An asymmetric allelic interaction drives allele transmission bias in interspecific rice hybrids

Abstract

Hybrid sterility (HS) between Oryza sativa (Asian rice) and O . glaberrima (African rice) is mainly controlled by the S1 locus. However, our limited understanding of the HS mechanism hampers utilization of the strong interspecific heterosis. Here, we show that three closely linked genes ( S1A4 , S1TPR , and S1A6 ) in the African S1 allele ( S1-g ) constitute a killer-protector system that eliminates gametes carrying the Asian allele ( S1-s ). In Asian–African rice hybrids ( S1-gS1-s ), the S1TPR-S1A4-S1A6 interaction in sporophytic tissues generates an abortion signal to male and female gametes. However, S1TPR can rescue S1-g gametes, while the S1-s gametes selectively abort for lacking S1TPR. Knockout of any of the S1-g genes eliminates the HS. Evolutionary analysis suggests that S1 may have arisen from newly evolved genes, multi-step recombination, and nucleotide variations. Our findings will help to overcome the interspecific reproductive barrier and use Asian–African hybrids for increasing rice production.

New Insights Into the Nature of Interspecific Hybrid Sterility in Rice

“…This result thus supported the independent origin theory of indica and japonica and was consistent with the finding reported by Wambugu et al (2015). The cloning of S1 locus, which is the most important genetic factor causing the hybrid sterility between two cultivated species, provides experimental evidence for the independent origin of Asian cultivated rice and African cultivated rice (Xie et al, 2019b).…”

“…From the mapping loci, 10 hybrid sterility loci or pairs of epistatic interaction were cloned and characterized at the molecular level, for which the genetics of seven loci-S1, S5, S7, Sa, Sc, hsa1, and qHMS7-follow the one-locus interaction model (Chen et al, 2008;Long et al, 2008;Yang et al, 2012;Kubo et al, 2016;Yu et al, 2016;Shen et al, 2017;Xie et al, 2017;Koide et al, 2018;Yu et al, 2018;Xie et al, 2019b). Most loci contain two or more closely linked genes interacting to cause gamete sterility, which can take these recognized forms: a single Mendelian factor, such as two genes at Sa, qHMS7 and hsa1 locus (Long et al, 2008;Kubo et al, 2016;Yu et al, 2018); three genes at S1 and S5 loci (Yang et al, 2012;Xie et al, 2017;Koide et al, 2018;Xie et al, 2019b); and genomic structural variation at the Sc locus (Shen et al, 2017). All can be regarded as interaction between different alleles from a single Mendelian factor to control hybrid sterility.…”

The wtf4 meiotic driver utilizes controlled protein aggregation to generate selective cell death

“…The Wtf4 poison forms distributed toxic aggregates and the Wtf4 antidote co-assembles with the Wtf4 poison and neutralizes the aggregate’s toxicity via trafficking to the vacuole ( Figure 6 ). This mechanism is unlike the mechanism of any other meiotic driver described to date ( Grognet et al, 2014 ; Didion et al, 2015 ; Long et al, 2008 ; Dawe et al, 2018 ; Rhoades et al, 2019 ; Dalstra et al, 2005 ; Hammond et al, 2012 ; Vogan et al, 2019 ; Chen et al, 2008 ; Akera et al, 2017 ; Bauer et al, 2012 ; Pieper et al, 2018 ; Herrmann et al, 1999 ; Shen et al, 2017 ; Yu et al, 2018 ; Bauer et al, 2007 ; Wu et al, 1988 ; Xie et al, 2019 ; Kruger et al, 2019 ; Lin et al, 2018 ; Svedberg et al, 2020 ), but there are very few mechanistically characterized killer meiotic drive systems (reviewed in Bravo Núñez et al, 2018b ).…”

Dramatically diverse Schizosaccharomyces pombe wtf meiotic drivers all display high gamete-killing efficiency

“…Our current work shows that many of these predicted drive genes are able to drive in the right genetic context. This work expands the rapidly growing number of bona fide drive genes identified in recent years [4,[16][17][18][33][34][35][36][37][38][39][40][41][42][43].…”