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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.

ABSTRACT: 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.

SUBMITTER: Wu J

PROVIDER: S-EPMC5712294 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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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.

Wu Jinwen J Chen Lin L Shahid Muhammad Qasim MQ Chen Minyi M Dong Qinglei Q Li Jirui J Xu Xiaosong X Liu Xiangdong X

Rice (New York, N.Y.) 20171202 1

<h4>Background</h4>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 harborin ...[more]

PMID: 29197985

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Project description:Double pollen fertility neutral genes, San and Sbn, can control pollen sterility in intersubspecific (indica × japonica) rice hybrids, which has excellent potential to increase rice yield. Previous studies showed that polyploidy could increase the interaction of three pollen sterility loci, i.e. Sa, Sb and Sc, which cause pollen sterility in autotetraploid rice hybrids, and hybrid fertility could be improved by double neutral genes, San and Sbn, in autotetraploid rice hybrids. We compared cytological and transcriptome data between autotetraploid and diploid rice hybrid during meiosis and single microspore stages to understand the molecular mechanism of neutral genes for overcoming pollen sterility in autotetraploid rice hybrids, which harbored double neutral genes. Cytological results revealed that the double neutral genes resulted in higher pollen fertility (76.74%) and lower chromosomal abnormalities in autotetraploid hybrid than in parents during metaphase I, metaphase II, anaphase I and anaphase II. Moreover, autotetraploid rice hybrid displayed stronger heterosis than a diploid hybrid. Compared with diploid rice hybrid, a total of 904 and 68 differently expressed genes (DEGs) were identified explicitly in autotetraploid hybrid at meiosis and single microspore stages, respectively. Of these, 133 and 41 genes were detected in higher-parent dominance and transgressive up-regulation dominance, respectively, which were considered autotetraploid potential heterosis genes, including a meiosis-related gene (Os01g0917500, MSP1) and two meiosis specific-genes (Os07g0624900 and Os04g0208600). Gene Ontology (GO) and Kyoto Encyclopedia of Gene and Genomes pathway (KEGG) analysis revealed that DEGs significantly enriched in amino acid metabolism and photosynthesis metabolism. These results indicated that meiosis-specific and meiosis-related genes, and amino acids and photosynthesis metabolism-related genes contribute to higher yield and pollen fertility in autotetraploid rice hybrid. This study provides a theoretical basis for molecular mechanisms of heterosis in autotetraploid rice harboring double neutral genes for pollen fertility.

Project description:BackgroundAutotetraploid rice is a useful germplasm for polyploid rice breeding. Our previous research showed that non-coding RNAs might be associated with low fertility in autotetraploid rice. However, little information is available on long non-coding RNAs (lncRNAs) involved in the low fertility of autotetraploid rice. In the present study, RNA-seq was employed to detect the differentially expressed meiosis-related lncRNAs in autotetraploid rice, and gene overexpression and knock out experiments were used to validate the potential function of candidate lncRNA.ResultsA total of 444 differentially expressed lncRNAs (DEL) were detected during anther and ovary meiosis in autotetraploid rice. Of these, 328 DEL were associated with the transposable elements, which displayed low expression levels during meiosis in autotetraploid rice. We used rapid amplification of cDNA ends (RACE) assay to validate 10 DEL and found that the lncRNAs were not assembly artifacts, and six of them were conserved in tetraploid rice. Moreover, 237 and 20 lncRNAs were associated with pollen mother cell (PMC) and embryo sac mother cell (EMC) meiosis in autotetraploid rice, respectively. The differential expressions of some meiosis-related targets and its DEL regulator, including MEL1 regulated by TCONS_00068868, LOC_Os12g41350 (meiotic asynaptic mutant 1) by TCONS_00057811 in PMC, and LOC_Os12g39420 by TCONS_00144592 in EMC, were confirmed by qRT-PCR. TCONS_00057811, TCONS_00055980 and TCONS_00130461 showed anther specific expression patterns and were found to be highly expressed during meiosis. CRISPR/Cas9 editing of lncRNA57811 displayed similar morphology compared to wild type. The overexpression of lncRNA57811 resulted in low pollen fertility (29.70%) and seed setting (33%) in rice.ConclusionThe differential expression levels of lncRNAs, associated with transposable elements and meiosis-regulated targets, might be endogenous noncoding regulators of pollen/embryo sac development that cause low fertility in autotetraploid rice. The results enhance our understanding about rice lncRNAs, and facilitate functional research in autotetraploid rice.

Dataset Information

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.

Publications

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.

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