Whole-genome duplications and paleopolyploidy 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 • 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 whole-genome duplication 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 Common ancestor ť Í 2 3~4 5~~6 1~ B 9 10 11 12 13 14 15 IS Ssccfiaromyces lineage £ / 123456 7 89 10 ~li 12 13 14 15 16 ~> r~ \ 3 Kfuyveromyces. lineage 1 2 3 4 5 G 7 S 9 10 11 12 13 14 15 1G Kelliseŕtf/2004, Nature 428 ? 3-156 7 a í! 10 11 1? 13 14 15 16 Y 1 2 3 4 5 B 7 S 3 10 11 12 13 14 15 16 j ____________f____________________ i,/-Í 2 3 4 í> 6 7 B 9 10 11 12 13 14 Ü 16 \ D -»X-»**-X - X^^X » ■ ^X^H -X-< - X-^X-í < XX^»í~chX -x-, l 1 2 3 4 5 6 7 B 9 10 11 12 13 14 15 16 J 3 S. carwJsÄas copyl K wfjttíi *- S. cerevisiae cony2 a) after divergence from K. waltii, the Saccharomyces lineage underwent a genome duplication event (2 copies of every gene and chromosome) b) duplicated genes underwent 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 Ciir 1 i ml; S. cerevisiae chromosome 4 with sister regions in other chromosomes duplicated genome of S. cerevisiae Kellis eta/. 2004, Nature 428 Chr13 Charles Darwin's abominable mystery solved? J ŕ'.' A /'" .■ ď' 7 f' j ■■ "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. MOEEĚE GjiTTinOBpETTTlS F-emB ■—■ Trla*Hlc 245 Mya De Bodt 5r:T3rl3i Earfy -jLľEÍ-E-fc 10 - HF assumed ancient whole-genome duplication events 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 Is Arabidopsis a paleotetraploid? Analysis of the genome sequence of the flowering plant Arabidopsis thaliana Ihc dr-iibldopsIs G-cmm-c Initiative' AGI (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. 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: 0\i ii u- ii P y-l äub^v inferred paleopolyploidy events *R1 OH 225-300+ S0-7D 0 0 11-14 2.5-4.5 R2 15D-170 O i) Sacchariim (sugarcane) Zea {maize) Otyza (rice) Triticum (wheat) Horcteuni (barley) Lyccsersicon (tomato) Solanum (potato) =-5 \ \ Heiiantbits (sunflower? — Lacrüca (lettuce) Glycine (soybean) Meoic&go truncatula 13~15 Q-----0^~2 GossJ'P''Jn' («Am) Arabiricpsis tĎaliana R3 -O- 25-40 -/"V Brassica CuirEntOplnlwi Ir Planí Blobgy Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity Adams and Wendel (2005) Michael Freeling1-3 and Brian C. Thomas2 Genome Res 16 (2006) Widespread genome duplications throughout the history of flowering plants (Cui et a/. 2006) • evidence for ancient genome-wide duplications in the basal angiosperm lineages including Nuphar advena (Nymphaeaceae) and the magnoliids Persea americana {Lauraceae), Liriodendron tulipifera {Magnoliaceae), and Saruma henry i(Aristolochiaceae) • independent genome duplications in the basal eudicot Eschscholzia californica (Papaveraceae) and the basal monocot Acorus americanus (Acoraceaě) • independent duplications documented for ancestral grass {Poaceae) and core eudicot lineages (R2 duplication) • gymnosperms: equivocal evidence for ancient polyploidy in Welwitschia mirabilis(Gnetales) and no evidence for polyploidy in pine {Pinus), although gymnosperms generally have much larger genomes than angiosperms! • an ancient duplication in Nuphar may represent a genome duplication (Rl) in the common ancestor of all or most extant angiosperms, except Amborella X' Gfyciw Whole-genome duplication in rice (Oryzasafivá) Rice-Rice Comparison 10 20 30 Rice Chr02 (Mb) Rice-Rice Comparison Rice Chr01 Chr02 Čhr03 ChrD4 ChrůS ChrOB ChrOr ChrOB ChrOÖ ChrlO Chrli Chr12 Rice ChlOf Chr02 Chr03 ChrW ChrOS chroe Chti>7 ChriJB Chr09 ChrlO Chr11 Chr12 10 20 Rice Chr06 (Mb) 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. duplicated segments in the rice genome Yu et al. (2005) The genomes of Oryza sativa A history of duplications. PLoS Biol 3 Paleopolyploid evolution in Brassica and the Brassiceae Brassica nigra / . \ Brassica cannata|ŕ ■* Brassica juncea /BBCC MSS ^ 4^ Brassica nlftraf*» Hraísica rapa Brassica napus n=19 • comparative genetic analysis allowed the identification of a minimum of 21 conserved genomic units within the Arabidopsis genome, which can be duplicated and rearranged to generate the present-day B. napus genome • the observed duplicated structure of the B. napus genome strongly suggests that the extant Brassica diploid species (n=8,9,10) evolved from a hexaploid ancestor N12 ■:■ I.'I I (MM MM!' i-'-v i ■ i Sis UIKfa N13 '■V-V, \ " / I &m-íĚ DSHt CJUHkp*11«2 I . v|~. . -. J d^-Mil :-j-/% j*1ú7Xi 1 CA Sůl 1 f> i j;& 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 n -.-■ ? i) ■■■-.:■: 8.10 1.« | C E1 h a C C arren&ifts SL ausBiacwn ATS i- ü :: '-- n FE 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 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) translocation (-» fusion) Brassica oleracea (2n=l8) paleotetraploid Lysak etal., 2007 Orychophragmus 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 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)