Doubling down on genomes: Polyploidy and crop plants

Abstract

Polyploidy, or whole genome multiplication, is ubiquitous among angiosperms. Many crop species are relatively recent allopolyploids, resulting from interspecific hybridization and polyploidy. Thus, an appreciation of the evolutionary consequences of (allo)polyploidy is central to our understanding of crop plant domestication, agricultural improvement, and the evolution of angiosperms in general. Indeed, many recent insights into plant biology have been gleaned from polyploid crops, including, but not limited to wheat, tobacco, sugarcane, apple, and cotton. A multitude of evolutionary processes affect polyploid genomes, including rapid and substantial genome reorganization, transgressive gene expression alterations, gene fractionation, gene conversion, genome downsizing, and sub- and neofunctionalization of duplicate genes. Often these genomic changes are accompanied by heterosis, robustness, and the improvement of crop yield, relative to closely related diploids. Historically, however, the genome-wide analysis of polyploid crops has lagged behind those of diploid crops and other model organisms. This lag is partly due to the difficulties in genome assembly, resulting from the genomic complexities induced by combining two or more evolutionarily diverged genomes into a single nucleus and by the significant size of polyploid genomes. In this review, we explore the role of polyploidy in angiosperm evolution, the domestication process and crop improvement. We focus on the potential of modern technologies, particularly next-generation sequencing, to inform us on the patterns and processes governing polyploid crop improvement and phenotypic change subsequent to domestication.

Silenced rRNA genes are activated and substitute for partially eliminated active homeologs in the recently formed allotetraploid, Tragopogon mirus (Asteraceae)

“…The advantage of duplicated genes and chromosomes in the nucleus is, however, not obvious in the short term because genome duplication is frequently associated with various problems, including genomic instability, transposon activation (Parisod et al, 2010), meiotic irregularities (Grandont et al, 2013) and expression imbalance (Adams and Wendel, 2005). One of the manifestations of genomic instability is homeologue loss, which is observed in many natural and synthetic allopolyploids Renny-Byfield and Wendel, 2014). The evolutionary significance, molecular mechanisms and impacts of such genomic instability on plant physiology remain unknown.…”

Genetic mapping in polyploids

“…It has been suggested that despite 150 years of breeding for increased yield, phenotypic selection methods have done nothing to raise average potato yields in that time (Jansky, 2009;Slater et al, 2016), in contrast to other major diploid crops like maize or rice. On the other hand, some authors remain convinced about the merit of polyploids and their potential to deliver higher yields through heterosis (Renny-Byfield and Wendel, 2014). I don't believe that polyploids lack the necessary qualities to rise to the challenges we are facing.…”

“…Many theories to explain their prevalence among crop species have been proposed, identifying features which may have appealed to early farmers in their domestication of wild species. Such features include their larger organs such as tubers, fruits or flowers (the so-called "gigas" effect) (Sattler et al, 2016), increased heterosis (Comai, 2005), their genomic plasticity (te Beest et al, 2011), phenotypic novelty (Udall and Wendel, 2006), their ability to be clonally propagated (Herben et al, 2017), increased seedling and juvenile vigour (Levin, 1983), the masking of deleterious alleles (Renny-Byfield and Wendel, 2014) or the possibility of seedlessness which accompanies aneuploidy (Bradshaw, 2016). It is currently believed that all flowering plants have experienced at least one whole genome duplication (WGD) during the course of their evolution, with many lineages undergoing multiple rounds of WGD followed by re-diploidisation (Vanneste et al, 2014).…”

The Impact of Genetic Changes during Crop Domestication

“…There is higher prevalence of recent polyploidy among major domestic crop species (34%) than among wild plant species (24%), with monocots exhibiting the most profound difference: 54% of the crops are recent polyploids versus 40% of the wild species [98]. Domesticated plants benefitted from the versatility of polyploids [99], such as broadening of adaptation, increase in harvested organ size (gigantism), fixation of heterozygosity, and the appearance of novel traits due to epistatic interactions. Genome duplication can serve as a postzygotic barrier reducing gene flow with wild progenitors [100].…”