Partial cytological diploidization of neoautotetraploid meiosis by induced cross-over rate reduction

Abstract

Polyploids, which arise from whole-genome duplication events, have contributed to genome evolution throughout eukaryotes. Among plants, novel features of neopolyploids include traits that can be evolutionarily or agriculturally beneficial, such as increased abiotic stress tolerance. Thus, in addition to being interesting from an evolutionary perspective, genome duplication is also increasingly recognized as a promising crop improvement tool. However, newly formed (neo)polyploids commonly suffer from fertility problems, which have been attributed to abnormal associations among the multiple homologous chromosome copies during meiosis (multivalents). Here, we test the long-standing hypothesis that reducing meiotic cross-over number may be sufficient to limit multivalent formation, favoring diploid-like bivalent associations (cytological diploidization). To do so, we developed Arabidopsis thaliana lines with low cross-over rates by combining mutations for HEI10 and TAF4b . Double mutants showed a reduction of ~33% in cross-over numbers in diploids without compromising meiotic stability. Neopolyploids derived from the double mutant show a cross-over rate reduction of about 40% relative to wild-type neotetraploids, and groups of four homologs indeed formed fewer multivalents and more bivalents. However, we also show that the reduction in multivalents comes with the cost of a slightly increased frequency of univalents and that it does not rescue neopolyploid fertility. Thus, while our results do show that reducing cross-over rates can reduce multivalent frequency in neopolyploids, they also emphasize that there are additional factors affecting both meiotic stability and neopolyploid fertility that will need to be considered in solving the neopolyploid fertility challenge.

Defective pollen tube tip growth induces neo-polyploid infertility

“…We showed previously that at least eight meiosis genes are targets of directional selection in a natural autotetraploid lineage of Arabidopsis arenosa and, for at least three of them, that naturally evolved tetraploid alleles help stabilize polyploid meiosis (7)(8)(9). But fitting with G. L. Stebbins's speculation from 75 years ago that there is also an "unexplained nonmeiotic factor" affecting neo-polyploid fertility (10), we recently showed that reducing multivalent frequency in Arabidopsis thaliana neo-tetraploids by reducing crossover numbers does not rescue fertility on its own (11). This result raised the question of what other factor (or factors) might contribute to the low fertility of neo-polyploids.…”

The genetic consequences of range expansion and its influence on diploidization in polyploids

“…A similar gene that experiences mutations of large effect which regulate pairing behavior is PrBn in Brassica napus (Jenczewski et al 2003), and an additional QTL of large effect has also been found in Arabidopsis suecica (Henry et al 2014). However, other identified pathways to the genetic control of meiosis have also been observed, such as MHS4 copy number regulation that may be preserved in angiosperms generally (Gonzalo et al 2019) and a complex landscape of epistatic interactions in Arabidopsis arenosa and A. thaliana neo-autopolyploids (Morgan et al 2020; Morgan et al 2022; Gonzalo et al 2023).…”

Genome-wide patterns of homoeologous gene flow in allotetraploid coffee

“…WGDs are among the most profound mutational changes observed in nature particularly because they result in global genomic redundancy, which has consequences that range from the gene to the population (Fox et al, 2020). At the gene level, genomic redundancy contributes to relaxation of selective constraints (Otto and Whitton, 2000;Douglas et al, 2015;Zhang et al, 2020;Conover and Wendel, 2022), transcriptional re-programming (Schnable et al, 2011;Combes et al, 2013;Yoo et al, 2013;Akama et al, 2014;Hu et al, 2016;Yang et al, 2016;Edger et al, 2017;Ramírez-González et al, 2018;Oberprieler et al, 2019;Landis et al, 2020;Song et al, 2020), altered epigenetic regulation (Madlung et al, 2002;Salmon et al, 2005;Shcherban et al, 2008;Fulneček et al, 2009;Akagi et al, 2016;Chen et al, 2017;Song et al, 2017;Ding and Chen, 2018;Rao et al, 2023), transposable element expansion (Ågren et al, 2016;Baduel et al, 2019), altered rates of homologous, ectopic, and intergenomic recombination (Chalhoub et al, 2014;Guo et al, 2014;Jarvis et al, 2017;Chen et al, 2018;Bertioli et al, 2019;Mason and Wendel, 2020;Gonzalo et al, 2023), chromosomal structural changes (Chester et al, 2012;Edwards et al, 2017;Gordon ...…”