A Co-Expression Network in Hexaploid Wheat Reveals Mostly Balanced Expression and Lack of Significant Gene Loss of Homeologous Meiotic Genes Upon Polyploidization

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.

Identification and validation of reference genes for RT-qPCR normalization in wheat meiosis

“…In addition, and as far as we know, although there are some massive approaches to study meiosis using transcriptomics and proteomics in cereals like maize [44][45][46] , rice 47,48 and other plants 49 , the only massive transcriptomic study covering the whole meiosis process in wheat anthers was performed by Crismani and colleagues 23 , using the Affymetrix GeneChip Wheat Genome Array. Recent studies have examined gene expression in wheat meiotic anthers using RNA-seq 31,38 . However, these studies were restricted to early meiosis.…”

“…Our results suggest that the presence of D subgenome has a more relevant effect than the presence/ausence of Ph1 locus on the pairwise variation (V) and on the number of RGs required for calculating the optimal NF, when the somatic tissues are included in the study. This may be explained by the dominance of the D subgenome over A and B in wheat (D > A > B) 36,37 , being the most dominantly expressed but with small differences among meiotic anthers, leaves and roots in hexaploid wheat 38 .…”

MutS homologue 4 and MutS homologue 5 Maintain the Obligate Crossover in Wheat Despite Stepwise Gene Loss following Polyploidization

“…It has been fine-mapped to a novel duplicated copy of the ZMM gene ZIP4 and verified using mutants that can be exploited to introgress DNA from distantly related germplasm (Rey et al, 2017). Ph1-ZIP4 on chromosome 5B originated from chromosome 3B, and the ancestral homeologous ZIP4 copies on 3A, 3B, and 3D are still present and expressed (Griffiths et al, 2006;Alabdullah et al, 2019). Therefore, increased ZIP4 gene dosage may bias recombination toward homologous chromosomes over homeologous chromosomes.…”

KnetMiner: a comprehensive approach for supporting evidence-based gene discovery and complex trait analysis across species

“…KnetMiner is being used extensively to drive gene-trait discovery research in the publicly funded Designing Future Wheat programme ( https://designingfuturewheat.org.uk/ ), see for example (Adamski et al, 2020;Alabdullah et al, 2019;Harrington et al, 2019) . Wheat ( Triticum aestivum ) is the third most-grown cereal crop in the world after maize and rice, and has a hexaploid 15 Gb genome which is 5 times the size of the human genome (The International Wheat Genome Sequencing Consortium (IWGSC) et al, 2018) .…”