Abstract
Unlike sexual reproduction, apomixis encompasses a number of reproductive strategies, which permit maternal genome inheritance without genetic recombination and syngamy. The key biological features of apomixis are the circumvention of meiosis (i.e., apomeiosis), the differentiation of unreduced embryo sacs and egg cells, and their autonomous development in functional embryos through parthenogenesis, and the formation of viable endosperm either via fertilization-independent means or following fertilization with a sperm cell. Despite the importance of apomixis for breeding of crop plants and although much research has been conducted to study this process, the genetic control of apomixis is still not well understood. Hypericum perforatum is becoming an attractive model system for the study of aposporous apomixis. Here we report results from a global gene expression analysis of H. perforatum pistils collected from sexual and aposporous plant accessions for the purpose of identifying genes, biological processes and molecular functions associated with the aposporous apomixis pathway. Across two developmental stages corresponding to the expression of aposporous apomeiosis and parthenogenesis in ovules, a total of 224 and 973 unigenes were found to be significantly up- and down-regulated with a fold change ≥ 2 in at least one comparison, respectively. Differentially expressed genes were enriched for multiple gene ontology (GO) terms, including cell cycle, DNA metabolic process, and single-organism cellular process. For molecular functions, the highest scores were recorded for GO terms associated with DNA binding, DNA (cytosine-5-)-methyltransferase activity and heterocyclic compound binding. As deregulation of single components of the sexual developmental pathway is believed to be a trigger of the apomictic reproductive program, all genes involved in sporogenesis, gametogenesis and response to hormonal stimuli were analyzed in great detail. Overall, our data suggest that phenotypic expression of apospory is concomitant with the modulation of key genes involved in the sexual reproductive pathway. Furthermore, based on gene annotation and co-expression, we underline a putative role of hormones and key actors playing in the RNA-directed DNA methylation pathway in regulating the developmental changes occurring during aposporous apomixis in H. perforatum.
Highlights
Apomixis defines a number of reproductive strategies, which, unlike sexual reproduction, permit the inheritance of the maternal genome without genetic recombination and syngamy
A transcriptome analysis was performed on pistils collected from sexual and aposporous genotypes (Table 1) at flower developmental stages spanning female sporogenesis and gametogenesis, i.e., floral stages 11–14 according to Galla et al (2011)
Apomictic samples collected at the late developmental stages, corresponding to gametogenesis, could be clearly separated from the apomictic samples collected at the early developmental stages, spanning apomeiosis and the differentiation of the aposporous initials
Summary
Apomixis defines a number of reproductive strategies, which, unlike sexual reproduction, permit the inheritance of the maternal genome without genetic recombination and syngamy This strategy of asexual reproduction is documented in more than 120 angiosperm genera (Carman, 1997); no major seed crop species are apomictic, and attempts to introduce the apomixis trait into crop plants from apomictic relatives via conventional breeding schemes have been largely unsuccessful (Barcaccia and Albertini, 2013). Gametophytic apomixis occurs with the parthenogenic development of unreduced egg cells from apomeiotic embryo sacs that can originate from a nucellar somatic cell (i.e., apospory) or a megaspore mother cell with no, or modified, meiosis (i.e., diplospory) These features deviate from sexuality as the capability to develop an embryo sac is strictly restricted to the reduced functional megaspore deriving from meiosis, and failure of the meiotic programme naturally results in the abortion of the ovule. Several lines of evidence suggest that such dramatic shifts in the reproductive process could rely on spatial and/or temporal changes in the expression of sexual pathway-related genes (Grimanelli et al, 2003; Sharbel et al, 2010)
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