Patterns of Transmission Ratio Distortion in Interspecific Lettuce Hybrids Reveal a Sex-Independent Gametophytic Barrier

Abstract

Interspecific crosses can result in progeny with reduced vitality or fertility due to genetic incompatibilities between species, a phenomenon known as hybrid incompatibility (HI). HI is often caused by a bias against deleterious allele combinations, which results in transmission ratio distortion (TRD). Here, we determined the genome-wide distribution of HI between wild lettuce, Lactuca saligna, and cultivated lettuce, L. sativa, in a set of backcross inbred lines (BILs) with single introgression segments from L. saligna introgressed into a L. sativa genetic background. Almost all BILs contained an introgression segment in a homozygous state except a few BILs, for which we were able to obtain only a single heterozygous introgression. Their inbred progenies displayed severe TRD with a bias toward the L. sativa allele and complete nontransmission of the homozygous L. saligna introgression, i.e., absolute HI. These HI might be caused by deleterious heterospecific allele combinations at two loci. We used an multilocus segregating interspecific F2 population to identify candidate conspecific loci that can nullify the HI in BILs. Segregation analysis of developed double-introgression progenies showed nullification of three HI and proved that these HI are explained by nuclear pairwise incompatibilities. One of these digenic HI showed 29% reduced seed set and its pattern of TRD pointed to a sex-independent gametophytic barrier. Namely, this HI was caused by complete nontransmission of one heterospecific allele combination at the haploid stage, surprisingly in both male and female gametophytes. Our study shows that two-locus incompatibility systems contribute to reproductive barriers among Lactuca species.

Genetic Dissection and Validation of Chromosomal Regions for Transmission Ratio Distortion in Intersubspecific Crosses of Rice

“…TRD acts as one of the selfish genetic elements, distorting segregation or non-Mendelian transmission of alleles that can alter allele transmission in hybrids among progenies of heterozygotes, since the gametes carrying competing alleles increase their transmission over other alleles (Masly et al, 2006;Moyle and Graham, 2006;Koide et al, 2008a;Phadnis and Orr, 2009;Phadnis, 2011). TRD has been described in intersubspecific and intrasubspecific hybrids in various animal and plant species, such as Drosophila (Mcdermott and Noor, 2012;Corbett-Detig et al, 2013), mouse (Bauer et al, 2005(Bauer et al, , 2007, mosquito (Shin et al, 2012), rice (Yang et al, 2012;Reflinur et al, 2014;Shen et al, 2017;Xie et al, 2019), Arabidopsis (Bikard et al, 2009;Leppala et al, 2013), and lettuce (Giesbers et al, 2019).…”

Recurrent breakdown and rebalance of segregation distortion in the genomes: battle for the transmission advantage

“…It was observed that two-locus interaction contributed significantly to the deviation of genotype frequencies in rice in the whole genome (Li et al 2017(Li et al , 2019. Likewise, digenic interactions were also responsible for SD among Lactuca species (Giesbers et al 2019). Evidence for SD caused by epistatic interactions was also observed in triticale across the whole genome (Alheit et al 2011).…”

“…Gametes from indica varieties were preferred (77.05%) after meiosis in inter-subspecific crosses, suggesting that the japonica alleles were always defeated under competition. Similarly, a genome-wide identification of SD in interspecific lettuce hybrids detected that all distorted regions were skewed towards Lactuca sativa alleles, leading to hybrid incompatibility (Giesbers et al 2019).…”

Fine Mapping of Two Interacting Loci for Transmission Ratio Distortion in Rice (Oryza sativa L.)

“…Transmission ratio distortion occurs before or after fertilization due to various reasons, such as meiotic drive, gametic competition, inbreeding depression, and hybrid incompatibilities ( Huang et al, 2013 ; Fishman and McIntosh, 2019 ). It can be caused either by incompatible allelic interaction at a single-locus ( Bauer et al, 2007 ; Corbett-Detig et al, 2013 ) or by two or multi-loci interaction, in which one gene effect is dependent on the presence/absence of other genes ( Giesbers et al, 2019 ). With regard to rice, numerous loci/regions have been identified for TRD ( Li et al, 2017 , 2019 ; Zhang et al, 2020a ).…”