Genome-wide transcription during early wheat meiosis is independent of synapsis, ploidy level and thePh1locus

Abstract

Polyploidization is a fundamental process in plant evolution. One of the biggest challenges faced by a new polyploid is meiosis, particularly discriminating between multiple related chromosomes so that only homologous chromosomes synapse and recombine to ensure regular chromosome segregation and balanced gametes. Despite its large genome size, high DNA repetitive content and similarity between homoeologous chromosomes, hexaploid wheat completes meiosis in a shorter period than diploid species with a much smaller genome. Therefore, during wheat meiosis, mechanisms additional to the classical model based on DNA sequence homology, must facilitate more efficient homologous recognition. One such mechanism could involve exploitation of differences in chromosome structure between homologues and homoeologues at the onset of meiosis. In turn, these chromatin changes, can be expected to be linked to transcriptional gene activity. In this study, we present an extensive analysis of a large RNA-Seq data derived from six different genotypes: wheat, wheat-rye hybrids and newly synthesized octoploid triticale, both in the presence and absence of the Ph1 locus. Plant material was collected at early prophase, at the transition leptotene-zygotene, when the telomere bouquet is forming and synapsis between homologues is beginning. The six genotypes exhibit different levels of synapsis and chromatin structure at this stage; therefore, recombination and consequently segregation, are also different. Unexpectedly, our study reveals that neither synapsis, whole genome duplication nor the absence of the Ph1 locus are associated with major changes in gene expression levels during early meiotic prophase. Overall wheat transcription at this meiotic stage is therefore highly resilient to such alterations, even in the presence of major chromatin structural changes. This suggests that post-transcriptional and post-translational processes are likely to be more important. Thus, further studies will be required to reveal whether these observations are specific to wheat meiosis, and whether there are significant changes in post-transcriptional and post-translational modifications in wheat and other polyploid species associated with their polyploidisation.

SPO11.2 is essential for programmed double‐strand break formation during meiosis in bread wheat (Triticum aestivum L.)

“…In both varieties, the D copy was more expressed than the B‐copy, which was more expressed than the A copy (Figure S4b). For the A copy, using available RNA‐Seq data (Lloyd et al ., 2014; Martin et al ., 2018; Ramirez‐Gonzalez et al ., 2018), we showed that both isoforms (with alternative ATG or with exon‐2 skipping) were expressed (Figure S4c), and that the main expressed form was the one with exon‐2 skipping. All together, these results showed that both B and D copies of the SPO11‐2 gene are functional, while the A copy is altered and no longer plays its full role.…”

“…The A copy is expressed, albeit significantly less than the other two copies. These results were in accordance with RNA‐Seq data in the literature derived from Chinese Spring developing anthers (Lloyd et al ., 2014) or from ph1 mutants (Martin et al ., 2018). Thus, the A copy is normally transcribed and translated, but deletion of two nucleotides (CG in T. urartu A progenitor or CC in B and D genomes; Figure 2b) in SPO11‐2 exon‐2 sequence creates a premature stop codon.…”

“…We quantified the signal intensity of each SPO11‐2 cDNA and normalized it against housekeeping gene (Ta54227: ATPase Paolacci et al ., 2009) using Quantity One software (Bio‐Rad, Hercules, CA, USA). RNA‐Seq data were those described in Lloyd et al, (2014), Martin et al, (2018) and Ramirez‐Gonzalez et al, (2018).…”

Bread wheat TaSPO11‐1 exhibits evolutionarily conserved function in meiotic recombination across distant plant species

“…The extreme conservation of the homoeologous SPO11‐1 genes and proteins within the Triticeae tribe suggests that they are all functional and presumably under strong selection pressure with regards to their essential role in meiosis. In accordance with this, expression data showed that all three homoeologous genes are equivalently expressed during meiosis (Martin et al ., 2018).…”

Centromere Satellite Repeats Have Undergone Rapid Changes in Polyploid Wheat Subgenomes

“…For example, gain or loss and neofunctionalization or subfunctionalization of genes, as well as changes in gene expression after polyploidization, have been described in plants (Jackson and Chen, 2010). In wheat, changes in ploidy did not initially produce dramatic changes in gene expression and did not substantially alter epigenetic marks (Martín et al, 2018;Ramírez-González et al, 2018). However, asymmetric elimination of repetitive rDNA sequences and epigenetic modifications were observed in polyploid formation in wheat (Guo and Han, 2014).…”