Meiosis transcriptome and co-expression network in hexaploid wheat

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 homologs and homoeologs 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 homologs 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. Further studies in wheat and other polyploid species will be required to reveal whether these observations are specific to wheat meiosis. The genetic mechanisms regulating meiotic progression in plants are still not fully understood. Our knowledge of the genes involved in meiosis in many crop species such as wheat is largely based on studies on model species. The latest advances of wheat genomics in particular the high-quality genome reference sequence and a developmental gene expression atlas, together with the gene expression data collected from meiotic samples have provided the prerequisite resources for building a co-expression gene network to facilitate wheat meiotic studies. We used the WGCNA package in R to build a meiotic gene co-expression network in wheat based on 130 wheat RNA-seq samples collected from a range of tissues including meiotic tissue (anthers at different meiotic stages). A set of 50,387 genes were expressed during meiosis (TPM ? 0.5 in one meiosis sample at least) and assigned to 66 modules according to their expression patterns. Three of the modules (modules 2, 28 and 41 containing 4940 genes, 544 genes and 313 genes, respectively) were significantly correlated with meiotic tissue samples (r > 0.5, FDR adjusted p < 0.001) but not with any other type of tissue. Gene Ontology (GO) term enrichment analysis showed that GO terms related to cell cycle, DNA replication, chromatin modifications and other processes occurring during meiosis were highly enriched (FDR adjusted p < 0.001) in the three modules. We also applied orthology informed approaches to evaluate the genes in the meiosis-related modules and found that wheat orthologs of meiosis genes were found in modules 2, 28 and 41. Module 2, in particular, was significantly enriched possessing 166 meiosis orthologs. The combination of co-expression network analysis in tandem with orthologue information will contribute to the discovery of new meiosis genes and greatly empowers reverse genetics approaches to validate the function of candidate genes. Ultimately this will lead to better understanding of the regulation of meiosis in wheat (and other polyploid plants) and subsequently improve wheat production. To our knowledge, this study represents the first meiotic co-expression gene network built in polyploids. Project Code: BB/J007188/1.

Data and Resources

Additional Info

Field Value
Author Martín, Azahara Carmen
Maintainer Earlham Institute
Last Updated September 3, 2019, 13:47 (UTC)
Created September 3, 2019, 13:38 (UTC)
Grassroots ID 029444b4-f523-4557-9603-f996e115ad03