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Genome-wide analysis of DNA polymorphisms, the methylome and transcriptome revealed that multiple factors are associated with low pollen fertility in autotetraploid rice.

ABSTRACT: Autotetraploid rice is a useful germplasm with high biomass production; however, low fertility is the main barrier in commercial utilization. In our previous study, differential expression of meiosis-related miRNAs was found to be involved in the pollen sterility of autotetraploid rice. However, genome-wide DNA variations and methylomes associated with low fertility of autotetraploid rice are still poorly understood. Here, we measured both global DNA variations and the methylome and compared them with the transcriptome during pollen development in autotetraploid rice by high-throughput sequencing. A total of 34416 SNPs, 6993 InDels, 1003 SVs and 25 CNVs were detected, and 11367 and 41117 differentially methylated regions showed hypermethylation and hypomethylation in 02428-4x. In total, 1110 genes displayed differentially expression in 02428-4x during meiosis, of these six harbored CNVs, including four upregulated genes with gain CNVs, such as LOC_Os11g38620. We identified 122 genes by comparing with the previous data that might be associated with low fertility during pollen development in 02428-4x. Of the 122 gens, 98 were displayed methylation and differential expression, including OsMADS98, CYP703A3 and OsABCG26. The downregulation of these three genes were confirmed by qPCR during meiosis of 02428-4x, which played pivotal roles in pollen fertility. These results indicate that the low fertility of autotetraploid rice is not only caused by the differential expression of genes involved in pollen development, but also by sequence variation and differential methylation, suggesting that the reason for pollen sterility in autotetraploid rice is complex and might be affected by multiple factors.

SUBMITTER: Li X

PROVIDER: S-EPMC6078310 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Genome-wide analysis of DNA polymorphisms, the methylome and transcriptome revealed that multiple factors are associated with low pollen fertility in autotetraploid rice.

Li Xiang X Yu Hang H Jiao Yamin Y Shahid Muhammad Qasim MQ Wu Jinwen J Liu Xiangdong X

PloS one 20180806 8

Autotetraploid rice is a useful germplasm with high biomass production; however, low fertility is the main barrier in commercial utilization. In our previous study, differential expression of meiosis-related miRNAs was found to be involved in the pollen sterility of autotetraploid rice. However, genome-wide DNA variations and methylomes associated with low fertility of autotetraploid rice are still poorly understood. Here, we measured both global DNA variations and the methylome and compared the ...[more]

PMID: 30080873

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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.

Project description:Background: Partial pollen and embryo sac sterilities are the two main reasons for low fertility in autotetraploid rice. Our previous study revealed that small RNAs changes may associate with pollen fertility in autotetraploid rice. However, knowledge on comparative analysis between the development of pollen and embryo sac by small RNAs in autotetraploid rice is still unknown. In the present study, WE-CLSM (whole-mount eosin B-staining confocal laser scanning microscopy) and high-throughput sequencing technology was employed to examine the cytological variations and to analyze small RNAs changes during pollen and embryo sac development in autotetraploid rice compared with its diploid counterpart. Results: A total of 321 and 368 differentially expressed miRNAs (DEM) were detected during development of pollen and embryo sac in autotetraploid rice, respectively. Gene Ontology enrichment analysis on the targets of miRNAs-enriched during the development of pollen and embryo sac in autotetraploid rice revealed 30 prominent functional gene classes, such as cell differentiation and signal transduction during embryo sac development. However, only 7 prominent functional gene classes, such as flower development and transcription factor activity, were detected during pollen development. The expression levels of 39 DEM, which revealed interaction with meiosis-related genes, showed opposite expression levels in pollen and embryo sac development. Of these DEM, osa-miR1436_L+3_1ss5CT and osa-miR167h-3p were associated with the female meiosis, while osa-miR159a.1 and osa-MIR159a-p5 were related with the male meiosis. 21nt-phasiRNAs were detected both during pollen and embryo sac development, while 24nt-phasiRNAs were found only in pollen development, which displayed down-regulation in autotetraploid compared to diploid rice and their spatial-temporal expression patterns were similar to osa-miR2275d. 24nt TEs-siRNAs were found to be up-regulated in embryo sac but down-regulated in pollen development. Conclusion: The above results not only provide the small RNAs changes during four landmark stages of pollen and embryo sac development in autotetraploid rice but also have identified specifically expressed miRNAs, especially meiosis-related miRNAs, pollen-24nt-phasiRNAs and TEs-siRNAs in autotetraploid rice. Together, these findings provide a foundation for understanding the effect of polyploidy on small RNAs expression patterns during pollen and embryo sac development that may lead to different abnormalities in autotetraploid rice.

Project description:BackgroundAutotetraploid rice hybrids have great potential to increase the production, but hybrid sterility is a major hindrance in the utilization of hybrid vigor in polyploid rice, which is mainly caused by pollen abortion. Our previous study showed that double pollen fertility neutral genes, Sa-n and Sb-n, can overcome hybrid sterility in autotetraploid rice. Here, we used an autotetraploid rice line harboring double neutral genes to develop hybrids by crossing with auto- and neo-tetraploid rice, and evaluated heterosis and its underlying molecular mechanism.ResultsAll autotetraploid rice hybrids, which harbored double pollen fertility neutral genes, Sa-n and Sb-n, displayed high seed setting and significant positive heterosis for yield and yield-related traits. Cytological observations revealed normal chromosome behaviors and higher frequency of bivalents in the hybrid than parents during meiosis. Transcriptome analysis revealed significantly higher expressions of important saccharides metabolism and starch synthase related genes, such as OsBEIIb and OsSSIIIa, in the grains of hybrid than parents. Furthermore, many meiosis-related and specific genes, including DPW and CYP703A3, displayed up-regulation in the hybrid compared to a parent with low seed setting. Many non-additive genes were detected in the hybrid, and GO term of carbohydrate metabolic process was significantly enriched in all the transcriptome tissues except flag leaf (three days after flowering). Moreover, many differentially expressed genes (DEGs) were identified in the yield-related quantitative trait loci (QTLs) regions as possible candidate genes.ConclusionOur results revealed that increase in the number of bivalents improved the seed setting of hybrid harboring double pollen fertility neutral genes. Many important genes, including meiosis-related and meiosis-specific genes and saccharides metabolism and starch synthase related genes, exhibited heterosis specific expression patterns in polyploid rice during different development stages. The functional analysis of important genes will provide valuable information for molecular mechanisms of heterosis in polyploid rice.

Dataset Information

Genome-wide analysis of DNA polymorphisms, the methylome and transcriptome revealed that multiple factors are associated with low pollen fertility in autotetraploid rice.

Publications

Genome-wide analysis of DNA polymorphisms, the methylome and transcriptome revealed that multiple factors are associated with low pollen fertility in autotetraploid rice.

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