Global Dynamic Transcriptome Programming of Rapeseed (Brassica napus L.) Anther at Different Development Stages

Li, Zhanjie; Zhang, Peipei; Lv, Jinyin; Cheng, Yufeng; Cui, Jianmin; Zhao, Huixian; Hu, Shengwu

doi:10.1371/journal.pone.0154039

Cited by 16 publications

(12 citation statements)

References 56 publications

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“…In the last decade, the large-scale microarray or RNA-sequencing technique has been widely applied for profiling transcripts of various plant tissues. The large-scale or genome-wide transcript profiling of reproductive tissues has been reported in Arabidopsis [39,55,56], tobacco [57][58][59], rice [8,23,25,60,61], maize [16,[62][63][64][65][66], and other species [42,67,68]. The newly developed technology for crop hybrid seed production, called Seed Production Technology (SPT), creates "maintainers" to propagate the seeds of recessive genic male sterile (ms) lines [54].…”

Section: Introductionmentioning

confidence: 99%

A Rapid Pipeline for Pollen- and Anther-Specific Gene Discovery Based on Transcriptome Profiling Analysis of Maize Tissues

Shi

Guo

et al. 2021

IJMS

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Recently, crop breeders have widely adopted a new biotechnology-based process, termed Seed Production Technology (SPT), to produce hybrid varieties. The SPT does not produce nuclear male-sterile lines, and instead utilizes transgenic SPT maintainer lines to pollinate male-sterile plants for propagation of nuclear-recessive male-sterile lines. A late-stage pollen-specific promoter is an essential component of the pollen-inactivating cassette used by the SPT maintainers. While a number of plant pollen-specific promoters have been reported so far, their usefulness in SPT has remained limited. To increase the repertoire of pollen-specific promoters for the maize community, we conducted a comprehensive comparative analysis of transcriptome profiles of mature pollen and mature anthers against other tissue types. We found that maize pollen has much less expressed genes (>1 FPKM) than other tissue types, but the pollen grain has a large set of distinct genes, called pollen-specific genes, which are exclusively or much higher (100 folds) expressed in pollen than other tissue types. Utilizing transcript abundance and correlation coefficient analysis, 1215 mature pollen-specific (MPS) genes and 1009 mature anther-specific (MAS) genes were identified in B73 transcriptome. These two gene sets had similar GO term and KEGG pathway enrichment patterns, indicating that their members share similar functions in the maize reproductive process. Of the genes, 623 were shared between the two sets, called mature anther- and pollen-specific (MAPS) genes, which represent the late-stage pollen-specific genes of the maize genome. Functional annotation analysis of MAPS showed that 447 MAPS genes (71.7% of MAPS) belonged to genes encoding pollen allergen protein. Their 2-kb promoters were analyzed for cis-element enrichment and six well-known pollen-specific cis-elements (AGAAA, TCCACCA, TGTGGTT, [TA]AAAG, AAATGA, and TTTCT) were found highly enriched in the promoters of MAPS. Interestingly, JA-responsive cis-element GCC box (GCCGCC) and ABA-responsive cis-element-coupling element1 (ABRE-CE1, CCACC) were also found enriched in the MAPS promoters, indicating that JA and ABA signaling likely regulate pollen-specific MAPS expression. This study describes a robust and straightforward pipeline to discover pollen-specific promotes from publicly available data while providing maize breeders and the maize industry a number of late-stage (mature) pollen-specific promoters for use in SPT for hybrid breeding and seed production.

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Section: Introductionmentioning

confidence: 99%

A Rapid Pipeline for Pollen- and Anther-Specific Gene Discovery Based on Transcriptome Profiling Analysis of Maize Tissues

Shi

Guo

et al. 2021

IJMS

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“…For instance, CL9691.Contig3 and Unigene23027 encoded stigma-specific peroxidase, CL831.Contig1 and Unigene47365 encoded mitogen-activated protein kinase (MAPK), and CL916.Contig6 and Unigene590 encoded pistil-specific extensin-like protein. Meanwhile, on the basis of previous studies [ 41 , 42 ], in another transcriptome analysis, some unigenes participating in pollen germination, pollen exine formation, pollen tube reception and pollen tube growth were found. For example, CL500.Contig1 and CL3143.Contig2 participated in pollen germination, CL12767.Contig2 took part in pollen exine formation, CL6315.Contig9 participated in pollen tube reception, and CL9992.Contig1 took part in pollen tube growth.…”

Section: Discussionmentioning

confidence: 95%

“…Unigene sequences were aligned by Blastx to protein databases such as NR (NCBI nonredundant protein), Swiss-Prot, KEGG (Kyoto Encyclopedia of Genes and Genomes) and COG (Cluster of Orthologous Groups) and aligned by Blastn to the nucleotide database NT ( E -value < 0.00001). In addition, we used Blast2 GO program [ 58 ] to obtain GO (Gene Ontology) [ 41 ] annotation of unigenes. GO has three ontologies describing molecular function, cellular component and biological process.…”

Section: Methodsmentioning

confidence: 99%

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Investigation of Differences in Fertility among Progenies from Self-Pollinated Chrysanthemum

Fan

Zhong

Wang

et al. 2018

IJMS

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Most chrysanthemum cultivars are self-incompatible, so it is very difficult to create pure lines that are important in chrysanthemum breeding and theoretical studies. In our previous study, we obtained a self-compatible chrysanthemum cultivar and its self-pollinated seed set was 56.50%. It was interesting that the seed set of its ten progenies ranged from 0% to 37.23%. Examination of the factors causing the differences in the seed set will lead to an improved understanding of chrysanthemum self-incompatibility, and provide valuable information for creating pure lines. Pollen morphology, pollen germination percentage, pistil receptivity and embryo development were investigated using the in vitro culture method, the paraffin section technique, scanning electron microscopy and transmission electron microscopy. Moreover, RNA sequencing and bioinformatics were applied to analyzing the transcriptomic profiles of mature stigmas and anthers. It was found that the self-pollinated seed set of “Q10-33-1①”,”Q10-33-1③”,”Q10-33-1④” and “Q10-33-1⑩” were 37.23%, 26.77%, 7.97% and 0%, respectively. The differences in fertility among four progenies were mainly attributable to differences in pollen germination percentage and pistil receptivity. Failure of the seed set in “Q10-33-1⑩” was possibly due to self-incompatibility. In the transcriptomic files, 22 potential stigma S genes and 8 potential pollen S genes were found out.

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“…The Cut1 gene encodes a long chain fatty acid condensing enzyme that converts fatty acids into cuticular wax (Millar et al, 1999), and many polysaccharide and fatty acid metabolic synthases are necessary for pollen viability and germination. Transcriptome analysis revealed dynamic changes in gene expression between early lipid metabolism and late carbohydrate metabolism during anther development (Li et al, 2016). The second mitosis occurs in rice with three-nucleated pollen (Tanaka, 1997).…”

Section: Introductionmentioning

confidence: 99%

Quantitative Proteomics and Transcriptomics Reveals Differences in Proteins During Anthers Development in Oryza longistaminata

et al. 2021

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Oryza longistaminata is an African wild rice species that possesses special traits for breeding applications. Self-incompatibility is the main cause of sterility in O. longistaminata, but here we demonstrated that its pollen vitality are normal. Lipid and carbohydrate metabolism were active throughout pollen development. In this study, we used I2-KI staining and TTC staining to investigate pollen viability. Aniline-blue-stained semithin sections were used to investigate important stages of pollen development. Tandem mass tags (TMT)-based quantitative analysis was used to investigate the profiles of proteins related to lipid and carbohydrate metabolism in 4-, 6-, and 8.5-mm O. longistaminata spikelets before flowering. Pollen was found to germinate normally in vitro and in vivo. We documented cytological changes throughout important stages of anther development, including changes in reproductive cells as they formed mature pollen grains through meiosis and mitosis. A total of 31,987 RNA transcripts and 8,753 proteins were identified, and 6,842 of the proteins could be quantified. RNA-seq and proteome association analysis indicated that fatty acids were converted to sucrose after the 6-mm spikelet stage, based on the abundance of most key enzymes of the glyoxylate cycle and gluconeogenesis. The abundance of proteins involved in pollen energy metabolism was further confirmed by combining quantitative real-time PCR with parallel reaction monitoring (PRM) analyses. In conclusion, our study provides novel insights into the pollen viability of O. longistaminata at the proteome level, which can be used to improve the efficiency of male parent pollination in hybrid rice breeding applications.

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Global Dynamic Transcriptome Programming of Rapeseed (Brassica napus L.) Anther at Different Development Stages

Cited by 16 publications

References 56 publications

A Rapid Pipeline for Pollen- and Anther-Specific Gene Discovery Based on Transcriptome Profiling Analysis of Maize Tissues

A Rapid Pipeline for Pollen- and Anther-Specific Gene Discovery Based on Transcriptome Profiling Analysis of Maize Tissues

Investigation of Differences in Fertility among Progenies from Self-Pollinated Chrysanthemum

Quantitative Proteomics and Transcriptomics Reveals Differences in Proteins During Anthers Development in Oryza longistaminata

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