Genomic mosaicism due to homoeologous exchange generates extensive phenotypic diversity in nascent allopolyploids

Abstract

Allopolyploidy is an important process in plant speciation, yet newly formed allopolyploid species typically suffer from extreme genetic bottlenecks. One escape from this impasse might be homoeologous meiotic pairing, during which homoeologous exchanges (HEs) generate phenotypically variable progeny. However, the immediate genome-wide patterns and resulting phenotypic diversity generated by HEs remain largely unknown. Here, we analyzed the genome composition of 202 phenotyped euploid segmental allopolyploid individuals from the 4th selfed generation following chromosomal doubling of reciprocal F1 hybrids of crosses between rice subspecies, using whole genome sequencing. We describe rampant occurrence of HEs that, by overcoming incompatibility or conferring superiority of hetero-cytonuclear interactions, generate extensive and individualized genomic mosaicism across the analyzed tetraploids. We show that the resulting homoeolog copy number alteration in tetraploids affects known-function genes and their complex genetic interactions, in the process creating extraordinary phenotypic diversity at the population level following a single initial hybridization. Our results illuminate the immediate genomic landscapes possible in a tetraploid genomic environment, and underscore HE as an important mechanism that fuels rapid phenotypic diversification accompanying the initial stages of allopolyploid evolution.

Comparative genomics and polyploid dynamics in tetraploid cotton (Gossypium)

“…In cotton, a few large-scale chromosomal inversions are associated with population differentiation and environmental adaptation among Gossypium hirsutum cultivars, consistent with the observation that SVs may drive differentiation [16]. In addition to SVs, homoeologous exchange (HE) between subgenomes may affect chromosome balance [24] and create diversity [25,26]. Although HEs are thought to be uncommon in cotton, unequal homoeologous exchanges of repeat sequence between A and D subgenomes subsequent to their formation might explain some of the changes in A and D subgenome size that arose after polyploidization [18,27].…”

Gradual evolution of allopolyploidy inArabidopsis suecica

“…This demonstrates that HE occurs in A. suecica and contributes to the intraspecific variation we observed in gene expression (Fig 5a, b). HE in allopolyploids is a main source of diversity, causing phenotypic changes in flower color in synthetic polyploid peanut 9 and extensive phenotypic change in synthetic polyploid rice at a population level 125 . However, the majority of HEs are probably deleterious as they will lead to gene loss: although the A. thaliana and A. arenosa genomes are largely syntenic, AS530 is missing 108 genes (Supplementary Figure 19) that are only present on the A. arenosa subgenome segment that has been replaced by the homeologous segment from the A. thaliana subgenome, and AS150/ASÖ5 are missing 53 genes that were only present on the A. thaliana subgenome.…”

Genomics Analyses Reveal Unique Classification, Population Structure and Novel Allele of Neo-Tetraploid Rice

“…Novel genomic variations have been detected in the polyploids of Arabidopsis (Madlung et al 2005), Brassica napus (Gaeta et al 2007;Song et al 1995) and wheat (Han et al 2005;Ozkan et al 2001;Shaked et al 2001). Recently, enormous amount of homoeologous exchanges (HEs) were found in segmental allotetraploid rice, which responsible for their genomic and phenotypic variations (Wu et al 2020). Here, NTRs were developed from the crossing decedents of ATRs from different ecotypes, which can be considered as a new segmental allotetraploid rice.…”