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

PLoS Genet. 2014 Jul 10;10(7):e1004476. doi: 10.1371/journal.pgen.1004476. eCollection 2014 Jul.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apomixis / genetics*
  • Arabidopsis / genetics*
  • Arabidopsis / growth & development
  • Cell Cycle / genetics
  • Epigenesis, Genetic
  • Gene Expression Regulation, Plant
  • Germ Cells / growth & development
  • Meiosis / genetics
  • Reproduction / genetics
  • Seeds / genetics
  • Seeds / growth & development
  • Sexual Development / genetics*
  • Transcription, Genetic*

Grants and funding

This project was supported by the University of Zürich, the Marie Curie project IDEAGENA (to AS), and grants from the “Staatssekretariat für Bildung und Forschung” in the framework of COST action FA0903 (to AS and UG) and the Swiss National Science Foundation (to UG). PR was supported by the DFG Cluster of excellence Inflammation at Interfaces (CL Nucleotide lab). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.