Various Spatiotemporal Expression Profiles of Anther-Expressed Genes in Rice

Faculty of Science, Tohoku University, Sendai, 980-8587 Japan
Plant and Cell Physiology (Impact Factor: 4.98). 10/2008; 49(10):1417-28. DOI: 10.1093/pcp/pcn128
Source: PubMed

ABSTRACT The male gametophyte and tapetum play different roles during anther development although they are differentiated from the same cell lineage, the L2 layer. Until now, it has not been possible to delineate their transcriptomes due to technical difficulties in separating the two cell types. In the present study, we characterized the separated transcriptomes of the rice microspore/pollen and tapetum using laser microdissection (LM)-mediated microarray. Spatiotemporal expression patterns of 28,141 anther-expressed genes were classified into 20 clusters, which contained 3,468 (12.3%) anther-enriched genes. In some clusters, synchronous gene expression in the microspore and tapetum at the same developmental stage was observed as a novel characteristic of the anther transcriptome. Noteworthy expression patterns are discussed in connection with gene ontology (GO) categories and gene annotations, which are related to important biological events in anther development, such as pollen maturation, pollen germination, pollen tube elongation and pollen wall formation.

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Available from: Nobuhiro Tsutsumi, Aug 10, 2015
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    • "Multiple transcriptomes and several proteomes have been reported for whole anthers, utilizing organs that have completed cell specification and are proceeding through meiosis (Lu et al. 2006; Ma et al. 2007; Wijeratne et al. 2007; Skibbe et al. 2009; Wang et al. 2010a; Aya et al. 2011; Deveshwar et al. 2011; Nan et al. 2011) and for anther developmental stages after meiosis (Ma et al. 2008). Using manual or laser capture microdissection, transcriptomes are also available for isolated meiotic plant cells (Tang et al. 2010; Schmidt et al. 2011; Yang et al. 2011) and for isolated sporophytic anther tissues such as the tapetum (Hobo et al. 2008; Huang et al. 2009). Mature pollen, containing the vegetative cell and sperm, has also been characterized from multiple species (Honys and Twell 2004; Ma et al. 2006, 2008; Calarco et al. 2012). "
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    ABSTRACT: Plants lack a germ line; consequently, during reproduction adult somatic cells within flowers must switch from mitotic proliferation to meiosis. In maize (Zea mays L.) anthers, hypoxic conditions in the developing tassel trigger pre-meiotic competence in the column of pluripotent progenitor cells in the center of anther lobes, and within 24 hr these newly specified germinal cells have patterned their surrounding neighbors to differentiate as the first somatic niche cells. Transcriptomes were analyzed by microarray hybridization in carefully staged whole anthers during initial specification events, after the separation of germinal and somatic lineages, during the subsequent rapid mitotic proliferation phase, and during final pre-meiotic germinal and somatic cell differentiation. Maize anthers exhibit a highly complex transcriptome constituting nearly three-quarters of annotated maize genes, and expression patterns are dynamic. Laser microdissection was applied to begin assigning transcripts to tissue and cell types and for comparison to transcriptomes of mutants defective in cell fate specification. Whole anther proteomes were analyzed at three developmental stages by mass spectrometric peptide sequencing using size-fractionated proteins to evaluate the timing of protein accumulation relative to transcript abundance. New insights include early and sustained expression of meiosis-associated genes (77.5% of well-annotated meiosis genes are constitutively active in 0.15 mm anthers), an extremely large change in transcript abundances and types a few days before meiosis (including a class of 1340 transcripts absent specifically at 0.4 mm), and the relative disparity between transcript abundance and protein abundance at any one developmental stage (based on 1303 protein-to-transcript comparisons).
    G3-Genes Genomes Genetics 06/2014; 4(6):993-1010. DOI:10.1534/g3.113.009738 · 2.51 Impact Factor
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    • "Several analyses of the rice transcriptome have revealed distinct gene expression profiles characterizing the pollen developmental stages (Hobo et al., 2008; Fujita et al., 2010; Wang et al., 2010; Deveshwar et al., 2011; Sato et al., 2011), while our study demonstrated that the anther tissues facilitated the expression of the repeat sequences, except for ribosomal DNAs (Table II). In Arabidopsis, many repeat sequences were preferentially expressed in the vegetative nucleus of the pollen, where epigenetic reprogramming releases transcriptional silencing (Slotkin et al., 2009). "
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    ABSTRACT: Genome-wide transcriptome analyses using microarray probes containing genes and repeat sequences have been performed to examine responses to low temperatures in Oryza sativa (rice). We focused particularly on the rice anther at the booting stage because a low temperature at this stage can result in pollen abortion. The five rice strains examined in this study showed different pollen fertilities due to a low-temperature treatment during the booting stage. The microarray analyses demonstrated that the low-temperature stress caused genome-wide changes in the transcriptional activities not only of genes, but also of repeat sequences in the rice anther. The degree of the temperature-responsive changes varied among the five rice strains. Interestingly, the low temperature-sensitive strains revealed more changes in the transcriptome when compared with the tolerant strains. The expression patterns of the repeat sequences, including miniature inverted-repeat transposable elements, transposons, and retrotransposons, were correlated with the pollen fertilities of the five strains, with the highest correlation coefficient being 0.979. Even in the low temperature-sensitive strains, the transcriptomes displayed distinct expression patterns. The elements responding to the low temperatures were evenly distributed throughout the genome, and the major cis-motifs involved in temperature-responsive changes were undetectable from the upstream sequences in the corresponding repeats. The genome-wide responses of transcription to the temperature shift may be associated with chromatin dynamics, which facilitates environmental plasticity. A genome-wide analysis using repeat sequences suggested that stress tolerance could be conferred by insensitivity to the stimuli.
    Plant physiology 12/2013; 164(2). DOI:10.1104/pp.113.230656 · 7.39 Impact Factor
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    • "Spatial and temporal transcriptome profiles represent snapshot of gene activity and thus have been extensively used for deciphering the role of individual genes/pathways or regulatory networks and plausible interactions among them (Adams 2008). In fact, in the past decade, multitude of microarray-based studies have been performed towards elucidating reproductive organ development in Arabidopsis (Alves-Ferreira et al. 2007; Becerra et al. 2006; Fait et al. 2006; Hennig et al. 2004; Wellmer et al. 2006; Wellmer et al. 2004; Zhang et al. 2005; Wilson et al. 2005b; Day et al. 2008), rice (Endo et al. 2004; Furutani et al. 2006; Hobo et al. 2008; Kondou et al. 2006; Lan et al. 2004; Hirano et al. 2008; Suwabe et al. 2008; Jiao et al. 2009; Wang et al. 2010; Fujita et al. 2010; Li et al. 2007a, b; Wang et al. 2005; Deveshwar et al. 2011), maize (Grimanelli et al. 2005; Liu et al. 2008; Lee et al. 2002), wheat (Wilson et al. 2005a), and other non-model plant systems (Hansen et al. 2009; Laitinen et al. 2005; Endo et al. 2002; Tebbji et al. 2010). One of the limitations of these studies is that most of these scored the number of probe sets rather than unique transcripts as an estimate of gene expression. "
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    ABSTRACT: Carefully analyzed expression profiles can serve as a valuable reference for deciphering gene functions. We exploited the potential of whole genome microarrays to measure the spatial and temporal expression profiles of rice genes in 19 stages of vegetative and reproductive development. We could verify expression of 22,980 genes in at least one of the tissues. Differential expression analysis with respect to five vegetative tissues and preceding stages of development revealed reproductive stage-preferential/-specific genes. By using subtractive logic, we identified 354 and 456 genes expressing specifically during panicle and seed development, respectively. The metabolic/hormonal pathways and transcription factor families playing key role in reproductive development were elucidated after overlaying the expression data on the public databases and manually curated list of transcription factors, respectively. During floral meristem differentiation (P1) and male meiosis (P3), the genes involved in jasmonic acid and phenylpropanoid biosynthesis were significantly upregulated. P6 stage of panicle, containing mature gametophytes, exhibited enrichment of transcripts involved in homogalacturonon degradation. Genes regulating auxin biosynthesis were induced during early seed development. We validated the stage-specificity of regulatory regions of three panicle-specific genes, OsAGO3, OsSub42, and RTS, and an early seed-specific gene, XYH, in transgenic rice. The data generated here provides a snapshot of the underlying complexity of the gene networks regulating rice reproductive development.
    Functional & Integrative Genomics 03/2012; 12(2):229-48. DOI:10.1007/s10142-012-0274-3 · 2.69 Impact Factor
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