PUBLISHED: 2 AUGUST 2016!| ARTICLE NUMBER: 16116 | DOI: 10.1038/NPLANTS.2016.116 news & views

DOMESTICATION Polyploidy boosts domestication A detailed phylogenetic study now shows that there is a compelling association between polyploidy and domestication, and that polyploidy more frequently occurs before domestication. Zhou Fang and Peter L. Morrell

olyploidy and domestication are both important phenomena in plant Pevolution. Many important crops are polyploid, including banana, canola, cotton, oat, potato, sugar cane, sweet Polyploidization potato and wheat. A debate regarding a possible correlation between polyploidy and domestication in plants has continued for several decades. Now reporting in Nature Plants, Salman-Minkov and colleagues1 have used statistical and computational approaches to examine the association between polyploidy and domestication based on a comprehensive data set. They concluded that domesticated plants have Cultigen Wild progenitor undergone more polyploidy events than their wild relatives, and that polyploidy more frequently occurred before Domestication domestication (Fig. 1). Polyploid plants have multiple chromosome sets (derived from the same Figure 1 | Two possible scenarios involving polyploidy and domestication. Polyploidy could precede species or related species) due to abnormal domestication (dashed line), or domestication could come first (dotted line). cell division or through hybridization. Because of the increase in genome size and thus genetic diversity, polyploids can the cultivated crops during domestication4,5. case). Due to genome downsizing, using carry more favourable genetic variants Some polyploids exhibit ‘gigantism’ for chromosome number to define polyploids is compared to their wild diploid relatives — traits that can mimic those observed in the problematic. Salman-Minkov and colleagues disease resistance and adaptation to diverse domestication syndrome, such as increased reconstructed the phylogeny of each genus environments, or increased adaptation to seed or grain size. Polyploids may therefore using publicly available sequence data. The the current local environment2. Polyploidy be more frequently the target of human polyploidy events were inferred based on increases the amount of raw material on efforts at domestication owing to increased shifts in chromosome numbers along the which natural and artificial selection can ‘curb appeal’. phylogeny. Ploidy shifts were mapped onto act, leading to increased adaptation to the However, in a few previous investigations, the phylogenetic tree using a probabilistic local environment due to novel variants little correlation was found between model of chromosome number evolution. in the polyploids or fixed heterozygosity. polyploidy and domestication5,6. Although Using this approach, the authors find a Genetic diversity can be greatly reduced polyploidization can confer fitness compelling association between polyploidy during a domestication bottleneck — so advantages, favourable new mutations are and plant domestication. the additional genetic diversity provided more quickly fixed and the fitness effect They also showed that polyploidy more by polyploidization can be crucial. In of these mutations can be more easily frequently occurs before domestication. addition, many genomic, transcriptomic identified in diploid species than polyploid Based on its advantages, polyploidy and epigenetic novelties are generated species. Therefore, it seemed reasonable that preceding domestication sounds intuitively through polyploidy3. Polyploidization also there is little association between polyploidy more reasonable than domestication alters dominance relationships among and domestication, because polyploidy is not followed by polyploidy. Higher genetic alleles; it is harder to select and fix recessive exclusively advantageous relative to diploidy diversity with more adaptive genetic mutations. Dominance can preserve in plant evolution. variants in polyploids could benefit function if any of several copies of an allele Salman-Minkov and colleagues the domestication process. However, remain. Polyploidization of a domesticate assembled a large data set with improved disentangling the order of polyploidy can also create genetic isolation from a wild phylogenetic comparative methods and a and domestication is challenging (Fig. 1). progenitor, effectively limiting gene flow more current definition of polyploidy. Early There are also studies in support of the between wild and domesticated plants so studies (such as ref. 6) used a chromosome ‘domestication followed by polyploidy’ that favourable traits can be maintained in number threshold (11 or 13, in their scenario; it was found that human activities

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++ 1(%'32 1#2#15#"ƥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ ɥ news & views resulted in artificial sympatry, hybridization all possible alleles at a locus, this would have of polyploidy in plant domestication. and polyploids in backyard gardens7. been, until recently, a very involved task that Polyploidization increases genetic diversity, Salman-Minkov and colleagues thoroughly required a great deal of effort to distinguish fosters adaptation to new environments, investigated this issue based on a much polymorphisms within homologous introduces new genetic combinations, and larger data set, and showed that polyploidy portions of the genome from divergence can create heterotic effects. Polyploidy followed by domestication is more between progenitor species9. Short-read accelerates domestication and the process of likely (Fig. 1). sequencing technologies have the advantage selecting favourable new traits. As all these Despite the significant association of creating reads from a single molecule areas are challenges currently facing crop between polyploidy and plant domestication, and thus a unique sample of a polyploid breeding, polyploidy formation should be as well as the finding that polyploidy genome, but can be difficult to map back to considered as an important potential path to usually occurs before domestication, a unique location in the reference genome10. future crop improvement. S there are several notable exceptions. The Because polyploidy creates at least a rough polyploidization of wheat, for example, doubling of genome size, twice as much Zhou Fang is in the Crop Science Division, was due to human cultivation after sequence is needed to achieve the same Bayer, Morrisville, North Carolina, USA. Peter domestication8. Polyploidy in wheat resulted level of coverage as in a diploid relative. L. Morrell is in the Department of Agronomy and in the emergence of the free-threshing grain This has been an issue for comparative Plant Genetics, University of Minnesota, St Paul, trait and increased the diversity in wheat resequencing studies, single-nucleotide Minnesota, USA. grains, such as grain hardness or softness3. polymorphism discovery, and for reference e-mail: [email protected] This study demonstrates the important genome assembly. Emerging long-read role played by polyploidy in plant evolution, sequencing technologies hold great promise References 1. Salman-Minkov, A., Sabath, N. & Mayrose, I. Nature Plants but polyploid crops have received less for the study of polyploid species because 2, 16115 (2016). research attention than their diploid relatives they can potentially create sequence reads 2. Ramsey, J. Proc. Natl Acad. Sci. USA 108, 7096–7101 (2011). since the advent of molecular markers. This of sufficient length to distinguish sequences 3. Renny-Byfield, S. & Wendel, J. F. Am. J. Bot. could be because in polyploid genomes, contributed by each of the chromosomes in 101, 1711–1725 (2014). 4. Dempewolf, H., Hodgins, K. A., Rummell, S. E., Ellstrand, N. C. multiple paralogues (copies of a gene) are a polyploid genome. & Rieseberg, L. H. Plant Cell 24, 2710–2717 (2012). found at each locus. A diploid organism The current study also has some 5. Meyer, R. S., DuVal, A. E. & Jensen, H. R. New Phytol. with two alleles at a locus can have one of limitations, such as the relatively low 196, 29–48 (2012). 6. Hilu, K. W. Am. J. Bot. 80, 1494–1499 (1993). three possible genotypes — but a tetraploid resolution of the phylogenetic placement. 7. Hughes, C. E. et al. Proc. Natl Acad. Sci. USA species can have genotypes AAAB, AABB, More precise timing of domestication 104, 14389–14394 (2007). and so on, all of which carry different events could provide deeper insight on this 8. Matsuoka, Y. Plant Cell Physiol. 52, 750–764 (2011). dosages of the same two alleles. While important topic. Nonetheless, the authors 9. Akhunov, E. D. et al. BMC Genomics 11, 702 (2010). 10. Morrell, P. L., Buckler, E. S. & Ross-Ibarra, J. Nature Rev. Genet. resequencing could potentially distinguish provide strong evidence for the importance 13, 85–96 (2012).

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