(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 • 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) 13 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; Clark and Donoghue (2017) Proc R Soc 399 – 381 319 – 297 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 (e.g.  - gamma WGD) De Bodt et al. 2005 Archaefructus liaoningensis (140 million year old fossil)  (319 – 297) Afropollis (245 million year old angiosperm pollen) lag 27 – 65 million years diversification (267 – 247) 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) Possible establishment of polyploid plants following the K/Pg mass extinction (66 million y. ago) Lohaus and Van de Peer (2016) Curr Opin Pl Biol ➢ 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 in land plants Van de Peer et al. (2017) Nat Review Zhang et al. (2017) Nature Orchids probably share a common WGD driving the early divergence of the family • largest vascular plant family • c. 28,000 species • 736 genera Huang et al. (2016) MBE Multiple WGDs across the Asteraceae family tree • the second largest family of vascular plants • some 24,700 species • enormous karyological variation 180 different mitotic chromosome counts • chromosome numbers from n = 2 to c. n = 216 Whole-genome duplications, 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 (49 million y. ago) contributed to the evolution of the tomato fruit phylogeny of xyloglucan endotransglucosylase/hydrolases (XTHs) T Solanaceae-specific genome triplication  core eudicot shared hexaploidy Gene and genome duplications, key innovations and coevolution Edger et al. (2015) PNAS • WGDs (core Brassicales, Brassicaceae) • chemical arms race • plants - glucosinolates • butterflies – countertactic (detoxification) • repeated escalation of key innovations (glucosinolate synthesis) → diversification in Brassicales plants and Pierinae butterflies over 80 million years Gene and genome duplications, key innovations and coevolution Edger et al. (2015) PNAS Whole-genome duplication and diploidization Wendel et al. (2016) Genome Biol Whole-genome duplication and diploidization Schranz et al. (2012) Curr Opin Plant Biol The WGD Radiation Lag-Time Model WGD NEO-MESOpolyploid MESOpolyploid NEO- PALEOpolyploid PALEOpolyploid Cytogenomic features of post-polyploid genome diploidization • recurrent WGDs • different age of WGDs • different diploidization rates T25K16 F6F3 F22L4 T1N6 T6A9 F22D16 F10O3 F15K9 F21B7 F21M11 F20D22 F19P19 T1G11 F13M7 T7A14 T25N20 F3F20 T20M3 T21E18 T2D23 F12K11 F22G5 F24B9 T6D22 T23G18 T27G7 F22O13 F7G19 T12M4 T31J12 F14J9 F21M12 F14N23 F20B24 T16B5 T19D16 T23J18 F12F1 T28K15 T12C24 F13K23 F3F19 T6J4 F13B4 F7A19 F14L17 T5E21 F10B6 T15D22 T16N11 F7H2 T24D18 F3O9 F19K19 F17F16 F20D23 T13M22 F1L3 F11A6 T10F20 T10O22 F15H18 F25I16 F14D16 T29M8 F18O14 #1 #2 #1 #2 #1 #2 #3 #1 #2 #3 Cytogenetic evidence for biased subgenome fractionation during post-polyploid diploidization. Tetraploid Hexaploid MBE 31 (2013) Class IIClass I 33 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 34 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 36 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 37 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 38 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 Australia: 15 genera, 47 species New Zealand: Pachycladon, 11 species The allopolyploid origin evidenced by single-copy nuclear gene phylogenies 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 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 ♂♀ Crucihimalayeae n = 8 Descurainieae/ Smelowskieae n = 7 allotetraploid ancestor n = 15 INTER-TRIBAL HYBRIDIZATION Pachycladon n = 10 crown group n = 4 - 7 n = 12 LONG DISTANCE DISPERSAL (15 genera / 42 spp.)Mandáková et al. (2010) Plant Cell (2010) BMC Evol Biol (2017) Mol Ecol Arabidella n = 24 Mesotetraploid Origin, Diploidization and Diversification of the Microlepidieae 2n = 4x = 30 2n = 8, 10, 12, 14, 20 (1 / 11) (1 / 3) AUTOPOLYPLOIDY c. 90 (-100) endemic spp. Does Ancient Polyploidy Explain the Rapid Species Radiation in Heliophila ? 45 Whole-Genome Triplication in the Southern African Tribe Heliophileae Mandakova et al. (2012) Taxon H. amplexicaulis (n = 11) Mandáková et al. (2017) Plant J  mesohexaploidy  mesotetraploidy Lineage-Specific Mesopolyploid WGDs in Brassicaceae Existing species and genomic diversity of many Brassicaceae clades result from post-polyploid diploidizations n = 14 n = (10, 12) 14 21 7, 8, 9, 10, 11, 12, 13, … 15 4, 5, 6, 7, 10, 12 Thelypodieae 26 g.: 244 spp. Brassiceae 47: 227 Microlepidieae 17: 56 Physarieae 7: 133 16 6, 8, 9 Biscutelleae 2: 46 (or more) 24 4, 5, 6, 7, 10, 12 Heliophileae 1: 100 21 or 24 (8, 9) 10, 11 (13) mesoHEXAPLOIDSmesoTETRAPLOIDS Two hypotetraploid Cardamine species: recent and starting diploidizations via descending dysploidy n = 16 n = 12n = 15 Mandáková et al. (2013) Plant Cell Mandáková et al. (2016) Am J Bot two Cardamine spp. 4x Cardamine cordifoliaCardamine pratensis n = 8 Cardamine 2x WGD sympatric parapatric / allopatric 2x 6x 12x 6x POST-POLYPLOID DIPLOIDIZATION, DESCENDING DYSPLOIDY & SPECIATION 4x n = 4n = 2 n = 6 n = 6 n = 6 n = 5 n = 2 n = 3n = 4 n = 6 n = 4 n = 3 n = 9 n = 6 n = 8 Speciation and diversification driven by post-polyploid diploidization via descending dysploidy ‘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).