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Male reproductive development: gene expression profiling of maize anther and pollen ontogeny.

ABSTRACT: During flowering, central anther cells switch from mitosis to meiosis, ultimately forming pollen containing haploid sperm. Four rings of surrounding somatic cells differentiate to support first meiosis and later pollen dispersal. Synchronous development of many anthers per tassel and within each anther facilitates dissection of carefully staged maize anthers for transcriptome profiling.Global gene expression profiles of 7 stages representing 29 days of anther development are analyzed using a 44 K oligonucleotide array querying approximately 80% of maize protein-coding genes. Mature haploid pollen containing just two cell types expresses 10,000 transcripts. Anthers contain 5 major cell types and express >24,000 transcript types: each anther stage expresses approximately 10,000 constitutive and approximately 10,000 or more transcripts restricted to one or a few stages. The lowest complexity is present during meiosis. Large suites of stage-specific and co-expressed genes are identified through Gene Ontology and clustering analyses as functional classes for pre-meiotic, meiotic, and post-meiotic anther development. MADS box and zinc finger transcription factors with constitutive and stage-limited expression are identified.We propose that the extensive gene expression of anther cells and pollen represents the key test of maize genome fitness, permitting strong selection against deleterious alleles in diploid anthers and haploid pollen. Because flowering plants show a substantial bias for male-sterile compared to female-sterile mutations, we propose that this fitness test is general. Because both somatic and germinal cells are transcriptionally quiescent during meiosis, we hypothesize that successful completion of meiosis is required to trigger maturation of anther somatic cells.

SUBMITTER: Ma J

PROVIDER: S-EPMC2646285 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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Male reproductive development: gene expression profiling of maize anther and pollen ontogeny.

Ma Jiong J Skibbe David S DS Fernandes John J Walbot Virginia V

Genome biology 20081219 12

<h4>Background</h4>During flowering, central anther cells switch from mitosis to meiosis, ultimately forming pollen containing haploid sperm. Four rings of surrounding somatic cells differentiate to support first meiosis and later pollen dispersal. Synchronous development of many anthers per tassel and within each anther facilitates dissection of carefully staged maize anthers for transcriptome profiling.<h4>Results</h4>Global gene expression profiles of 7 stages representing 29 days of anther d ...[more]

PMID: 19099579

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Project description: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.

Project description:BackgroundCotton (Gossypium hirsutum) anther development involves a diverse range of gene interactions between sporophytic and gametophytic tissues. However, only a small number of genes are known to be specifically involved in this developmental process and the molecular mechanism of the genetic male sterility (GMS) is still poorly understand. To fully explore the global gene expression during cotton anther development and identify genes related to male sterility, a digital gene expression (DGE) analysis was adopted.ResultsSix DGE libraries were constructed from the cotton anthers of the wild type (WT) and GMS mutant (in the WT background) in three stages of anther development, resulting in 21,503 to 37,352 genes detected in WT and GMS mutant anthers. Compared with the fertile isogenic WT, 9,595 (30% of the expressed genes), 10,407 (25%), and 3,139 (10%) genes were differentially expressed at the meiosis, tetrad, and uninucleate microspore stages of GMS mutant anthers, respectively. Using both DGE experiments and real-time quantitative RT-PCR, the expression of many key genes required for anther development were suppressed in the meiosis stage and the uninucleate microspore stage in anthers of the mutant, but these genes were activated in the tetrad stage of anthers in the mutant. These genes were associated predominantly with hormone synthesis, sucrose and starch metabolism, the pentose phosphate pathway, glycolysis, flavonoid metabolism, and histone protein synthesis. In addition, several genes that participate in DNA methylation, cell wall loosening, programmed cell death, and reactive oxygen species generation/scavenging were activated during the three anther developmental stages in the mutant.ConclusionsCompared to the same anther developmental stage of the WT, many key genes involved in various aspects of anther development show a reverse gene expression pattern in the GMS mutant, which indicates that diverse gene regulation pathways are involved in the GMS mutant anther development. These findings provide the first insights into the mechanism that leads to genetic male sterility in cotton and contributes to a better understanding of the regulatory network involved in anther development in cotton.

Dataset Information

Male reproductive development: gene expression profiling of maize anther and pollen ontogeny.

Publications

Male reproductive development: gene expression profiling of maize anther and pollen ontogeny.

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