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Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation.

ABSTRACT: Seeds of flowering plants can be formed sexually or asexually through apomixis. Apomixis occurs in about 400 species and is of great interest for agriculture as it produces clonal offspring. It differs from sexual reproduction in three major aspects: (1) While the sexual megaspore mother cell (MMC) undergoes meiosis, the apomictic initial cell (AIC) omits or aborts meiosis (apomeiosis); (2) the unreduced egg cell of apomicts forms an embryo without fertilization (parthenogenesis); and (3) the formation of functional endosperm requires specific developmental adaptations. Currently, our knowledge about the gene regulatory programs underlying apomixis is scarce. We used the apomict Boechera gunnisoniana, a close relative of Arabidopsis thaliana, to investigate the transcriptional basis underlying apomeiosis and parthenogenesis. Here, we present the first comprehensive reference transcriptome for reproductive development in an apomict. To compare sexual and apomictic development at the cellular level, we used laser-assisted microdissection combined with microarray and RNA-Seq analyses. Conservation of enriched gene ontologies between the AIC and the MMC likely reflects functions of importance to germline initiation, illustrating the close developmental relationship of sexuality and apomixis. However, several regulatory pathways differ between sexual and apomictic germlines, including cell cycle control, hormonal pathways, epigenetic and transcriptional regulation. Enrichment of specific signal transduction pathways are a feature of the apomictic germline, as is spermidine metabolism, which is associated with somatic embryogenesis in various plants. Our study provides a comprehensive reference dataset for apomictic development and yields important new insights into the transcriptional basis underlying apomixis in relation to sexual reproduction.

SUBMITTER: Schmidt A

PROVIDER: S-EPMC4091798 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation.

Schmidt Anja A Schmid Marc W MW Klostermeier Ulrich C UC Qi Weihong W Guthörl Daniela D Sailer Christian C Waller Manuel M Rosenstiel Philip P Grossniklaus Ueli U

PLoS genetics 20140710 7

Seeds of flowering plants can be formed sexually or asexually through apomixis. Apomixis occurs in about 400 species and is of great interest for agriculture as it produces clonal offspring. It differs from sexual reproduction in three major aspects: (1) While the sexual megaspore mother cell (MMC) undergoes meiosis, the apomictic initial cell (AIC) omits or aborts meiosis (apomeiosis); (2) the unreduced egg cell of apomicts forms an embryo without fertilization (parthenogenesis); and (3) the fo ...[more]

PMID: 25010342

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Project description:Polyploidization of the plant genome affects the phenotype of individuals including their morphology, i.e. size and form. In autopolyploids, we expect mainly nucleotypic effects, from a number of monoploid genomes (i.e. chromosome sets) or genome size, seen from an increase in size or dimension of the polyploids compared with the diploids (or lower ploids). To identify nucleotypic effects, confounding effects of hybridity (observed in allopolyploids), postpolyploidization processes or environmental effects need to be considered. We morphometrically analysed five ploidy cytotypes of the sexual-apomictic species Potentilla puberula cultivated ex situ under the same experimental conditions. Sexuals are mainly tetraploid, while higher ploidy (penta- to octoploidy) is typically associated with the expression of apomixis. The cytotypes likely arose via autopolyploidization although historic involvement of another species in the origin of apomicts cannot be fully ruled out, suggested by a slight molecular differentiation among reproductive modes. We (i) revisited molecular differentiation using amplified fragment length polymorphisms and performed a morphometric analysis to test (ii) if cytotypes are morphologically differentiated from each other and (iii) if the size of individuals is related to their ploidy. Weak molecular differentiation of sexual versus apomictic individuals was confirmed. Cytotypes and reproductive modes were also morphologically poorly differentiated from each other, i.e. apomicts largely resampled the variation of the sexuals and did not exhibit a unique morphology. Overall size of individuals increased moderately but significantly with ploidy (ca. 14 % in the comparison of octo- with tetraploids). The results support an autopolyploid origin of the P. puberula apomicts and suggest a nucleotypic effect on overall plant size. We discuss taxonomic consequences of the results in the context of data on reproductive relationships among cytotypes and their ecological preferences and evolutionary origin, and conclude that cytotypes are best treated as intraspecific variants within a single species.

Project description:BackgroundPaspalum notatum Flügge is a subtropical grass native to South America, which includes sexual diploid and apomictic polyploid biotypes. In the past decade, a number of apomixis-associated genes were discovered in this species through genetic mapping and differential expression surveys. However, the scarce information on Paspalum sequences available in public databanks limited annotations and functional predictions for these candidates.ResultsWe used a long-read 454/Roche FLX+ sequencing strategy to produce robust reference transcriptome datasets from florets of sexual and apomictic Paspalum notatum genotypes and delivered a list of transcripts showing differential representation in both reproductive types. Raw data originated from floral samples collected from premeiosis to anthesis was assembled in three libraries: i) sexual (SEX), ii) apomictic (APO) and iii) global (SEX + APO). A group of physically-supported Paspalum mRNA and EST sequences matched with high level of confidence to both sexual and apomictic libraries. A preliminary trial allowed discovery of the whole set of putative alleles/paralogs corresponding to 23 previously identified apomixis-associated candidate genes. Moreover, a list of 3,732 transcripts and several co-expression and protein -protein interaction networks associated with apomixis were identified.ConclusionsThe use of the 454/Roche FLX+ transcriptome database will allow the detailed characterization of floral alleles/paralogs of apomixis candidate genes identified in prior and future work. Moreover, it was used to reveal additional candidate genes differentially represented in apomictic and sexual flowers. Gene ontology (GO) analyses of this set of transcripts indicated that the main molecular pathways altered in the apomictic genotype correspond to specific biological processes, like biotic and abiotic stress responses, growth, development, cell death and senescence. This data collection will be of interest to the plant reproduction research community and, particularly, to Paspalum breeding projects.

Dataset Information

Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation.

Publications

Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation.

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