Xiaoming Wang

The Green Revolution (GR) dramatically increased the yield of bread wheat (Triticum aestivum L.); however, whether and how GR reshaped the wheat root system remains largely unknown. Here, a large-scale transcriptomic and phenotypic investigation was performed on seedling roots of 406 worldwide bread wheat accessions, and this analysis revealed differences in the transcriptomes and phenotypes between landraces and modern cultivars. The GR allele Reduced height (Rht)-D1b was the main genetic factor driving this phenotypic diversity, and it conferred a significantly larger seedling root to modern cultivars by increasing cell length and root meristem size. In this case, the translational reinitiation of TaRht-D1 underlies the genetic effects of Rht-D1b. In contrast, another GR allele, Rht-B1b, has no significant effect on root-related traits, although both alleles have similar genetic effects on reducing plant height. This unexpected effect of Rht-D1b on root systems, coupled with its effect on plant height, contributes to a substantially larger root-shoot ratio in modern wheat cultivars. These findings reveal previously overlooked benefits of GR alleles in modern wheat cultivars and provide clues for their future application in enhancing the seminal root system.

Polyploidy contains multiple gene copies, known as homoeologs. Differential expression of homoeologs confers expression plasticity and facilitates the adaptation and domestication of major polyploid crops. However, how this homoeolog expression bias is produced and genetically regulated remains elusive. Here we uncover substantial variation in homoeolog expression bias among the root transcriptomes of a natural population of 406 bread wheat (Triticum aestivum ssp. aestivum) accessions collected worldwide. We develop a new model allowing us to identify 14,727 quantitative trait loci regulating the variation in homoeolog expression bias (hebQTLs), indicating that homoeolog expression bias is genetically regulated and can be predicted using genotyping data. The hebQTLs mostly regulate the expression of homoeologs in the same subgenome and downregulate expression to produce homoeolog expression bias, suggesting that intra-subgenomic rather than inter-subgenomic interactions induce homoeolog expression bias. Furthermore, we determine that hebQTL-regulated homoeologs exhibit higher genetic diversity and weaker biological functions than their counterparts. Notably, the downregulation of 38.4% of hebQTL-regulated homoeologs is compensated for by the upregulation of other homoeologs within the triad. Our findings reveal how homoeolog expression is coordinated at the genetic level and provide an avenue for leveraging homoeolog expression bias to improve polyploid crops.

Background: Differences in the relative level of expression of homoeologs, known as homoeolog expression bias, are widely observed in allopolyploids. While the evolution of homoeolog expression bias through hybridization has been characterized, on shorter timescales such as those found in crop breeding programs, the extent to which homoeolog expression bias is preserved or altered between generations remains elusive. Results: Here we use biparental mapping populations of hexaploid wheat (Triticum aestivum) with a common “Paragon” parent to explore the inheritance of homoeolog expression bias in the F₅ generation. We found that homoeolog expression bias is inherited for 26–27% of triads in both populations. Most triads conserved a similar homoeolog expression bias pattern as one or both parents. Inherited patterns were largely driven by changes in the expression of one homoeolog, allowing homoeolog expression bias in subsequent generations to match parental expression. Novel patterns of homoeolog expression bias occurred more frequently in the biparental population from a landrace × elite cross, than in the population with two elite parents. Conclusions: These results demonstrate that there is significant reprogramming and stabilization of homoeolog expression bias within a small number of generations that differs significantly based on the parental lines used in the crossing.

Summary: Differences in the relative level of expression of homoeologs, known as homoeolog expression bias (HEB), are widely observed in allopolyploids. While the evolution of homoeolog expression bias through hybridisation has been characterised, on shorter timescales the extent to which homoeolog expression bias is preserved or altered between generations remains elusive. Here we use biparental mapping populations of hexaploid wheat ( Triticum aestivum ) with a common Paragon parent to explore the inheritance of homoeolog expression bias in the F ₅ generation. We found that homoeolog expression bias is inherited for 26-27% of triads in both populations. Most triads (∼70%) conserved a similar homoeolog expression bias pattern as one or both parents. Inherited patterns were largely driven by changes in the expression of one homoeolog, allowing homoeolog expression bias in subsequent generations to match parental expression. Novel patterns of homoeolog expression bias occurred more frequently in the biparental population from a landrace x elite cross, than in the population with two elite parents. These results demonstrate that there is significant reprogramming and stabilisation of homoeolog expression bias within a small number of generations that differs significantly based on the parental lines used in the crossing.

The differential expression of homoeologous genes confers expression plasticity and facilitates the adaptation and domestication of major polyploid crops. However, how this homoeolog expression bias (HEB) is regulated remains elusive. Here, transcriptome analysis of 406 wheat ( Triticum aestivum ; AABBDD) accessions revealed great variation in HEB among accessions. We identified 14,727 QTLs regulating HEB (hebQTLs), indicating that HEB is genetically regulated and can be predicted using genotyping data. The hebQTLs only regulate the expression of homoeologs in the same subgenome and downregulate their expression to result in HEB, suggesting that intra-subgenomic rather than inter-subgenomic interactions induce HEB. Furthermore, non-hebQTL-regulated homoeologs have stronger biological functions, are under higher selection pressure and exhibit lower genetic diversity than hebQTL-regulated homoeologs and compensate for the downregulated expressions of hebQTL-regulated homoeologs. Our findings reveal how homoeolog expression is coordinated at the genetic level and provide an avenue for leveraging HEB to improve polyploid crops.

Harnessing genetic diversity in major staple crops through the development of new breeding capabilities is essential to ensure food security¹. Here we examined the genetic and phenotypic diversity of the A. E. Watkins landrace collection² of bread wheat (Triticum aestivum), a major global cereal, by whole-genome re-sequencing of 827 Watkins landraces and 208 modern cultivars and in-depth field evaluation spanning a decade. We found that modern cultivars are derived from two of the seven ancestral groups of wheat and maintain very long-range haplotype integrity. The remaining five groups represent untapped genetic sources, providing access to landrace-specific alleles and haplotypes for breeding. Linkage disequilibrium-based haplotypes and association genetics analyses link Watkins genomes to the thousands of identified high-resolution quantitative trait loci and significant marker–trait associations. Using these structured germplasm, genotyping and informatics resources, we revealed many Watkins-unique beneficial haplotypes that can confer superior traits in modern wheat. Furthermore, we assessed the phenotypic effects of 44,338 Watkins-unique haplotypes, introgressed from 143 prioritized quantitative trait loci in the context of modern cultivars, bridging the gap between landrace diversity and current breeding. This study establishes a framework for systematically utilizing genetic diversity in crop improvement to achieve sustainable food security.

Wheat (Triticum aestivum L.) is one of the most important cereal crops worldwide, and its production is challenged by global climate change and a shortage of resources. The root system plays a vital role in uptaking water and nutrients and sensing soil environmental signals, and it has great potential to improve the final yield and stress tolerance of wheat. In order to further explore the genes regulating root development, this study focused on qRS-6D, located on chromosome 6D and spanning from 462,701,391 to 465,068,943, which was significantly associated with the total root length, root volume, root surface, and root fresh weight in our previous GWAS analysis. Firstly, its genetic effects were validated using an F₆ segregating population by comparing the root-related traits of homologous lines harboring the alternative haplotypes of this QTL. Then, the number of causal genes of this QTL was narrowed down to four with a transcriptome-wide association study. Additionally, qRS-6D has been demonstrated to have genetic effects on several yield- (kernel length, kernel width, and thousand-kernel weight) and plant structure-related traits (plant height, peduncle length, total tiller number, productive tiller number, flag leaf length, and flag leaf angle). Relatively, the frequency of the favorable haplotype increased with the wheat breeding practice. This study provides a reliable genetic locus to improve root development and structure and evaluate its application potential in wheat breeding improvement.

The haplotypes selected by modern wheat breeding to improve aboveground traits enlarge the root systems of wheat seedlings.

The root system, as a fundamental organ for uptaking water and nutrients and interacting with the local environmental conditions, has been postulated to be the foundation for a second Green Revolution. However, the status of the root system during modern wheat breeding remains to be elucidated. Here, by analyzing the phenotypes of 406 wheat accessions on a large scale, we found the root systems of modern cultivars were synchronisely changed along with the above-ground traits. Furthermore, the genomic blocks with phenotypic effects on both above- and below-ground traits were observed to be enriched in the selection sweeps, highlighting that modern wheat breeding contributed to the synchronised changes. More importantly, the haplotypes selected by breeders within the selection sweeps synergistically improved both the above- and below-ground traits, suggesting that modern wheat breeding has improved the root system indirectly, which may contribute to the higher grain yields of modern wheat cultivars. Our results demonstrated that modern wheat breeding synergistically improved the above- and below-ground traits.