Polyploidization results in genome duplication and is an important step in evolution and speciation. The Malus genome confirmed that this genus was derived through auto-polyploidization, yet the genetic and meiotic mechanisms for polyploidization, particularly for aneuploidization, are unclear in this genus or other woody perennials. In fact the contribution of aneuploidization remains poorly understood throughout Plantae. We add to this knowledge by characterization of eupolyploidization and aneuploidization in 27,542 F1 seedlings from seven diploid Malus populations using cytology and microsatellite markers. We provide the first evidence that aneuploidy exceeds eupolyploidy in the diploid crosses, suggesting aneuploidization is a leading cause of genome duplication. Gametes from diploid Malus had a unique combinational pattern; ova preserved euploidy exclusively, while spermatozoa presented both euploidy and aneuploidy. All non-reduced gametes were genetically heterozygous, indicating first-division restitution was the exclusive mode for Malus eupolyploidization and aneuploidization. Chromosome segregation pattern among aneuploids was non-uniform, however, certain chromosomes were associated for aneuploidization. This study is the first to provide molecular evidence for the contribution of heterozygous non-reduced gametes to fitness in polyploids and aneuploids. Aneuploidization can increase, while eupolyploidization may decrease genetic diversity in their newly established populations. Auto-triploidization is important for speciation in the extant Malus. The features of Malus polyploidization confer genetic stability and diversity, and present heterozygosity, heterosis and adaptability for evolutionary selection. A protocol using co-dominant markers was proposed for accelerating apple triploid breeding program. A path was postulated for evolution of numerically odd basic chromosomes. The model for Malus derivation was considerably revised. Impacts of aneuploidization on speciation and evolution, and potential applications of aneuploids and polyploids in breeding and genetics for other species were evaluated in depth. This study greatly improves our understanding of evolution, speciation, and adaptation of the Malus genus, and provides strategies to exploit polyploidization in other species.
References
[1]
Bretagnolle F, Thompson JD (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytologies 129: 1–22.
[2]
Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131: 452–462.
[3]
Fawcett JA, Maere S, Van de Peer Y (2009) Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event. Proc Natl Acad Sci USA 14: 5737–5742.
[4]
Tang H, Bowers J, Wang X, Paterson A (2010) Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci USA 1: 472–477.
[5]
Masterton J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421–423.
[6]
Wood TE, Takebayashic N, Barker MS, Mayrosee I, Greenspoon PB, et al. (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106: 13875–13879.
[7]
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, et al. (2010) The genome of the domesticated apple (Malus×domestica Borkh). Nat Genet 42: 833–839.
[8]
Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33: 589–639.
[9]
Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement – A review. Euphytica 133: 3–8.
[10]
Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, et al. (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16: 738–749.
[11]
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6: 836–846.
[12]
Yuan Y, Zhang Z, Chen Z, Olmstead RG (2006) Tracking ancient polyploids: a retroposon insertion reveals an extinct diploid ancestor in the polyploid origin of Belladonna. Mol Biol Evol 23: 2263–2267.
[13]
Yu Z, Haberer G, Matthes M, Rattei T, Mayer KF, et al. (2010) Impact of natural genetic variation on the transcriptome of autotetraploid. Arabidopsis thaliana. Proc Natl Acad Sci USA 41: 17809–17814.
[14]
Cai X, Xu SS (2007) Meiosis-driven genome variations in plants. Curr Genomics 8: 151–161.
[15]
Griffiths S, et al. (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439: 749–752.
[16]
Simillion C, Vandepoele K, Van Montagu MCE, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 21: 13627–13632.
[17]
Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34: 401–437.
[18]
Hughes CE, Govindarajulu R, Robertson A, Filer DL, Harris SA, et al. (2007) Serendipitous backyard hybridization and the origin of crops. Proc Natl Acad Sci USA 36: 14389–14394.
[19]
Ha M, Kim E, Chen ZJ (2009) Duplicate genes increase expression diversity in closely related species and allopolyploids. Proc Natl Acad Sci USA 7: 2295–2300.
[20]
Senchina DS, Alvarez I, Cronn RC, Liu B, Rong J, et al. (2003) Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol Biol Evol 20: 633–643.
[21]
Venditti C, Meade A, Pagel M (2009) Phylogenies reveal new interpretation of speciation and the Red Queen. Nature 463: 349–352.
[22]
Cifuentes M, Grandont L, Moore G, Chèvre MA, Jenczewski E (2010) Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytol 186: 29–36.
[23]
Yoshizumi T, Tsumoto Y, Takiguchi T, Nagata N, Yamamoto YY, et al. (2006) Increased level of polyploidy1, a conserved repressor of cyclina2 transcription, controls endoreduplication in Arabidopsis. Plant Cell 18: 2452–2468.
[24]
Schranz ME, Mitchell-Olds T (2006) Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell 18: 1152–1165.
[25]
Blanc G, Kenneth H, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667–1678.
[26]
Dzialuk A, Chybicki I, Welc M, Sliwinska E, Burczyk J (2007) Presence of triploids among oak species. Ann Bot 99: 959–964.
[27]
Liu SL, Adams KL (2010) Dramatic change in function and expression pattern of a gene duplicated by polyploidy created a paternal effect gene in the Brassicaceae. Mol Biol Evol 27: 2817–2828.
[28]
Janick J, Cummins JN, Brown SK, Hemmat M (1996) in Fruit Breeding Tree and Tropical Fruits. In: Janick J, Moore JN, editors. pp. 1–77. (John Wiley and Sons).
[29]
Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, et al. (2002) Development and characterization for 140 new microsatellites in apple (Malus×domestica Borkh). Mol Breed 10: 217–241.
[30]
Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, et al. (2006) Microsatellite markers spanning the apple (Malus×domestica Borkh) genome. Tree Genet Genomes 2: 202–224.
[31]
Han YP, Gasic K, Marron B, Beever JE, Korban SS (2007) A BAC-based physical map of the apple genome. Genomics 89: 630–637.
[32]
Einset J (1944) The occurrence of a tetraploid and two triploid apple seedlings in progenies of diploid parents. Science 99: 345.
[33]
Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, et al. (2004) The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc Natl Acad Sci USA 3: 886–890.
Selmecki AM, Dulmage K, Cowen LE, Anderson JB, Berman J (2009) Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genet 5(10): e1000705. doi:10.1371/journal.pgen.1000705.
[36]
Dermen H (1965) Colchiploidy and histological imbalance in triploid apple and pear. Am J Bot 52: 353–359.
[37]
Orr HA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6: 119–127.
[38]
Mandáková T, Joly S, Krzywinski M, Mummenhoff K, Lysak MA (2010) Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell 22: 2277–2290.
Boughey AS (1959) Origin and dispersal of flowering plants. Nature 184: 1200–1201.
[41]
Van Ooijen JW (1996) JoinMap 4 Software for the Calculation of Genetic Linkage Maps in Experimental Populations. Netherland: Kyazma B V.
[42]
Scheid OM, Jakovleva L, Afsar K, Maluszynska J, Paszkowski J (1996) A change of ploidy can modify epigenetic silencing. Proc Natl Acad Sci USA 14: 7114–7119.
[43]
Eckardt NA (2010) A double lock on polyploidy-associated epigenetic gene silencing. Plant Cell 22: 3.
[44]
Harding J, Singh F, Mol JNM (1991) Genetics and breeding of ornamental species. Dordrecht-Boston-London: Kluwer Academic Publishers.
[45]
Vainstein A (2002) Breeding for ornamentals: classical and molecular approaches. The Netherlands: Kluwer Academic Publishers.
[46]
Luque D, Rivasb G, Alfonsob C, Carrascosaa JL, JRodríguezc JF, Castón JR, et al. (2009) Infectious bursal disease virus is an icosahedral polyploid dsRNA virus. Proc Natl Acad Sci USA 7: 2148–2152.
[47]
Mendell J, Clements KD, Choat JH, Angert ER (2008) Extreme polyploidy in a large bacterium. Proc Natl Acad Sci USA 18: 6730–6734.
[48]
Wong S, Nutler G, Wolfer KH (2002) Gene order evolution and paleopolyploidy in hemiascomycete yeasts. Proc Natl Acad Sci USA 14: 9272–9277.
[49]
Sankoff D (2009) Reconstructing the History of Yeast Genomes. PLoS Genet 5(5): e1000483.
[50]
Evans BJ, Kelley DB, Melnick DJ, David C, Cannatella DC (2005) Evolution of RAG-1 in polyploid clawed frogs. Mol Biol Evol 22: 1193–1207.
[51]
Dehal P, Boore JL (2005) Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate. PLoS Biol 3(10): e314. doi:10.1371/journal.pbio.0030314.
[52]
Pratt C, Paik JSS, Way RD, Einset J (1978) Chromosome numbers of apple species, cultivars, and sports. J Am Soc Hortic Sci 103: 690–693.
[53]
Gaudillière JP, Rheinberger HJ (2004) Classical Genetic Research and its Legacy. UK: Routledge.
[54]
Lunn D, Spiegelhalter D, Thomas A, Best N (2009) The BUGS project: Evolution, critique and future directions (with discussion). Statistics in Medicine 28: 3049–3082.
