Yohei Koide

Sex‐independent transmission ratio distortion system responsible for reproductive barriers between Asian and African rice species

* A sex-independent transmission ratio distortion (siTRD) system detected in the interspecific cross in rice was analyzed in order to understand its significance in reproductive barriers. The S(1) gene, derived from African rice Oryza glaberrima, induced preferential abortion of both male and female gametes possessing its allelic alternative (), from Asian rice O. sativa, only in the heterozygote. * The siTRD was characterized by resolving it into mTRD and fTRD occurring through male and female gametes, respectively, cytological analysis of gametophyte development, and mapping of the S(1) locus using near-isogenic lines. The allelic distribution of the S(1) locus in Asian and African rice species complexes was also analyzed. * The siTRD system involved at least two components affecting male and female gametogeneses, respectively, including a modifier(s) that enhances fTRD. The chromosomal location of the major component causing the mTRD was delimited within an approx. 40 kb region. The S(1) locus induced hybrid sterility in any pairwise combination between Asian and African rice species complexes. * The allelic state of the S(1) locus has diverged between Asian and African rice species complexes, suggesting that the TRD system has a significant role in the reproductive barriers in rice.

The Evolution of Sex-Independent Transmission Ratio Distortion Involving Multiple Allelic Interactions at a Single Locus in Rice

Transmission ratio distortion (TRD) is frequently observed in inter- and intraspecific hybrids of plants, leading to a violation of Mendelian inheritance. Sex-independent TRD (siTRD) was detected in a hybrid between Asian cultivated rice and its wild ancestor. Here we examined how siTRD caused by an allelic interaction at a specific locus arose in Asian rice species. The siTRD is controlled by the S6 locus via a mechanism in which the S6 allele acts as a gamete eliminator, and both the male and female gametes possessing the opposite allele (\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document}) are aborted only in heterozygotes (\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}/S_{6}^{\mathrm{a}}\) \end{document}). Fine mapping revealed that the S6 locus is located near the centromere of chromosome 6. Testcross experiments using near-isogenic lines (NILs) carrying either the S6 or \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document} alleles revealed that Asian rice strains frequently harbor an additional allele (\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{n}}\) \end{document}) the presence of which, in heterozygotic states (\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}/S_{6}^{\mathrm{n}}\) \end{document} and \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}/S_{6}^{\mathrm{n}}\) \end{document}), does not result in siTRD. A prominent reduction in the nucleotide diversity of S6 or \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document} carriers relative to that of \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{n}}\) \end{document} carriers was detected in the chromosomal region. These results suggest that the two incompatible alleles (S6 and \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document}) arose independently from \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{n}}\) \end{document} and established genetically discontinuous relationships between limited constituents of the Asian rice population.

Complex genetic nature of sex-independent transmission ratio distortion in Asian rice species: the involvement of unlinked modifiers and sex-specific mechanisms

Transmission ratio distortion (TRD), in which one allele is transmitted more frequently than the opposite allele, is presumed to act as a driving force in the emergence of a reproductive barrier. TRD acting in a sex-specific manner has been frequently observed in interspecific and intraspecific hybrids across a broad range of organisms. In contrast, sex-independent TRD (siTRD), which results from preferential transmission of one of the two alleles in the heterozygote through both sexes, has been detected in only a few plant species. We previously reported an S6 locus-mediated siTRD, in which the S6 allele from an Asian wild rice strain (Oryza rufipogon) was transmitted more frequently than the S6a allele from an Asian cultivated rice strain (O. sativa) through both male and female gametes in heterozygous plants. Here, we report on the effect of a difference in genetic background on S6 locus-mediated siTRD, based on the analysis using near-isogenic lines and the original wild strain as a parental strain for crossing. We found that the degree of TRD through the male gametes varied depending on the genetic background of the female (pistil) plants. Despite the occurrence of TRD through both male and female gametes, abnormality was detected in ovules, but not in pollen grains, in the heterozygote. These results suggest the involvement of unlinked modifiers and developmentally distinct, sex-specific genetic mechanisms in S6 locus-mediated siTRD, raising the possibility that siTRD driven by a single locus may be affected by multiple genetic factors harbored in natural populations.

Two loosely linked genes controlling the female specificity for cross-incompatibility in rice

Cross-incompatibility caused by endosperm abortion was found in advanced generations of backcrossing between the Asian wild (W593) and cultivated (T65wx) rice strains. The near isogenic line, T65WxS6(W593), carrying a segment of chromosome 6 from W593 showed a low seed setting when pollinated with pollen grains of T65wx in spite of the fact that the reciprocal cross gave a high seed setting. The unidirectional or asymmetric crossing barrier was previously explained by an interaction between Cif and cim, both of which acted sporophytically, resulting in the cross-incompatibility reactions in the female (CIF) and male (CIM), respectively. In the genetic model, endosperm abortion is induced only when CIF gametes are fertilized with CIM gametes. This predicted that the double homozygote for Cif and cim might be self-incompatible since the plant expresses both CIF and CIM simultaneously. However, we failed to obtain such a self-incompatible plant by transferring Cif into a cim plant. The present results showed that CIF is controlled not only by Cif but also by an additional gene(s) loosely linked with it. We propose here that Cif1 (formerly named as Cif) and Cif2 determine CIF. In addition, Cif2 and Cim were not separated due to restriction of recombination, which might explain why it is difficult to obtain a self-incompatible rice plant expressing both CIF and CIM.

Genetic basis of transgressive segregation in rice heading phenotypes

Transgressive segregation produces hybrid progeny phenotypes that exceed parental phenotypes. Unlike heterosis, extreme phenotypes caused by transgressive segregation are heritably stable. We examined transgressive phenotypes of flowering time in rice. Our previous study examined days to flowering (heading; DTH) in six F2 populations for which the parents had distal DTH, and found very few transgressive phenotypes. Here, we demonstrate that transgressive segregation in F2 populations occurred between parents with proximal DTH. DTH phenotypes of the A58 × Kitaake F2 progenies frequently exceeded those of both parents. Both A58 and Kitaake are japonica rice cultivars adapted to Hokkaido, Japan, which is a high-latitude region, and have short DTH. Among the four known loci required for short DTH, three loci had common alleles in A58 and Kitaake, and only the one locus had different alleles. This result indicates that there is a similar genetic basis for DTH between the two varieties. We identified five new quantitative trait loci (QTLs) associated with transgressive DTH phenotypes by genome-wide single nucleotide polymorphism (SNP) analysis. Each of these QTLs showed different degrees of additive effects on DTH, and two QTLs had epistatic effect on each other. These results demonstrated that genome-wide SNP analysis facilitated detection of genetic loci associated with the extreme phenotypes and revealed that the transgressive phenotypes were produced by exchanging complementary alleles of a few minor QTLs in the similar parental genotypes.

Genetic variation in blast resistance in rice germplasm from West Africa

The genetic variation in resistance to blast (Pyricularia oryzae Cavara) in 195 rice accessions comprising 3 species of the AA genome complex (Asian rice [Oryza sativa L.], African rice [Oryza glaberrima Steud.] and wild rice [Oryza barthii]) was investigated based on their patterns of reaction to standard differential blast isolates (SDBIs) and SSR marker polymorphism data. Cluster analysis of the polymorphism data of 61 SSR markers identified 3 major clusters: cluster A (mainly Japonica Group or upland accessions), cluster B (mainly Indica Group or lowland accessions) and cluster C (O. glaberrima and O. barthii). The accessions were classified again into 3 resistance groups based on reactions to SDBIs: group Ia (susceptible), group Ib (middle resistance) and group II (high resistance). Group Ia included only a few differential varieties, susceptible controls and the Japonica Group cultivar Nipponbare. Accessions in clusters A and B included all 3 resistance groups and showed a wide variation in blast resistance, but cluster C contained only group Ib. These results demonstrated that variations in Asian rice (O. sativa) accessions in West Africa were skewed toward high resistance and that variations in O. glaberrima and O. barthii were limited and lower than the Asian rice accessions.