A co-expression network in hexaploid wheat reveals mostly balanced expression and lack of significant gene loss of homeologous meiotic genes upon polyploidization

Abstract

14Polyploidization has played an important role in plant evolution. However, upon polyploidization the 15 process of meiosis must adapt to ensure the proper segregation of increased numbers of chromosomes 16 to produce balanced gametes. It has been suggested that meiotic gene (MG) duplicates return to a 17 single copy following whole genome duplication to stabilise the polyploid genome. Therefore, upon 18 the polyploidization of wheat, a hexaploid species with three related (homeologous) genomes, the 19 stabilization process may have involved rapid changes in content and expression of MGs on 20 homeologous chromosomes (homeologs). To examine this hypothesis, sets of candidate MGs were 21 identified in wheat using co-expression network analysis and orthology informed approaches. In total, 22 130 RNA-Seq samples from a range of tissues including wheat meiotic anthers were used to define 23 co-expressed modules of genes. Three modules were significantly correlated with meiotic tissue 24 samples but not with other tissue types. These modules were enriched for GO terms related to cell 25 cycle, DNA replication and chromatin modification, and contained orthologs of known MGs. Overall 26 74.4 % of genes within these meiosis-related modules had three homeologous copies which was 27 similar to other tissue-related modules. Amongst wheat MGs identified by orthology, rather than co-28 expression, the majority (93.7 %) were either retained in hexaploid wheat at the same number of 29 copies (78.4 %) or increased in copy number (15.3%) compared to ancestral wheat species. 30 Furthermore, genes within meiosis-related modules showed more balanced expression levels between 31 homeologs than genes in non-meiosis-related modules. Taken together our results do not support 32 extensive gene loss nor changes in homeolog expression of MGs upon wheat polyploidization. The 33 construction of the MG co-expression network allowed identification of hub genes and provided key 34 targets for future studies. 35 36 Author summary 37 All flowering plants have undergone a polyploidization event(s) during their evolutionary history. One 38of the biggest challenges faced by a newly-formed polyploid is meiosis, an essential event for sexual 39 reproduction and fertility. This process must adapt to discriminate between multiple related 40 chromosomes and to ensure their proper segregation to produce fertile gametes. The meiotic 41 mechanisms responsible for the stabilisation of the extant polyploids remain poorly understood except 42 in wheat, where there is now a better understanding of these processes. It has been proposed that 43 meiotic adaptation in established polyploids could involve meiotic gene loss following the event of 44 polyploidization. To test this hypothesis in hexaploid wheat, we have computationally predicted sets 45 of hexaploid wheat meiotic genes based on expression data from different tissue types, including 46 meiotic anther tissue, and orthology informed approaches. We have calculated homeolog expression 47 patterns and numbe...

A separation-of-functionZIP4wheat mutant allows crossover between related chromosomes and is meiotically stable

“…Thus, on the polyploidisation of wheat, and despite the pre-existence of three ZIP4 copies, duplication and divergence of TaZIP4-B2 was required to promote homologous pairing-synapsis and prevent a potential 50% loss of grain number. These observations contrast with previous studies of polyploid brassicas, which exhibited more extensive chromosome rearrangements and loss of gene content upon polyploidisation [35,36] than is observed in wheat [9]. The absence of the main locus limiting homoeologous recombination in brassicas, BnaPh1 [37], reveals the importance of homoeologous CO suppression for preservation of genome stability in other polyploids.…”

“…Previous studies have revealed extensive chromosome rearrangements in some polyploids leading to changes in gene content and/or expression [3,5,6,7]. However, recent large-scale genome sequencing and RNA analysis has revealed that homoeologous (related) chromosomes of hexaploid wheat ( Triticum aestivum L.) did not exhibit extensive gene loss or expression changes following polyploidisation [8,9]. This suggests that a major factor rapidly evolved upon wheat polyploidisation to control the behaviour of its multiple genomes during meiosis, hence preserving fertility.…”

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

“…This manuscript has been released as a pre-print at (Alabdullah et al, 2019). The authors would like to acknowledge the UK biotechnology and Biological Sciences Research Council (BBSRC; ) for supporting this work.…”

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, 2020). 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 Figure 1 Diverse and heterogenous FAIR data sets are harmonized into a knowledge graph using the KnetBuilder software.…”