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Analysis of anther transcriptomes to identify genes contributing to meiosis and male gametophyte development in rice

ABSTRACT: Background – In flowering plants, the anther is the site of male gametophyte development. Two major events in the development of the male germline are meiosis and the asymmetric division in the male gametophyte that gives rise to the vegetative and generative cells, and the following mitotic division in the generative cell that produces two sperm cells. Anther transcriptomes have been analyzed at progressive stages of development by using microarray and sequence by synthesis technologies to identify genes that regulate anther development. Here we have carried out a comprehensive analysis of rice anther transcriptomes at four distinct stages of development with a focus to identify regulatory components contributing to male meiosis and germline development. Further, these transcriptomes have been compared with transcriptomes of 10 stages of rice vegetative and seed development to identify genes that express specifically during anther development. Results - To understand the molecular processes that lead to male gametophyte development, transcriptome profiling of four stages of anther development in rice [pre-meiotic (PMA), meiotic (MA), anthers at single-celled (SCP) and tri-nucleate pollen (TPA)] was conducted. Around 22,000 genes were found to be expressed in at least one of the anther developmental stages, with the highest number in MA (18,090) and lowest (15,465) in TPA. Comparison of these transcriptome profiles to an in-house generated microarray-based transcriptomics database comprising of 10 stages/tissues of vegetative as well as reproductive development in rice resulted in the identification of 1,000 genes that are specifically expressed in anther stages. Of them the expression of 453 genes was found to be specific to TPA, whereas 78 and 184 genes were expressed specifically in MA and SCP. Gene ontology and pathway analysis of specifically expressed genes revealed that transcription factors and protein folding, sorting and degradation pathway genes dominated in MA, whereas in TPA, those coding for cell structure and signal transduction components were in abundance. Interestingly, about 50% of the genes with anther-specific expression have not been annotated so far. Conclusions - These data not only provide the transcriptome constituents of four landmark stages of anther development but also identify genes that express exclusively in these stages and therefore may contribute to specific aspects of anther and/or male gametophyte development in rice. Moreover, these gene sets assist in building a deeper understanding of underlying regulatory networks and in selecting candidates for gene function validation.

ORGANISM(S): Oryza sativa Oryza sativa Indica Group

PROVIDER: GSE27726 | GEO | 2011/06/10

SECONDARY ACCESSION(S): PRJNA138101

REPOSITORIES: GEO

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Project description:Background – In flowering plants, the anther is the site of male gametophyte development. Two major events in the development of the male germline are meiosis and the asymmetric division in the male gametophyte that gives rise to the vegetative and generative cells, and the following mitotic division in the generative cell that produces two sperm cells. Anther transcriptomes have been analyzed at progressive stages of development by using microarray and sequence by synthesis technologies to identify genes that regulate anther development. Here we have carried out a comprehensive analysis of rice anther transcriptomes at four distinct stages of development with a focus to identify regulatory components contributing to male meiosis and germline development. Further, these transcriptomes have been compared with transcriptomes of 10 stages of rice vegetative and seed development to identify genes that express specifically during anther development. Results - To understand the molecular processes that lead to male gametophyte development, transcriptome profiling of four stages of anther development in rice [pre-meiotic (PMA), meiotic (MA), anthers at single-celled (SCP) and tri-nucleate pollen (TPA)] was conducted. Around 22,000 genes were found to be expressed in at least one of the anther developmental stages, with the highest number in MA (18,090) and lowest (15,465) in TPA. Comparison of these transcriptome profiles to an in-house generated microarray-based transcriptomics database comprising of 10 stages/tissues of vegetative as well as reproductive development in rice resulted in the identification of 1,000 genes that are specifically expressed in anther stages. Of them the expression of 453 genes was found to be specific to TPA, whereas 78 and 184 genes were expressed specifically in MA and SCP. Gene ontology and pathway analysis of specifically expressed genes revealed that transcription factors and protein folding, sorting and degradation pathway genes dominated in MA, whereas in TPA, those coding for cell structure and signal transduction components were in abundance. Interestingly, about 50% of the genes with anther-specific expression have not been annotated so far. Conclusions - These data not only provide the transcriptome constituents of four landmark stages of anther development but also identify genes that express exclusively in these stages and therefore may contribute to specific aspects of anther and/or male gametophyte development in rice. Moreover, these gene sets assist in building a deeper understanding of underlying regulatory networks and in selecting candidates for gene function validation. Overall twelve samples were analyzed representing four anther development stages, with three replicates of each stage.

Project description:Gene expression throughout the reproductive process in rice (Oryza sativa) beginning with primordia development through pollination/fertilization to zygote formation was analyzed. We analyzed 25 stages/organs of rice reproductive development including early microsporogenesis stages with 57,381 probe sets, and identified around 26,000 expressed probe sets in each stage. Fine dissection of 25 reproductive stages/organs combined with detailed microarray profiling revealed dramatic, coordinated and finely tuned changes in gene expression. Decrease of expressed genes in the pollen maturation process was observed in a similar way with Arabidopsis and maize. An almost equal number of ab initio predicted genes and cloned genes appeared or disappeared coordinated with developmental stage progression. A large number of organ-/stage-specific genes were identified; notably 2,593 probe sets for developing anther, including 932 probe sets corresponding to ab initio predicted genes. Analysis of cell cycle-related genes revealed that several CDKs, cyclins and components of SCF E3 ubiquitin ligase complexes were expressed specifically in reproductive organs. Cell wall biosynthesis or degradation protein genes and transcription factor genes expressed specifically in reproductive stages were also newly identified. Rice genes homologous to reproduction-related genes in other plants showed expression profiles both consistent and inconsistent with their predicted functions. The rice reproductive expression atlas is likely to be the deepest and most comprehensive dataset available, indispensable for unraveling functions of many specific genes in plant reproductive processes that have not yet been thoroughly analyzed. This SuperSeries is composed of the following subset Series: GSE13988: Rice expression atlas (1): Anther development GSE14298: Rice expression atlas (2): Pollination - Fertilization GSE14299: Rice expression atlas (3): Early embryogenesis GSE14300: Rice expression atlas (4): Vegetative tissues GSE14301: Rice expression atlas (5): Anther development (Agilent data) Refer to individual Series

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Analysis of anther transcriptomes to identify genes contributing to meiosis and male gametophyte development in rice

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