Island species radiation and karyotypic stasis in Pachycladon allopolyploids

. 2010 Nov 29 ; 10 () : 367. [epub] 20101129

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid21114825

BACKGROUND: Pachycladon (Brassicaceae, tribe Camelineae) is a monophyletic genus of ten morphologically and ecogeographically differentiated, and presumably allopolyploid species occurring in the South Island of New Zealand and in Tasmania. All Pachycladon species possess ten chromosome pairs (2n = 20). The feasibility of comparative chromosome painting (CCP) in crucifer species allows the origin and genome evolution in this genus to be elucidated. We focus on the origin and genome evolution of Pachycladon as well as on its genomic relationship to other crucifer species, particularly to the allopolyploid Australian Camelineae taxa. As species radiation on islands is usually characterized by chromosomal stasis, i.e. uniformity of chromosome numbers/ploidy levels, the role of major karyotypic reshuffling during the island adaptive and species radiation in Pachycladon is investigated through whole-genome CCP analysis. RESULTS: The four analyzed Pachycladon species possess an identical karyotype structure. The consensual ancestral karyotype is most likely common to all Pachycladon species and corroborates the monophyletic origin of the genus evidenced by previous phylogenetic analyses. The ancestral Pachycladon karyotype (n = 10) originated through an allopolyploidization event between two genomes structurally resembling the Ancestral Crucifer Karyotype (ACK, n = 8). The primary allopolyploid (apparently with n = 16) has undergone genome reshuffling by descending dysploidy toward n = 10. Chromosome "fusions" were mediated by inversions, translocations and centromere inactivation/loss. Pachycladon chromosome 3 (PC3) resulted from insertional fusion, described in grasses. The allopolyploid ancestor originated in Australia, from the same or closely related ACK-like parental species as the Australian Camelineae allopolyploids. However, the two whole-genome duplication (WGD) events were independent, with the Pachycladon WGD being significantly younger. The long-distance dispersal of the diploidized Pachycladon ancestor to New Zealand was followed by the Pleistocene species radiation in alpine habitats and characterized by karyotypic stasis. CONCLUSIONS: Karyotypic stasis in Pachycladon suggests that the insular species radiation in this genus proceeded through homoploid divergence rather than through species-specific gross chromosomal repatterning. The ancestral Pachycladon genome originated in Australia through an allopolyploidization event involving two closely related parental genomes, and spread to New Zealand by a long-distance dispersal. We argue that the chromosome number decrease mediated by inter-genomic reshuffling (diploidization) could provide the Pachycladon allopolyploid founder with an adaptive advantage to colonize montane/alpine habitats. The ancestral Pachycladon karyotype remained stable during the Pleistocene adaptive radiation into ten different species.

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Devos KM. Grass genome organization and evolution. Curr Opin Plant Biol. 2009;13:1–7. PubMed

Schnable PS. et al.The B73 maize genome: complexity, diversity and dynamics. Science. 2009;326:1112–1115. doi: 10.1126/science.1178534. PubMed DOI

Paterson AH. et al.The Sorghum bicolor genome and the diversification of grasses. Nature. 2009;457:551–556. doi: 10.1038/nature07723. PubMed DOI

The International Brachypodium Initiative. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature. 2010;463:763–768. doi: 10.1038/nature08747. PubMed DOI

Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Quraishi UM, Calcagno T, Cooke R, Delseny M, Feuillet C. Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell. 2008;20:11–24. doi: 10.1105/tpc.107.056309. PubMed DOI PMC

Bowers JE, Chapman BA, Rong J, Paterson AH. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature. 2003;422:433–438. doi: 10.1038/nature01521. PubMed DOI

Barker MS, Kane NC, Matvienko M, Kozik A, Michelmore RW, Knap SJ, Rieseberg LH. Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol Biol Evol. 2008;25:2445–2455. doi: 10.1093/molbev/msn187. PubMed DOI PMC

Ming R. et al.The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus) Nature. 2008;452:991–996. doi: 10.1038/nature06856. PubMed DOI PMC

Lysak MA, Koch MA, Pecinka A, Schubert I. Chromosome triplication found across the tribe Brassiceae. Genome Res. 2005;15:516–525. doi: 10.1101/gr.3531105. PubMed DOI PMC

Mandáková T, Joly S, Krzywinski M, Mummenhoff K, Lysak MA. Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell. 2010;22:2277–2290. doi: 10.1105/tpc.110.074526. PubMed DOI PMC

Schranz ME, Mitchell-Olds T. Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell. 2006;18:1152–1165. doi: 10.1105/tpc.106.041111. PubMed DOI PMC

Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, dePamphilis CW, Wall PK, Soltis PS. Polyploidy and angiosperm diversification. Am J Bot. 2009;96:336–348. doi: 10.3732/ajb.0800079. PubMed DOI

Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoond PB, Rieseberg LH. The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA. 2009;106:13875–13879. doi: 10.1073/pnas.0811575106. PubMed DOI PMC

Moore DM. Chromosome numbers of Falkland Inslands angiosperms. Br Antarct Surv Bull. 1967;14:69–82.

Carr GD. In: Evolution and speciation of island plants. Stuessy TF, Ono M, editor. Cambridge: University Press; 1998. Chromosome evolution and speciation in Hawaiian flowering plants; pp. 5–47. full_text.

Stuessy TF, Crawford DJ. In: Evolution and speciation of island plants. Stuessy TF, Ono M, editor. Cambridge: Cambridge University Press; 1998. Chromosomal stasis during speciation in angiosperms of oceanic islands; pp. 307–324. full_text.

Weiss H, Sun B-Y, Stuessy TF, Kim CH, Kato H, Wakabayashi M. Karyology of plant species endemic to Ullung Island (Korea) and selected relatives in peninsular Korea and Japan. Bot J Linn Soc. 2002;138:93–105. doi: 10.1046/j.1095-8339.2002.00013.x. DOI

Carr GD, Kyhos DW. Adaptive radiation in the Hawaiian silversword alliance: II. Cytogenetics of artificial and natural hybrids. Evolution. 1986;40:969–976. PubMed

Heenan PB, Mitchell AD. Phylogeny, biogeography, and adaptive radiation of Pachycladon (Brassicaceae) in the mountains of South Island, New Zealand. J Biogeogr. 2003;30:1737–1749. doi: 10.1046/j.1365-2699.2003.00941.x. DOI

Heenan PB. A new species of Pachycladon (Brassicaceae) from limestone in eastern Marlborough, New Zealand. New Zeal J Bot. 2009;47:155–161. doi: 10.1080/00288250909509803. DOI

Heenan PB, Mitchell AD, Koch M. Molecular systematics of the New Zealand Pachycladon (Brassicaceae) complex: generic circumscription and relationship to Arabidopsis sens. lat. and Arabis sens. lat. New Zeal J Bot. 2002;40:543–562. doi: 10.1080/0028825X.2002.9512815. DOI

McBreen K, Heenan PB. Phylogenetic relationships of Pachycladon (Brassicaceae) species based on three nuclear and two chloroplast DNA markers. New Zeal J Bot. 2006;44:377–386. doi: 10.1080/0028825X.2006.9513029. DOI

Joly S, Heenan PB, Lockhart PJ. An inter-tribal hybridization event precedes the adaptive species radiation of Pachycladon (Brassicaceae) in New Zealand. Mol Phylogen Evol. 2009;51:365–372. doi: 10.1016/j.ympev.2009.02.015. PubMed DOI

Mitchell AD, Heenan PB. Genetic variation within the Pachycladon (Brassicaceae) complex based on fluorescent AFLP data. J Roy Soc New Zeal. 2002;32:427–443. doi: 10.1080/03014223.2002.9517702. DOI

Heenan PB. Artificial intergeneric hybrids between the New Zealand endemic Ischnocarpus and Pachycladon (Brassicaceae) New Zeal J Bot. 1999;37:595–601. doi: 10.1080/0028825X.1999.9512656. DOI

Yogeeswaran K, Voelckel C, Joly S, Heenan PB. In: Wild Crop Relatives: Genomic and Breeding Resources Wild Relatives of Oilseeds. Kole C, editor. Tokyo: Springer-Verlag; Pachycladon. in press .

Dawson MI. Index of chromosome numbers of indigenous New Zealand spermatophytes. New Zeal J Bot. 2000;38:47–150. doi: 10.1080/0028825X.2000.9512673. DOI

Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ. The dynamic ups and downs of genome size evolution in Brassicaceae. Mol Biol Evol. 2009;26:85–98. doi: 10.1093/molbev/msn223. PubMed DOI

Al-Shehbaz IA, Beilstein MA, Kellogg EA. Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Pl Syst Evol. 2006;259:89–120. doi: 10.1007/s00606-006-0415-z. DOI

German DA, Friesen N, Neuffer B, Al-Shehbaz IA, Hurka H. Contribution to ITS phylogeny of the Brassicaceae, with special reference to some Asian taxa. Plant Syst Evol. 2009;283:33–56. doi: 10.1007/s00606-009-0213-5. DOI

Heenan PB, Dawson MI, Smissen RD, Bicknell RA. An artificial intergeneric hybrid derived from sexual hybridization between the distantly related Arabidopsis thaliana and Pachycladon cheesemanii (Brassicaceae) Bot J Linn Soc. 2008;157:533–544. doi: 10.1111/j.1095-8339.2008.00778.x. DOI

Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I. Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci USA. 2006;103:5224–5229. doi: 10.1073/pnas.0510791103. PubMed DOI PMC

Schranz ME, Lysak MA, Mitchell-Olds T. The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomics. Trends Plant Sci. 2006;11:535–542. doi: 10.1016/j.tplants.2006.09.002. PubMed DOI

Barber JC, Ortega JF, Santos-Guerra A, Marrero A, Jansen RK. Evolution of endemic Sideritis (Lamiaceae) in Macaronesia: Insights from a chloroplast DNA restriction site analysis. Syst Bot. 2000;25:633–647. doi: 10.2307/2666725. DOI

Mummenhoff K, Franzke A. Gone with the bird: late Tertiary and Quaternary intercontinental long-distance dispersal and allopolyploidization in plants. Syst Biodivers. 2007;5:255–260. doi: 10.1017/S1477200007002393. DOI

Baldwin BG, Wagner WL. Hawaiian angiosperm radiations of North American origin. Ann Bot. 2010;105:849–879. doi: 10.1093/aob/mcq052. PubMed DOI PMC

Lindqvist C, Albert VA. Origin of the Hawaiian endemic mints within North American Stachys (Lamiaceae) Am J Bot. 2002;89:1709–1724. doi: 10.3732/ajb.89.10.1709. PubMed DOI

Dierschke T, Mandáková T, Lysak MA, Mummenhoff K. A bicontinental origin of polyploid Australian/New Zealand Lepidium species (Brassicaceae)? Evidence from genomic in situ hybridization. Ann Bot. 2009;104:681–688. doi: 10.1093/aob/mcp161. PubMed DOI PMC

Hair JB. Biosystematics of the New Zealand flora, 1945-1964. New Zeal J Bot. 1966;4:559–595.

Murray BG, de Lange PJ. In: Biology of island floras. Bramwell D, editor. Cambridge: Cambridge University Press; Chromosomes and evolution in New Zealand endemic angiosperms and gymnosperms. in press .

Warwick SI, Al-Shehbaz IA. Brassicaceae: chromosome number index and database on CD-Rom. Plant Syst Evol. 2006;259:237–248. doi: 10.1007/s00606-006-0421-1. DOI

Goodson BE, Santos-Guerra A, Jansen RK. Molecular systematics of Descurainia (Brassicaceae) in the Canary Islands: biogeographic and taxonomic implications. Taxon. 2006;55:671–682. doi: 10.2307/25065643. DOI

Rustan ØH. Revision of the genus Diplotaxis (Brassicaceae) in the Cape Verde Islands, W Africa. Nord J Bot. 1996;16:19–50. doi: 10.1111/j.1756-1051.1996.tb00213.x. DOI

Hewson HJ. In: Flora of Australia. George AS, editor. Vol. 8. Canberra: Australian Publishing Service; 1982. Brassicaceae; pp. 231–357.

Boivin K, Acarkan A, Mbulu R-S, Clarenz O, Schmidt R. The Arabidopsis genome sequence as a tool for genome analysis in Brassicaceae. A comparison of the Arabidopsis and Capsella rubella genomes. Pl Physiol. 2004;135:735–744. doi: 10.1104/pp.104.040030. PubMed DOI PMC

Kuittinen H, de Haan AA, Vogel C, Oikarinen S, Leppälä J, Koch M, Mitchell-Olds T, Langley CH, Savolainen O. Comparing the linkage maps of the close relatives Arabidopsis lyrata and A. thaliana. Genetics. 2004;168:1575–1584. doi: 10.1534/genetics.103.022343. PubMed DOI PMC

Schranz ME, Windsor AJ, Song B-H, Lawton-Rauh A, Mitchell-Olds T. Comparative genetic mapping in Boechera stricta, a close relative of Arabidopsis. Plant Physiol. 2007;144:286–298. doi: 10.1104/pp.107.096685. PubMed DOI PMC

Schubert I. Chromosome evolution. Curr Opin Plant Biol. 2007;10:109–115. doi: 10.1016/j.pbi.2007.01.001. PubMed DOI

Mandáková T, Lysak MA. Chromosomal phylogeny and karyotype evolution in x = 7 crucifer species (Brassicaceae) Plant Cell. 2008;20:2559–2570. doi: 10.1105/tpc.108.062166. PubMed DOI PMC

Luo MC. et al.Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae. Proc Natl Acad Sci USA. 2009;106:15780–15785. doi: 10.1073/pnas.0908195106. PubMed DOI PMC

Thomas BC, Pedersen B, Freeling M. Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res. 2006;16:934–946. doi: 10.1101/gr.4708406. PubMed DOI PMC

Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E. Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biol J Linn Soc. 2004;82:485–501. doi: 10.1111/j.1095-8312.2004.00335.x. DOI

Kim S, Sultan SE, Donoghue MJ. Allopolyploid speciation in Persicaria (Polygonaceae): Insights from a low-copy nuclear region. Proc Natl Acad Sci USA. 2008;105:12370–12375. doi: 10.1073/pnas.0805141105. PubMed DOI PMC

Shimizu-Inatsugi R, Lihova J, Iwanaga H, Kudoh H, Marhold K, Savolainen O, Watanabe K, Yakubov VV, Shimizu KK. The allopolyploid Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri. Mol Ecol. 2009;18:4024–4048. doi: 10.1111/j.1365-294X.2009.04329.x. PubMed DOI

Comai L, Tyagi AP, Winter K, Holmes-Davis R, Reynolds SH, Stevens Y, Byers B. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell. 2000;12:1551–1567. doi: 10.1105/tpc.12.9.1551. PubMed DOI PMC

Yoong LK, Souckova-Skalicka K, Sarasan V, Clarkson JJ, Chase MW, Kovarik A, Leitch AR. A genetic appraisal of new synthetic Nicotiana tabacum (Solanaceae) and the Kostoff synthetic tobacco. Am J Bot. 2006;93:875–883. doi: 10.3732/ajb.93.6.875. PubMed DOI

Tate JA, Symonds VV, Doust AN, Buggs RJA, Mavrodiev EV, Majurev LC, Soltis PS, Soltis DE. Synthetic polyploids of Tragopogon miscellus and T. mirus (Asteraceae):60 years after Ownbey's discovery. Am J Bot. 2009;96:979–988. doi: 10.3732/ajb.0800299. PubMed DOI

Andreasen K, Baldwin BG. Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S-26 S rDNA internal and external transcribed spacers. Mol Biol Evol. 2001;18:936–944. PubMed

Kay KM, Whittall JB, Hodges SA. A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol. 2006;6:36. doi: 10.1186/1471-2148-6-36. PubMed DOI PMC

Stebbins GL. Variation and Evolution in Plants. New York: Columbia University Press; 1950.

Levin DA. The role of chromosomal change in plant evolution. Oxford: Oxford University Press; 2002.

Kyhos DW, Carr GD. Chromosome stability and lability in plants. Evol Theory. 1994;10:227–248.

Jordan GJ. An investigation of long-distance dispersal based on species native to both Tasmania and New Zealand. Aust J Bot. 2001;49:333–340. doi: 10.1071/BT00024. DOI

Lockhart PJ, McLenachan PA, Havell D, Glenny D, Huson D, Jensen U. Phylogeny, radiation, and transoceanic dispersal of New Zealand alpine buttercups: molecular evidence under split decomposition. Ann Missouri Bot Gard. 2001;88:458–477. doi: 10.2307/3298586. DOI

Mitchell AD, Heenan PB, Murray BG, Molloy BPJ, de Lange PJ. Evolution of the south-west Pacific genus Melicytus (Violaceae): evidence from DNA sequence data, cytology, and sex expression. Aust Syst Bot. 2009;22:143–157. doi: 10.1071/SB08042. DOI

Ford KA, Ward JM, Smissen RD, Wagstaff SJ, Breitwieser I. Phylogeny and biogeography of Craspedia (Asteraceae: Gnaphalieae) based on ITS, ETS and psbAtrnH sequence data. Taxon. 2007;56:783–794. doi: 10.2307/25065861. DOI

Wagstaff SJ, Heenan PB, Sanderson MJ. Classification, origins, and patterns of diversification in New Zealand Carmichaelinae (Fabaceae) Am J Bot. 1999;86:1346–1356. doi: 10.2307/2656781. PubMed DOI

Vorontsova MS, Hoffmann P, Maurin O, Chase MW. Molecular phylogenetics of tribe Poranthereae (Phyllanthaceae; Euphorbiaceae sensu lato) Am J Bot. 2007;94:2026–2040. doi: 10.3732/ajb.94.12.2026. PubMed DOI

Smissen RD, Garnock-Jones PJ, Chambers GK. Phylogenetic analysis of ITS sequences suggests a Pliocene origin for the bipolar distribution of Scleranthus (Caryophyllaceae) Aust Syst Bot. 2003;16:301–315. doi: 10.1071/SB01032. DOI

Wagstaff SJ, Wege J. Patterns of diversification in New Zealand Stylidiaceae. Am J Bot. 2002;89:865–874. doi: 10.3732/ajb.89.5.865. PubMed DOI

Crisp M, Cook L, Steane D. Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Phil Trans R Soc Lond B. 2004;359:1551–1571. doi: 10.1098/rstb.2004.1528. PubMed DOI PMC

McGlone MS, Duncan RP, Heenan PB. Endemism, species selection and the origin and distribution of the vascular plant flora of New Zealand. J Biogeogr. 2001;28:199–216. doi: 10.1046/j.1365-2699.2001.00525.x. DOI

Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy DJ, Porch N, Wyrwoll K-H. Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol Ecol. 2008;17:4398–4417. doi: 10.1111/j.1365-294X.2008.03899.x. PubMed DOI

Bailey CD, Koch MA, Mayer M, Mummenhoff K, O'Kane SL, Warwick SI, Windham MD, Al-Shehbaz IA. Toward a global phylogeny of the Brassicaceae. Mol Biol Evol. 2006;23:2142–2160. doi: 10.1093/molbev/msl087. PubMed DOI

Beilstein MA, Al-Shehbaz IA, Mathews S, Kellogg E. Brassicaceae phylogeny inferred from phytochrome A and ndhF sequence data: tribes and trichomes revisited. Am J Bot. 2008;95:1307–1327. doi: 10.3732/ajb.0800065. PubMed DOI

Ijdo JW, Wells RA, Baldini A, Reeders ST. Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res. 1991;19:4780. doi: 10.1093/nar/19.17.4780. PubMed DOI PMC

Kocsis E, Trus BL, Steer CJ, Bisher ME, Steven AC. Image averaging of flexible fibrous macromolecules: The clathrin triskelion has an elastic proximal segment. J Struct Biol. 1991;107:6–14. doi: 10.1016/1047-8477(91)90025-R. PubMed DOI

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