Abstract
Polyploidization has played an important role in plant evolution. However, upon polyploidization, the process of meiosis must adapt to ensure the proper segregation of increased numbers of chromosomes to produce balanced gametes. It has been suggested that meiotic gene (MG) duplicates return to a single copy following whole genome duplication to stabilize the polyploid genome. Therefore, upon the polyploidization of wheat, a hexaploid species with three related (homeologous) genomes, the stabilization process may have involved rapid changes in content and expression of MGs on homeologous chromosomes (homeologs). To examine this hypothesis, sets of candidate MGs were identified in wheat using co-expression network analysis and orthology informed approaches. In total, 130 RNA-Seq samples from a range of tissues including wheat meiotic anthers were used to define co-expressed modules of genes. Three modules were significantly correlated with meiotic tissue samples but not with other tissue types. These modules were enriched for GO terms related to cell cycle, DNA replication, and chromatin modification and contained orthologs of known MGs. Overall, 74.4% of genes within these meiosis-related modules had three homeologous copies which was similar to other tissue-related modules. Amongst wheat MGs identified by orthology, rather than co-expression, the majority (93.7%) were either retained in hexaploid wheat at the same number of copies (78.4%) or increased in copy number (15.3%) compared to ancestral wheat species. Furthermore, genes within meiosis-related modules showed more balanced expression levels between homeologs than genes in non-meiosis-related modules. Taken together, our results do not support extensive gene loss nor changes in homeolog expression of MGs upon wheat polyploidization. The construction of the MG co-expression network allowed identification of hub genes and provided key targets for future studies.
Highlights
Meiosis is a specialized mode of cell division which generates haploid gametes
This involved the definition of 19,801 triads (59,403 genes), 7,565 duplets (15,130 genes), 15,109 monads, and 18,250 genes from the “others” group with various copy numbers, based on the Ensembl Plants database for the high confidence (HC) genes of hexaploid wheat (International Wheat Genome Sequencing Consortium, 2018) (IWGSC v1.1 gene annotation; Table S1)
Comparison of copy number of genes expressed in the eight different tissues showed that 70.9% of the genes expressed during meiosis belonged to triads
Summary
Meiosis is a specialized mode of cell division which generates haploid gametes. Prior to meiosis, chromosomes are replicated. Homologous chromosomes (homologs) locate each other and intimately align (synapse) along their length. Within this paired structure, chromosomes recombine and crossover before being accurately segregated (Kleckner, 1996; Mercier et al, 2015; Zickler and Kleckner, 2015). Chromosomes recombine and crossover before being accurately segregated (Kleckner, 1996; Mercier et al, 2015; Zickler and Kleckner, 2015) This complex and dynamic process is essential to maintain genome stability and integrity over sexual life cycles and to generate genome variation, which is a major evolutionary driving force (Capilla et al, 2016; Melamed-Bessudo et al, 2016). Segregation of the chromosomes to produce balanced gametes requires correct pairing, synapsis, and recombination between only true homologs, rather than any of the other highly related chromosomes (homeologs) (Ramsey and Schemske, 2002; Comai, 2005; Stenberg and Saura, 2013)
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