Differential expression analysis of sexual and apomictic Boechera uncovers FAS4 as crucial for gametogenesis

Abstract

During sexual reproduction of higher plants, seed formation is initiated by double fertilization of egg and central cell. In contrast, pseudogamous apomicts form embryos asexually by parthenogenesis of the egg, but initiation of endosperm development still depends on central cell fertilization. It can be envisioned that these differences are determined during gametogenesis and specification of gametophytic cells. To deepen the understanding of the transcriptional basis underlying sexual and apomictic reproduction, we applied tissue type-specific RNA-Seq. We compared expression in reproductive tissues of different Boechera accessions at distinct developmental stages. This confirmed previous evidence for an enrichment of RNA helicases at onset of reproductive development. We further identified a small number of members of this gene family as differentially expressed in female reproductive ovule tissues harbouring mature gametophytes from apomictic and sexual accessions. This included homologs of A. thaliana FASCIATED STEM 4 (FAS4) and of ENHANCED SILENCING PHENOTYPE 3 (ESP3), which have previously been identified as potential candidates for gametogenesis and apomixis, respectively. Unlike in A. thaliana, for either of them additional homologs or copies of related genes are present in Boechera, indicating complex evolutionary histories. As the expression patterns implied potential roles of FAS4 during gametogenesis, we first studied A. thaliana lines carrying mutant alleles. Indeed, we observed defects during male and female gametogenesis and severely reduced transmission efficiencies through both parents. In conclusion, our study identifies FAS4 as crucial for plant reproduction and suggests the potential for sub-functionalization of additional homologous genes in Boechera to shape reproductive development.

The phenomenon of autonomous endosperm in sexual and apomictic plants

“…It is likely that molecular mechanisms controlling the development of all components of the seed are more complex in different natural apomicts. In pseudogamous apomicts, endosperm development depends on the fertilization of the central cell, whereas parthenogenesis appears to remain repressed in the absence of fertilization as recently shown for Boechera ( Schmidt et al , 2014 ; Kirioukhova et al , 2018 ; Binmöller et al , 2022 ). Nevertheless, the alternation of the methylation status in the central cell by the FIS-PRC2 complex is probably the clue mechanism of AE initiation, at least in sexual plants.…”