Whole-genome duplications and paleopolyploidy Populus trichocarpa Whole-genome duplications B mired uced Autotriploid Au tötet rap lo id cjamete Diploid Autotetraploíd Diploids Introgression AUTOPOLYPLOIDY ALLOPOLYPLOIDY Diploids Inviable Fj hybrid Al lotet raploŕd Au tötet raploids Allotetraploid Au tötet rapi oid Fusion of unreduced gametes or somatic genome doubling in zygote X Allotetraploid Allohexaploid Diploid Unreduced ^gamete AJ lotet rapioid Diploids Autotetraploid Al lotet rap! oid Cunient Biology 00 o o C\J _*: o o on o T—1 V) >- J. ai o "O o O 0Ü >- -H s_ a u ~i _L O 03 Examples of allopolyploid speciation Arabidopsis thaliana 2n=2x=10 X A. arenosa 2n=4x=32 Unreduced gamete A sueoica 2n=4x=26 B Spartina maritima 2n=6x=60 X S. aitemiflora 2n=6x=62 S, x townsendii 2n=6x=61 (Sterile) Genome doubling S. anglica 2n=12x=122 Fertile Senech squaiidus 2n=2x=20 X S. vulgaris 2n=4x=40 S. x baxteri 2n=3x=30 (Sterile) Genome doubling S. cambrensis 2n=6x=60 Fertile Gossypium herbaceum 2n=2x=26 X - G. raimondii 2n=2x=26 Diploid hybrid Genome doubling G, hirsutum 2n=4x=52 Current Biology Hegarty and Hiscock 2008, Current Biology 18 Whole-genome duplications of different age neopolyploidy mesopolyploidy paleopolyploidy time Whole-genome duplications in protozoa • Aury etal. (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 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 eta/. 2004, Nature 428 Whole-genome duplications in yeast Co m i nún ancestor / Í 2 3~í Š~G 1~ S 9 10 11 12 13 U 15 16 Saccfiaromycez lineage G / I 2 3 4 5 e 7 B 9 10 11 12 lÜ 14 15 16 \ z' 1 \ 3 Kluyveramyces lineage 2 3 4 5 6 7 S 9 10 11 12 13 14 IS 1B 1 2 3 4 S 6 7 8 9 10 11 12 13 11 15 16 1 J 3 4 5 6 7 8 9 10 11 12 13 14 15 16 3 Kellisertf/2004, Nature 428 í 1 2 3 4 B B ? É S) 10 11 13 13 14 1í 1Ě I x - X X XX x- x x ■ '56 7 B 9 10 11 12 13 14 15 16 Bf 1 3 4 6 h«---*•—» 9 .U 12 13 14 16 2 3 5 7 í 11 13 15 4 / 1 3 4 S 9 10 12 13 14 16 a) after divergence from /£ w/a/ŕ/Ä 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 Duplicated nature of the 5. cerevisiae genome duplicated genome of S. cerevisiae S. cerevisiae chromosome 4 with sister regions in other chromosomes Kellis eta/. 2004, Nature 428 G(ir13 Is Arabidopsis a paleotetraploid? Analysis of the genome sequence of the flowering plant Arabidopsis tha liana Ihcfräbldop^te Genome Initiative'AG I (2000) 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. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla The French-Italian Public Consortium for Grapevine Genome Characterization* Nature 449, 2007 Monocotyledons Dicotyledons Eurosids 1 Eurosids II 0. saliva P. trichocarpa V. vinifera A. thaliana P \ /a V Xß Zf Formation ot the /f palaeo-hexaploid /f genome ^. Flowerin g plants The formation of the palaeo-hexaploid ancestral genome occurred after divergence from monocotyledons and before the radiation of the Eurosids. Star = a WGD (tetraploidization) event. ® Populus ® Arabidopsís ® Caríca ® Vttis Tang et a/. 2008, Science 320 The y 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 efal. 2008, Genome Research The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus) Ming et al. (2008) Nature 452 The papaya genome (372 Mb) is three times the size of the Arabidopsis genome, but contains fewer genes, including significantly fewer disease-resistance gene analogues. Comparison of the five sequenced genomes suggests a minimal angiosperm gene set of 13,311. A lack of recent genome duplication, atypical of other angiosperm genomes sequenced so far, may account for the smaller papaya gene number in most functional groups. Nonetheless, striking amplifications in gene number within particular functional groups suggest roles in the evolution of tree-like habit, deposition and remobilization of starch reserves, attraction of seed dispersal agents, and adaptation to tropical daylengths. Papaya (Caricaceae) and Arabidopsis (Brassicaceae) belong to the Brassicales; both families diverged c. 72 million years ago Genome duplications in rice {Oryza safiva) Rice-Rice Comparison 10 20 30 Rice Chr02 (Mb) Rice Chr01 ChrOZ ChfOJ ChrD4 Chr05 Chr0& Chr07 ChröB Crirtig ChdO Chfii Chr12 B Rice-Rice Comparison Rite 40 ■ Chr01 íř-----"~—~, " • Chr02 *—. ' ^^55aí^_^il^^ ' ■ ChfOJ £30 ŕ ' í**-^> ', ■*'■' ChrfM B> ; . • ,. ',' • ChrOS S 20 . ... «i ' ., . ■ ■ ChrDB ChrtJT cc ' * ~-~l' ' ChrOS 10 • ChrOS ' ''■' ^^-^y^--^ - ChiiO \ --St' Chrti Chi-12 ) 10 20 30 Rice Chr06 (Mb) duplicated segments in the rice genome Duplicated segments of chromosomes 2 (A) and 6 (B) in Oryza sativa subsp. indica. Shown on the x-axis is the position of a gene on the indicated chromosome, and shown on the y-axis is the position of its homolog on any of the rice chromosomes, with chromosome number encoded by the colors indicated at the right. Yu et al. (2005) The genomes of Oryza sativa A history of duplications. PLoS Biol 3 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) 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. MOE&SE Gym no perms Arglo&[HmiE - Mareceats (Cow) EUdlCBlE ApotÉ Cenozolc ■55 UfB z F 2R 1H assumed ancient as.5 93.5 99.5 112 125 Cretata-DUE Í45 öya Tj.-or an Gens.Tianlaľi whole-genome Ail ;r rc::3i i duplication events Lafe JĽ'-aES^ — :ae Mj3 Ear-y TnasHlc 2*5 Mja tet< íl. 200 id DIG s^eclea Fal»D(zotc De Bod 5 1 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 Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event Jeffrey A. Fawcett*1*'1, Steven Maerea'b'1, and Yves Van de peera'b'2 PNAS 106 (2009) ^Department of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Gent, Belgium; and department of Plant Biotechnology and Genetics, Ghent University, 9052 Gent, Belgium 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 ? Phylogenese tree of flowering plants with assumed W6Ď events > 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) Jurassic Cretaceous Tertiary orange bars = dating of WGDs in literature > the KT extinction event -extinction of 60% of plant species, as well as a majority of animals, including dinosaurs i r-iv 1J5my ■TT my item» — >9äHly m c i? =. 2. Physcomilrslla palans Moeb Eschsctiolzia califomica Solenurn tuberosum Solanum lycoparsicum Lacüjca saliva Euasferlds II Vitis vimľera Lotus japonieus Medicago iruncatula Glycine max Papulus uichücarpa Salix Gossypium htrsuüjm Carica papůya Arabidopsis thaliana Acorus amencanus Musa spp. Oryz3sativa Sorghum btCOlor \ m B S Š' m c o ň 3 ■r- ./i i í a, u Q Fawcett et al., PNAS 106 (2009) Whole-genome duplication (W6Ď) events in angiosperm evolution Eudicots Fabidae Malvidae Asteríds r Monocots Magnoliids ť--------------- Soltis and Soltis (2009), Annu. Rev. Plant Biol. Whole-genome duplication, diploidization, and the consequences Genome evolution through cyclic polyploidy Dipols* Fo \r -j : \ Duplicate gene ioes Fovpols) Duplicate gene ioes- Cu-*if: C*j ii u- ii P y-l äub^v Gene duplicate retention after WGD due to rapid functional evolution ^. al n>v OA a Non-WGD WGD a1 a2 Polyploid Semon and Wolfe (2007) .a. a2 S u bf Lr rationalization a1 _Qz^ a2 IMeofunctionaiization ô__s* al a2 Sub-neofunctIU-l- í [utttfpftníd ' W14SE1 lim n (iFBSř llpWtľZrJEHrc U ĽA ' !iľV* HlMTh lotMAMHStt 'J 5LR1Ľ ĽJCSb y ZMiilít lAKUli ťf l«tl JJluV'm.- iWľľ'í L] j*ji.Lfl* uwa pWITCE' BiíJíflípOl JJÉ1 b, .v-:■'.-, ,osul ^ IM,-,,..;.. Park\r\ et a/. 2005 Paleopolyploid evolution in ßrassiceae analyzed by comparative chromosome painting Chromosome triplication found across the tribe Brassiceae Martin A, Lysak,13-4 Marcus A. Koch,2 Ales Pecinka,3 and Ingo Schubert3 'jodrell Laboratory, Royal Botanic GaFdens, Kew, Richmond, SuFFey TM9 3AB, United Kingdom; 2Institute for Plant Sciences, University of Heidelberg, 69 J20 Heidelberg, Germany;JInstitute of Plant Genetics and Crop Plant Research (IPK), 06466 Gatessieben, Germany A. thaliana chromosome 4 0 An 8.7-Mb BAC contig of Arabidopsis thaliana was used for comparative painting in 21 species of the tribe Brassiceae : Genome Research 15: 516-525 (2005) 8.7 Mb The 8.7-Mb segment was found triplicated in the majority of Brassiceae species 2n = 14, 16, 18, 20, 22, 28, 30, 34, 36, 38 rzKľfy =-!» I IB El Ei Q C G. onentafis G S. Mustriacum ■V as 41 ľ 13 ja Fl F2 H H Diplotaxis erucoides (2n=l4) Moricandia arvensis (2n=28) Congruence between cytogenetic and molecular phylogenetic data. Brassiceae have a common hexaploid ancestor. hexaploid ancestor c: Noccaea montana Lepidium virginicum Calepina irregularis Conringia planisiliqua Sisymbrium altissimum Cakile maritima Psychine stylosa Carrichtera annua Vella spinosa Rapistrum rugosum Cordylocarpus muricatus Sinapis arvensis T~ Brassica nigra Brassica nigra Sinapis alba i: 4 rt Phylogenetic relationships based on the chloroplast 5-trriL (UAA)-trď(GAA) region Sinapis alba |~ Diplotaxis siifolia Sinapidendron frutescens — Eruca sativa — Moricandia arvensis T~ Diplotaxis erucoides Erucastrum gallicum Raphanus sativus Raphanus sativus Raphanus sativus Brassica oleraceae Brassica rapa L— Brassica juncea C g '-4-J U E o c QJ CD T^^lS Lysak et al. 2005 Further cytogenetic evidence of the paleohexaploidy event in the ancestry of Brassiceae BAC contig covering the upper arm of A. thaliana chromosome 3 used for comparative painting in Brassiceae spp. Physorhynchus chamaerapistrum (2n=32) Morisia monanthos (2n=l4) ^j translocation (-» fusion) Brassica oleracea (2n=l8) paleotetraploid Lysak et al. 2007 OrychophraQmus violaceous (2n = 24) Congruence between phylogenetic and cytogenetic data? Paleotetraploid origin of Orychophragmus hexaploid ancestor {Lysakefal. 2005) tetraploid ancestor 9 ä 57 f<5 91 100 l;4 í i 100 92 100 100 Brassica rapa Raphanus raphanistrum Moricantíia arvensis Brassioa elongate Cakite maritima Erucaria hispanica Brassica nigra Sinapis pub&scens Erucastrum canariertse Coincya monensis Crambe hispanica CratWe orienlsiis Carricníera annua Veita spino sa Succowia batearica Fortiiynia twngei Ziila spino sa Sctiouwia purpurea 100 Caiepina irregularis Conringia orientalis Conringia perfoiiata CO S o c/i c/i o O Orychophragmus vbiaceus Sisymbrium irio Sisymbrium officinale v'true" diploids /(Lysak et al. 2005) modified from Warwick <& Sauder 2005 'Recent' paleopolyploidy event in soybean glycine max) • 2n=40 karyotype, derived from at least two rounds of whole-genome duplication or polyploidy events • cytogenetically, soybean behaves like a diploid and has disomic inheritance • fluorescence in situ mapping of seven putatively gene-rich BACs from chromosome 19 revealed that there is extensive homeology with another chromosome pair FISH mapping of seven BACs from chromosome 19 on pachytene chromosomes from soybean. BACs were localized on the long arm of chromosome 19. The inset highlights secondary signals from the putative homeologous chromosome. Walling etal. 2006 r ' '/■'sír''' ?-<;-> Whole-genome duplications in the evolution of flowering plants (and Brassicaceae) ancG 3ancG ISancG & M 6ancG r é I2anc(i 36 ancG Lineage II £ Cahcaceae Cieomaceae Aethionemeae Lineage I Brassi ceae other tribes Lineage III Brassicaceae Karyotype evolution in Australian Camelineae species / Stenopetalum nutans (n=4) ? • t Arabidella eremigena (n=5) m % Ballantinia antipoda (n=6) Australian Camelineae species experienced a whole-genome duplication followed by chromosome number reduction AK1 2 3 4 5 6 7 8 Ancestral Crucifer Karyotype (n=8) $*< >< >* «=^> All 24 genomic blocks (GBs) of the ACK (n=8) are duplicated in Stenopetalum nutans. Out of 48 GBs, 39 remained intact, whereas 9 were split into two or three sub-blocks. In Ballantinia, only 18 GBs are duplicated; 6 GBs were found as single copies. Sn1 Sn2 Sn3 Sn4 r45SrDNA« Mlb 12. S2 IIa 45S rDNA Alb Bl< Blb 02 J5S rDNA Pl LI iií x hkSN2 C2 XI b Wla Xl< Wlb VI S2 T2 hkSN3 AK1 ^^ ^ * n\ í. Sn2-v J.. * T^ Sn3N Analysis of single-copy nuclear genes shows the retention as well as the loss of gene paralogs after the WGD event(s) CAD5 Stenopetatum nutans 76272 c3 Stenopetatum nutans 0/3929 ca Stenopetalum nutans 86929 c3 Stenopetalum vetutinum c8 Stenopetalum nutans aesac Baitantinia antipoda es Baitantinia antipoda c4 Pachyctaclon fastigiata Pachyctaclon exHis Boectoeia hofboeltii Cmcihimataya motUssima Transtienngia bursifoHa ssp. ůursí/otiB ms Stenopetalum vetutinum c2 Stenepefeium vetutinum c7 Arabidetla eremigena <* Arabidetla eremigena ce CapseSta bursapestoris d AraĎŕítopsrs r.'"o.Vs/m Araůrdops/s Jyrsrs ssp. tyra/a Otimarabidapsis cabuEcs Stenopetatum nutans ism c: Stenopetatum nutans 86929 c; Stenopetatum nutans 76272 * Pachyctaclon fastigiata Pachyctaclon exHis Baitantinia antipoda 0 Stenopetalum vetutinum d Arabidetla eremigena c3 Arabidetla eremigena d Brass ■'■.-: rapa ssp. pefcinemsrs i. ■=.■;.-.■,■■'.: ■■■:? ape/aŕum c-Lspiríium apetatum c3 Pachyctaclon fastigiata 4/1 Pscňycfatíon en/aí 1/1 Pscňycfatíon tatisiliqua 1/5 Pscňycfatíon wsflfj" 1/1 ftacňycísfían etíeesemsnií 6/1 Pacňycíatíon ejtríŕs Stenopetalum vetutinum d Baitantinia antipoda c3 Stenopetalum nutans 76272 c3 Stenopetalum nutans 06929 c3 Stenopetalum nutans 7*212 es Stenopetalum nutansiezrzcA Stenopetalum nutans e6929c7 Stenopetalum nutans Arabidetla eremigena es Arabidetla eremigena d Crucihimataya molüssima c TVansůejTJTfl/a bursifolia c3 öoeeftera /nnbosDv d CapseBa bursa-pastoňs d CapseJJa Ďtrrsa-pasŕcrá c2 AraĎŕítopsrsffraifara Arabŕdcpsj's ■lyra/a ssp. lyraŕa c 1 Oiimarabidopsis cabuUca c3 Ortmsratitícpsis cabulica tZ Pachyctaclon en/sň 1/1 físcftyc/atíon wsflfe" 1/1 Pscňycfatíon tatisiliqua 1/5 Pscňycfatíon ncvsezeŕantŕwe 271 Pscňycfatíon Äsírffiíaía' 4/1 ŕbc/íycíadon steŕfote 2/4 Pachyctaclon exUis Brassica napus Thetíungietla spp. d Lepiríium apetatum d Mesopolyploid WGD events in Brassicaceae revealed by comparative chromosome painting Biscutelleae whole-genome duplication whole-genome triplication > Brassiceae Cochlearieae (Cochlearia pyrenaica, 2n=12) Iberideae [iberis umbellata, 2n=18) Physarieae Lysak et al. 2005, 2007 Model of genome evolution in Brassicaceae: cyclic whole-genome duplication and diploidization n=8-12 n=8 chromosome no reduction WGD n=4 < n=5 WGD AK1 3 ] 4 3 I 7 1 AK1 1 i 4 * * J t n=16 chromosome no. reduction n=6 I: 73 72 Summary '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)