Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants

Abstract

Background: Polyploidy or whole-genome duplication is now recognized as being present in almost all lineages of higher plants, with multiple rounds of polyploidy occurring in most extant species. The ancient evolutionary events have been identified through genome sequence analysis, while recent hybridization events are found in about half of the world's crops and wild species. Building from this new paradigm for understanding plant evolution, the papers in this Special Issue address questions about polyploidy in ecology, adaptation, reproduction and speciation of wild and cultivated plants from diverse ecosystems. Other papers, including this review, consider genomic aspects of polyploidy.

Approaches: Discovery of the evolutionary consequences of new, evolutionarily recent and ancient polyploidy requires a range of approaches. Large-scale studies of both single species and whole ecosystems, with hundreds to tens of thousands of individuals, sometimes involving 'garden' or transplant experiments, are important for studying adaptation. Molecular studies of genomes are needed to measure diversity in genotypes, showing ancestors, the nature and number of polyploidy and backcross events that have occurred, and allowing analysis of gene expression and transposable element activation. Speciation events and the impact of reticulate evolution require comprehensive phylogenetic analyses and can be assisted by resynthesis of hybrids. In this Special Issue, we include studies ranging in scope from experimental and genomic, through ecological to more theoretical.

Conclusions: The success of polyploidy, displacing the diploid ancestors of almost all plants, is well illustrated by the huge angiosperm diversity that is assumed to originate from recurrent polyploidization events. Strikingly, polyploidization often occurred prior to or simultaneously with major evolutionary transitions and adaptive radiation of species, supporting the concept that polyploidy plays a predominant role in bursts of adaptive speciation. Polyploidy results in immediate genetic redundancy and represents, with the emergence of new gene functions, an important source of novelty. Along with recombination, gene mutation, transposon activity and chromosomal rearrangement, polyploidy and whole-genome duplication act as drivers of evolution and divergence in plant behaviour and gene function, enabling diversification, speciation and hence plant evolution.

Keywords: Polyploidy; adaptation; angiosperms; bryophytes; chromosomes; crops; ecology; evolution; genomics; hybrids; phylogeny; speciation; weeds; whole-genome duplication (WGD).

Fig. 1.

Simplified phylogeny of the green plant lineage focusing on the occurrence of WGD (whole-genome duplication) events. Polyploidy events (yellow diamonds) refer to either single or multiple rounds of WGD (i.e. duplication or triplication) and are labelled where applicable (Greek letters; see references below). Complete genome sequences have clearly established that WGD has remarkably shaped the evolutionary history of angiosperms compared with the other major clades of green plants. Estimates for the age of angiosperms have suggested the range of 167–199 million years ago (Mya) (Bell et al., 2010). Then rapid radiations responsible for the extant angiosperm diversity occurred after the early diversification of Mesangiospermae 139–156 Mya (Moore et al., 2007; Bell et al., 2010) with a burst of diversification specific for the Cretaceous, <125 Mya (age of the earliest angiosperm macrofossil; Cascales-Miñana et al., 2016). Early divergence times are from Bell et al. (2010) and Leliaert et al. (2012); for angiosperms from Fawcett et al. (2009), Jiao et al. (2011) and Li et al. (2016); and for gymnosperms from Lu et al. (2014). Dashed lines indicate imprecise timing or approximate representation of lineage divergence. WGD events are from Jiao et al. (2011); Leliart et al. (2011); D’Hont et al. (2012); Beike et al. (2014); Renny-Byfield and Wendel (2014); Li et al. (2015, 2016); Scott et al. (2016); Shaw et al. (2016); and Bombarely et al. (2016). See corresponding publications for precise estimates of time divergence and occurrence of WGD. AGF, hypothetical ancestral green flagellate; ANA, basal angiosperms including Amborellales, Nymphaeales, Austrobaileyales; following a standardized method, Greek letters are used to name polyploidy events along the phylogenetic tree, starting from the α (alpha) and β (beta) events that have been identified in the arabidopsis genome (Bowers et al., 2003).

Fig. 2.

Metaphase chromosomes of diploid, tetraploid and hexaploid wheats stained with the DNA stain 4',6-diamidino-2-phenylindole (DAPI; cyan) and showing fluorescent in situ hybridization signal (magenta) from the 120 bp tandemly repeated (pSc119.2) DNA family common to many Triticeae species (see Contento et al., 2005). This repeat family originated before the split of rye, barley, wheat and other grasses in the tribe, but has been amplified differentially in the different species. It forms large blocks at sub-telomeric and intercalary chromosomal regions in the B genome wheats, both seen in the seven chromosome pairs in the diploid (A), tetraploid (B) and hexaploid (C), but has only few sites in about half of the A and D genome chromosomes with weak single sub-telomeric foci (B, C). (A) Aegilops speltoides (2n = 2x = 14, genome constitution B'B'); (B) Triticum durum (2n = 4x = 28, AABB); (C) T. aestivum (2n = 6x = 28, AABBDD). Scale bar = 10 μm.