Comprehensive Network Analysis of Anther-Expressed Genes in Rice by the Combination of 33 Laser Microdissection and 143 Spatiotemporal Microarrays

Bioscience and Biotechnology Center, Nagoya University, Nagoya, Japan.
PLoS ONE (Impact Factor: 3.23). 10/2011; 6(10):e26162. DOI: 10.1371/journal.pone.0026162
Source: PubMed


Co-expression networks systematically constructed from large-scale transcriptome data reflect the interactions and functions of genes with similar expression patterns and are a powerful tool for the comprehensive understanding of biological events and mining of novel genes. In Arabidopsis (a model dicot plant), high-resolution co-expression networks have been constructed from very large microarray datasets and these are publicly available as online information resources. However, the available transcriptome data of rice (a model monocot plant) have been limited so far, making it difficult for rice researchers to achieve reliable co-expression analysis. In this study, we performed co-expression network analysis by using combined 44 K agilent microarray datasets of rice, which consisted of 33 laser microdissection (LM)-microarray datasets of anthers, and 143 spatiotemporal transcriptome datasets deposited in RicexPro. The entire data of the rice co-expression network, which was generated from the 176 microarray datasets by the Pearson correlation coefficient (PCC) method with the mutual rank (MR)-based cut-off, contained 24,258 genes and 60,441 genes pairs. Using these datasets, we constructed high-resolution co-expression subnetworks of two specific biological events in the anther, "meiosis" and "pollen wall synthesis". The meiosis network contained many known or putative meiotic genes, including genes related to meiosis initiation and recombination. In the pollen wall synthesis network, several candidate genes involved in the sporopollenin biosynthesis pathway were efficiently identified. Hence, these two subnetworks are important demonstrations of the efficiency of co-expression network analysis in rice. Our co-expression analysis included the separated transcriptomes of pollen and tapetum cells in the anther, which are able to provide precise information on transcriptional regulation during male gametophyte development in rice. The co-expression network data presented here is a useful resource for rice researchers to elucidate important and complex biological events.

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    • "ophyte , meta - analyses can be used to identify genes with common expression and activities between multiple data sets . The data can be used to construct in silico - derived co - expression networks and are based on the assumption that genes with similar expression patterns are likely to interact with each other . In a pioneering study in rice , Aya et al . ( 2011 ) adopted a co - expression analysis to identify ' meiosis ' and ' pollen wall synthesis ' sub - net - works . The study analysed 176 microarray data sets , in - cluding LM - microarray data separating tapetum and male gametophyte cells , to identify a robust pollen wall syn - thesis co - expression network , enriched for sporopollenin "
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    ABSTRACT: Key message Overview of pollen transcriptome studies. Pollen development is driven by gene expression, and knowledge of the molecular events underlying this process has undergone a quantum leap in the last decade through studies of the transcriptome. Here, we outline historical evidence for male haploid gene expression and review the wealth of pollen transcriptome data now available. Knowledge of the transcriptional capacity of pollen has progressed from genetic studies to the direct analysis of RNA and from gene-by-gene studies to analyses on a genomic scale. Microarray and/or RNA-seq data can now be accessed for all phases and cell types of developing pollen encompassing 10 different angiosperms. These growing resources have accelerated research and will undoubtedly inspire new directions and the application of system-based research into the mechanisms that govern the development, function and evolution of angiosperm pollen.
    Full-text · Article · Mar 2015 · Plant Reproduction
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    • "Fundamental insight into male reproduction can thus result in agricultural innovations in the multi-billion dollar hybrid seed industry. 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). "
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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).
    Full-text · Article · Jun 2014 · G3-Genes Genomes Genetics
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    • "Nonetheless, transcriptome studies are a valuable tool to detect novel specific or abundant transcripts or prevalent pathways when comparing specific cell types and developmental stages, but have to be connectable with other datasets. Excellent ways to provide this connectivity are publically available datasets of raw data together with detailed description of how they were obtained, as well as studies that produce a whole gene expression atlas, e.g., in rice with 25 reproductive stages (Fujita et al., 2010), and later with 33 laser-assisted micro-dissected anther samples and 143 spatiotemporal samples (Aya et al., 2011), in barley with 15 tissues of different developmental stages (Druka et al., 2006), in Arabidopsis with 79 samples through development (Schmid et al., 2005), or in maize with 60 diverse tissues (Sekhon et al., 2011). Data from Arabidopsis, maize and more plant species can be easily accessed and mined using the eFP Browser (; "
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    ABSTRACT: Although a number of genes that play key roles during the meiotic process have been characterized in great detail, the whole process of meiosis is still not completely unraveled. To gain insight into the bigger picture, large-scale approaches like RNA-seq and microarray can help to elucidate the transcriptome landscape during plant meiosis, discover co-regulated genes, enriched processes, and highly expressed known and unknown genes which might be important for meiosis. These high-throughput studies are gaining more and more popularity, but their beginnings in plant systems reach back as far as the 1960's. Frequently, whole anthers or post-meiotic pollen were investigated, while less data is available on isolated cells during meiosis, and only few studies addressed the transcriptome of female meiosis. For this review, we compiled meiotic transcriptome studies covering different plant species, and summarized and compared their key findings. Besides pointing to consistent as well as unique discoveries, we finally draw conclusions what can be learned from these studies so far and what should be addressed next.
    Full-text · Article · Jun 2014 · Frontiers in Plant Science
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