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Editorial |
Towards a Comprehensive Understanding of Molecular Mechanisms of Sexual Reproduction in Higher Plants
Laboratory of Plant Reproductive Genetics, Graduate School of Life Sciences, Tohoku University, Japan
Sexual reproduction in higher plants includes a key phase for producing male and female gametes (i.e. microsporogenesis, microgametogenesis, megasporogenesis and megagametogenesis), in addition to the ensuing pollination and fertilization. Development of the gametes is regulated by gametophytic and sporophytic gene expression (McCormick 2004
); for example, gametophytic microspores are influenced by gene expression in sporophytic tapetum cells of anthers. Such networks of gene expression during gamete development are quite important for the understanding of sexual reproduction, because failure of gene regulation often results in a defect of fertilization, which is known as male and/or female sterility. To date, many reproductive tissue-specific genes have been identified and characterized (Taylor and Hepler 1997, Endo et al. 2004, Kagi and Gross-Hardt 2007). However, the total picture of gene regulation of events during sexual reproduction is still not clear. This special issue consists of four original articles about transcriptome analysis focused on male gamete development, two original articles about mutant analysis of male or female gamete development, and one review article about male sterility. All the papers take up a common theme about ‘gene regulation in plant reproduction’, and should help towards a comprehensive understanding of sexual reproduction in higher plants.
Tapetum cells, which are the innermost cell layer of the anther wall, are important for feeding nutrients to microspores, and pollen maturation is accompanied by the characteristic gene expression of microspore/pollen and tapetum. Therefore, analyses of separated transcriptomes of microspore/pollen and tapetum are necessary to gain an understanding of male gametophyte development. Laser microdissection (LM) is a powerful tool for isolating specific cells from complicated plant tissues (Nakazono et al. 2003), and can be applied to these separated transcriptomes. In this issue, authors of four papers have referred to the LM 44K-microarray (44K-LMM) of microspore/pollen and tapetum in japonica rice. First, Suwabe and colleagues established the 44K-LMM with amplified labeled RNAs isolated from microspore/pollen and tapetum cells, which were physically separated from a cross-section of rice anthers. In order to validate the 44K-LMM data, they compared the 44K-LMM data with that of 156 previously characterized anther-specific genes, which were identified by Endo et al. (2004). From this validation, it was demonstrated that the 44K-LMM is highly reliable, and can be used for further comprehensive analysis of gene networks in the development of the male gametophyte (pp. 1407-1416). Secondly, Hobo and colleagues characterized 44K-LMM data by using in silico analyses (cluster analysis, gene ontology, and searching gene regulatory cis-elements and mutant phenotypes). Interestingly, synchronous gene expression between the microspore and tapetum was observed as a novel characteristic in these transcriptomes. Further detailed analyses will reveal the significance of this synchronous expression in the development of the male gamete. In addition, about half of the Tos17 insertion lines in microspore/pollen- or tapetum-specific genes showed sterile or low fertility phenotypes, indicating that these genes were necessary for the development of anther tissues (pp. 1417-1428). These two fundamental papers clearly indicate that these precise transcriptome data sets of male gametophyte development are useful for understanding various phenomena in the anther, and will shed light on new research fields of plant reproduction.
The relationship between phytohormones and microspore/pollen and tapetum transcriptomes is one of the most interesting findings using this 44K-LMM. The phytohormones are important for plant growth, development, differentiation, etc. However, only a few functions in microspore/pollen and tapetum development are known. To date, many genes encoding the regulation of biosynthesis, perception and signal transduction of several phytohormones have been identified and characterized (Guo and Ecker 2004, Guilfoyle and Hagen 2007, Li and Jin 2007, Ueguchi-Tanaka et al. 2007, Verslues and Zhu 2007, McSteen and Zhao 2008). The comprehensive investigation of gene expression of these genes will help to understand the functions of the phytohormone in the development of microspore/pollen and tapetum. In this issue, Hirano and colleagues surveyed the expression profile of genes related to seven phytohormones during rice anther development by using the 44K-LMM (pp. 1429- 1450). Interestingly, genes encoding enzymes involved in the biosynthesis of ethylene, gibberellin and IAA were highly expressed in mature pollen. In fact, gibberellin and IAA were highly accumulated in the mature anther. These analyzed data for phytohormone-related genes will be an important milestone for the understanding of microspore/pollen and tapetum development from the viewpoint of phytohormones.
On the other hand, the cis-regulatory elements of genes are closely related to spatiotemporal gene expression (Yamaguchi-Shinozaki and Shinozaki 2005). The huge microarray data sets are good examples for identification of cis-regulatory elements. In this issue, Mihara and colleagues established a new algorithm to extract candidates for cis-regulatory elements from promoter regions of rice associated with 44K-LMM data. Furthermore, they added the 44K-LMM data into a database termed the SALAD database, which was recently developed (pp. 1451-1464). In this database, we can compare the expression profiles of 44K-LMM data in any gene clusters based on annotation similarity (or paralogous genes of rice). This allowed them to compare candidates for cis-elements in the gene regions of paralogous genes, and found candidates more frequently for members which conferred specific gene expression than for negative control paralogous genes. Furthermore, the display of this 44K-LMM in the SALAD database clusterings will provide genome-wide useful information in plant reproductive biology, and will be applicable to any LMM data in other fields of plant biology.
Exine, which is formed around the microspore during microsporogenesis, is the outer layer of the pollen grain, and its morphology is highly diverged among plant species. On formation of exine, the tapetum cell, which functions as a nurse cell by secretion of nutrients and other secondary metabolites, has an important role (Goldberg et al. 1993). In male-sterile mutants, several types of exine formation mutants were identified and characterized (Ariizumi and Toriyama 2007). However, knowledge of the molecular mechanism of formation of the complex exine architecture is far from comprehensive. Suzuki and colleagues identified 12 novel mutants (kns1 to kns12) whose pollen grains had an abnormal exine structure. Interestingly, 11 kns mutants did not affect the pollen viability. The KNS2 gene was cloned and encoded sucrose-phosphate synthase, indicating that the KNS2 enzyme might be required for synthesis of primexine or callose wall (pp. 1465-1477). Combining sterile mutants and fertile mutants which both have abnormal exine architecture will help to understand fully the molecular mechanism of exine formation. Furthermore, such an understanding will affect pollen biology (e.g. self-incompatibility, pollen–stigma interaction; Watanabe et al. (2008)).
The female gamete (egg cell) is formed in the ovule through megasporogenesis and megagametogenesis. As a result, four different kinds of cells (egg cell, synergid cell, central cell and antipodal cell) are differentiated in the embryo sac. This differentiation pattern is quite distinct from that of microsporogenesis and pollen maturation (Goldberg et al. 1993, Reiser and Fisher 1993). From the molecular dissection of female-sterile lines, a few molecules regulating embryo sac development and pollen tube guidance have been isolated and characterized (Kagi and Gross-Hardt 2007). Furthermore, in vitro analysis of pollen tube guidance using Torenia fournieri showed that synergid cells emitted a diffusible guidance molecule (Higashiyama and Hamamura 2008). In this issue, Shimizu and colleagues characterized the mma3 mutant, a female gametophytic lethal mutant. The MAA3 gene was a homologous gene to that encoding yeast Sen1 helicase, suggesting that RNA molecules could be responsible for nucleolar organization and tube guidance (pp. 1478-1483). This finding will open up a new field of plant reproductive biology as well as other phenomena regulated via cell–cell communications.
Cytoplasmic male sterility (CMS) is an important trait for the F1 hybrid breeding program in rice, beet, onion, etc. (Hanson and Bentolila 2004). CMS occurs as a result of incompatibility between the nuclear genome and the mitochondrial genome, and is a good model system for understanding the interaction of different genomes. Fujii and Toriyama reviewed the recent progress in understanding the molecular mechanisms of CMS, focusing especially on the relationship between pollen fertility and anterograde/retrograde signaling (pp. 1484-1494). Because anterograde/retrograde signaling was observed in several other phenomena in higher plants (e.g. photosynthesis, respiration, gravity sensing, RNA editing), this review article will contribute to research in plant reproductive biology as well as other general biology.
In summary, sexual reproduction has been an unexplored field in plant science. Although it includes important phenomena related to agriculture (such as CMS, self-incompatibility and sex determination), molecular genetic studies of these phenomena have been done as specified independent research without taking an entire overview of plant reproduction. Because recent advanced technology enables us to perform comprehensive analyses of gene regulation, there now is a chance to take steps forward to understand all of the complex mechanisms of sexual plant reproduction. The knowledge contained in this special issue will contribute to opening up new fields of understanding of the reproductive process in higher plants.
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