcanic activity)  the KT extinction event extinction of 60% of plant species, as well as a majority of animals, including dinosaurs Whole-genome duplication, diploidization, and the consequences Adams and Wendel (2005) Genome evolution through cyclic polyploidy Gene duplicate retention after WGD due to rapid functional evolution Semon and Wolfe (2007) Consequences of WGD events: the Solanaceae-specific genome triplication contributed to the evolution of the tomato fruit phylogeny of xyloglucan endotransglucosylase/hydrolases (XTHs) T Solanaceae-speficific genome triplication  core eudicot shared hexaploidy 23 n = 5 n = 6 n = 7 n = 8 (n = 7) n = 4 n = 8 Evolution of the Ancestral Crucifer Genome – ANCIENT POLYPLOIDS 4x or 6x n = (15) 16 or (21) 24 whole-genome duplication descending dysploidy block resfuffling I 24 Lysak et al. (2005) Genome Res, (2007) Plant Physiol Diplotaxis erucoides 2n = 14 III I II Morisia monanthos 2n = 14 Moricandia arvensis 2n = 28 III I II Brassica oleracea 2n = 18 I III II I II IIIParkin et al. (2005) Genetics Brassica napus (AACC, n = 19), A genome (N1-N10) Brassicas Are Ancient Hexaploids (Mesopolyploids) Diploidization in Brassica is marked by the asymmetrical evolution of polyploid genomes 26 The density of orthologous genes in three subgenomes (LF, MF1 and MF2) of B. rapa compared to A. thaliana. Wang et al. (2011) Nat Genet 27 Three B. rapa Subgenomes Contain Genome Block Associations Unique to the tPCK Ancestral Genome n = 7 translocation Proto-Calepineae Karyotype tPCK Cheng et al. (2013) Plant Cell, Mandakova and Lysak (2008) Plant Cell 71genomic blocks 28 n = 7 n = 21 WGT Whole-Genome Triplication Spurred Genome and Taxonomic Diversity in Brassica and Tribe Brassiceae n = 15 n = 8 n = 7 n = 9 n = 11 n = 14 n = 10diversification tPCK – ancestral diploid genome of Brassica 6x Cheng et al. (2013) Plant Cell WGT MBE 31 (2013) Class IIClass I Polyploid Evolution in Australian and New Zealand Crucifer Genera Pachycladon 2n = 20 Ballantinia Stenopetalum 2n = 8-12 Polyploid Origin of Pachycladon (n=10) P. enysii P. novae-zelandiae P. cheesemanii P. exile 10 chromosomes 48 blocks 16 chromosomes 48 blocks Ancestral Karyotype (4x) Mandakova, Heenan and Lysak (2010) BMC Evol Biol ~ 1 – 2 mya Stenopetalum nutansBallantinia antipoda Stenopetalum lineare U2 T2 S2 V1 W1a X1a W1b X1b J1 I1 M1a K1 L1 U1 4 chromosomes 48 blocks 5 chromosomes 44 blocks 6 chromosomes 40 blocks ACK, 4x16 chromosomes 48 blocks ~ 6 – 9 mya Mandakova et al. (2010) Plant Cell 33 Stenopetalum ♀ Arabidella, Ballantinia, Blennodia, Cuphonotus, Geococcus, Harmsiodoxa, Microlepidium, Phlegmatospermum Menkea (n = 6) ancestral allopolyploid genome (n = 14 ?) Crucihimalayeae (n = 8) Smelowskieae (n = 6) (n = 4, 5) (n = 5, 6, 7)  Allopolyploid origin of the Microlepidieae Mandáková et al., unpublished ndhF phylogeny ACK-like allotetraploid (n ~ 16) Pachycladon (n = 10) Stenopetalum (n = 4) Reshuffling of 2 x 24 Genomic Blocks in Polyploids of Different Age ~ 1 – 2 mya ~ 6 – 9 mya c. 90 (-100) endemic spp. Does Ancient Polyploidy Explain the Rapid Species Radiation in Heliophila ? 36 Whole-Genome Triplication in the Southern African Tribe Heliophileae Mandakova et al. (2012) Taxon H. amplexicaulis (n = 11) 37 Whole-Genome Duplications Drive Genome Diversification α Cleomaceae Aethionemeae Smelowskieae Lepidieae Descurainieae AUS Camelineae, Pachycladon Boechereae Halimolobeae OreophytoneaePhysarieae Microlepidieae Alyssopsideae YinshanieaeCardamineae Erysimeae Anchonieae Euclidieae Dontostemoneae Chorisporeae Hesperideae Anastaticeae Buniadeae Biscutelleae Eutremeae Thlaspideae Brassiceae Thelypodieae Isatideae Sisymbrieae Cochlearieae Alysseae Aphragmeae Megacarpaeeae Notothlaspideae Iberideae Heliophileae Noccaeeae Conringieae Kernereae Asteae Schizopetaleae Eudemeae Calepineae Arabideae Cremolobeae Lineage III Lineage I Lineage II expanded Lineage II ‘Many more, if not all, higher plant species, considered as diploids because of their genetic and cytogenetic behaviour, are actually ancient polyploids’ (Paterson et al. 2005).