Zhengzhao Yang

Major crops are all survivors of domestication bottlenecks. Studies have focused on the genetic loci related to the domestication syndrome, while the contribution of ancient haplotypes remains largely unknown. Here, an ancestral genomic haploblock dissection method is developed and applied to a resequencing dataset of 386 tetraploid/hexaploid wheat accessions, generating a pan-ancestry haploblock map. Together with cytoplastic evidences, we reveal that domesticated polyploid wheat emerged from the admixture of six founder wild emmer lineages, which contributed the foundation of ancestral mosaics. The key domestication-related loci, originated over a wide geographical range, were gradually pyramided through a protracted process. Diverse stable-inheritance ancestral haplotype groups of the chromosome central zone are identified, revealing the expanding routes of wheat and the trends of modern wheat breeding. Finally, an evolution model of polyploid wheat is proposed, highlighting the key role of wild-to-crop and interploidy introgression, that increased genomic diversity following bottlenecks introduced by domestication and polyploidization.

Accurate germplasm characterization is a vital step for accelerating crop genetic improvement, which remains largely infeasible for crops such as bread wheat (Triticum aestivum L.), which has a complex genome that undergoes frequent introgression and contains many structural variations. Here, we propose a genomic strategy called ggComp, which integrates resequencing data with copy number variations and stratified single-nucleotide polymorphism densities to enable unsupervised identification of pairwise germplasm resource-based Identity-By-Descent (gIBD) blocks. The reliability of ggComp was verified in wheat cultivar Nongda5181 by dissecting parental-descent patterns represented by inherited genomic blocks. With gIBD blocks identified among 212 wheat accessions, we constructed a multi-scale genomic-based germplasm network. At the whole-genome level, the network helps to clarify pedigree relationship, demonstrate genetic flow, and identify key founder lines. At the chromosome level, we were able to trace the utilization of 1RS introgression in modern wheat breeding by hitchhiked segments. At the single block scale, the dissected germplasm-based haplotypes nicely matched with previously identified alleles of "Green Revolution" genes and can guide allele mining and dissect the trajectory of beneficial alleles in wheat breeding. Our work presents a model-based framework for precisely evaluating germplasm resources with genomic data. A database, WheatCompDB (http://wheat.cau.edu.cn/WheatCompDB/), is available for researchers to exploit the identified gIBDs with a multi-scale network.

Intracellular gene transfers (IGTs) between the nucleus and organelles, including plastids and mitochondria, constantly reshape the nuclear genome during evolution. Despite the substantial contribution of IGTs to genome variation, the dynamic trajectories of IGTs at the pangenomic level remain elusive. Here, we developed an approach, IGTminer, that maps the evolutionary trajectories of IGTs using collinearity and gene reannotation across multiple genome assemblies. We applied IGTminer to create a nuclear organellar gene (NOG) map across 67 genomes covering 15 Poaceae species, including important crops. The resulting NOGs were verified by experiments and sequencing data sets. Our analysis revealed that most NOGs were recently transferred and lineage specific and that Triticeae species tended to have more NOGs than other Poaceae species. Wheat (Triticum aestivum) had a higher retention rate of NOGs than maize (Zea mays) and rice (Oryza sativa), and the retained NOGs were likely involved in photosynthesis and translation pathways. Large numbers of NOG clusters were aggregated in hexaploid wheat during 2 rounds of polyploidization, contributing to the genetic diversity among modern wheat accessions. We implemented an interactive web server to facilitate the exploration of NOGs in Poaceae. In summary, this study provides resources and insights into the roles of IGTs in shaping interspecies and intraspecies genome variation and driving plant genome evolution.

Bread wheat (Triticum aestivum) became a globally dominant crop after incorporating the D genome from the donor species Aegilops tauschii, but the evolutionary history that shaped the D genome during this process remains to be clarified. Here, we propose a renewed evolutionary model linking Ae. tauschii and the hexaploid wheat D genome by constructing an ancestral haplotype map covering 762 Ae. tauschii and hexaploid wheat accessions. We dissected the evolutionary trajectories of Ae. tauschii lineages and reported a few independent intermediate accessions, demonstrating that low-frequency inter-sublineage gene flow had enriched the diversity of Ae. tauschii. We discovered that the D genome of hexaploid wheat was inherited from a unified ancestral template, but with a mosaic composition that was highly mixed and derived mainly from three Ae. tauschii L2 sublineages located in the Caspian coastal region. This result suggests that early agricultural activities facilitated innovations in D-genome composition and finalized the success of hexaploidization. We found that the majority (51.4%) of genetic diversity was attributed to novel mutations absent in Ae. tauschii, and we identified large Ae. tauschii introgressions from various lineages, which expanded the diversity of the wheat D genome and introduced beneficial alleles. This work sheds light on the process of wheat hexaploidization and highlights the evolutionary significance of the multi-layered genetic diversity of the bread wheat D genome.

Abstract Background The massive structural variations and frequent introgression highly contribute to the genetic diversity of wheat, while the huge and complex genome of polyploid wheat hinders efficient genotyping of abundant varieties towards accurate identification, management, and exploitation of germplasm resources. Results We develop a novel workflow that identifies 1240 high-quality large copy number variation blocks (CNVb) in wheat at the pan-genome level, demonstrating that CNVb can serve as an ideal DNA fingerprinting marker for discriminating massive varieties, with the accuracy validated by PCR assay. We then construct a digitalized genotyping CNVb map across 1599 global wheat accessions. Key CNVb markers are linked with trait-associated introgressions, such as the 1RS·1BL translocation and 2N v S translocation, and the beneficial alleles, such as the end-use quality allele Glu-D1d (Dx5 + Dy10) and the semi-dwarf r-e-z allele. Furthermore, we demonstrate that these tagged CNVb markers promote a stable and cost-effective strategy for evaluating wheat germplasm resources with ultra-low-coverage sequencing data, competing with SNP array for applications such as evaluating new varieties, efficient management of collections in gene banks, and describing wheat germplasm resources in a digitalized manner. We also develop a user-friendly interactive platform, WheatCNVb ( http://wheat.cau.edu.cn/WheatCNVb/ ), for exploring the CNVb profiles over ever-increasing wheat accessions, and also propose a QR-code-like representation of individual digital CNVb fingerprint. This platform also allows uploading new CNVb profiles for comparison with stored varieties. Conclusions The CNVb-based approach provides a low-cost and high-throughput genotyping strategy for enabling digitalized wheat germplasm management and modern breeding with precise and practical decision-making.