Pervasive interactions of Sa and Sb loci cause high pollen sterility and abrupt changes in gene expression during meiosis that could be overcome by double neutral genes in autotetraploid rice

BACKGROUND: Intersubspecific autotetraploid rice hybrids possess high hybrid vigor; however, low pollen fertility is a critical hindrance in its commercial utilization. Our previous study demonstrated that polyploidy could increase the multi-loci interaction and cause high pollen abortion in autotetraploid rice hybrids. However, there is little known about the critical role of pollen sterility locus or loci in the intersubspecific hybrids. We developed autotetraploid rice hybrids harboring heterozygous genotypes (S ⁱ S ⁱ S ʲ S ʲ) at different pollen sterility loci by using the near isogenic lines of Taichung65-4×. Moreover, autotetraploid lines carrying double neutral genes, Sa ⁿ and Sb ⁿ , were used to assess their effect on fertility restoration. RESULTS: Cytological studies showed that the deleterious genetic interactions at Sa and Sb pollen sterility loci resulted in higher pollen sterility (76.83%) and abnormal chromosome behavior (24.59%) at metaphase I of meiosis in autotetraploid rice hybrids. Transcriptome analysis revealed 1092 differentially expressed genes (DEG) in a hybrid with the pervasive interactions at Sa and Sb pollen sterility loci, and most of the genes (about 83%) exhibited down regulation. Of the DEG, 60 were associated with transcription regulation and 18 genes were annotated as meiosis-related genes. Analysis on the hybrids developed by using autotetraploid rice harboring double neutral genes, Sa ⁿ and Sb ⁿ , revealed normal pollen fertility, and transcriptome analysis showed non-significant difference in number of DEG among different hybrids. CONCLUSIONS: Our finding revealed that pervasive interactions at Sa and Sb pollen sterility loci cause high sterility in the autotetraploid hybrids that lead to the down-regulation of important meiosis-related genes and transcription regulation factors. Moreover, we also found that the hybrids sterility could be overcome by double neutral genes, Sa ⁿ and Sb ⁿ , in autotetraploid rice hybrids. The present study provided a strong evidence for the utilization of heterosis in autotetraploid rice hybrids.