Genomes of Aegilops umbellulata provide new insights into unique structural variations and genetic diversity in the U-genome for wheat improvement

Authors: SINGH, JATINDER - North Dakota State University; GUDI, SANTOSH - North Dakota State University; MAUGHAN, JEFF - Brigham Young University; LIU, ZHAOHUI - North Dakota State University; Kolmer, James; Rouse, Matthew; GUPTA, RAJEEV - North Dakota State University; Chen, Xianming; LASSERRE-ZUBER, PAULINE - Inrae; RIMBERT, HELENE - Inrae; SEHGAL, SUNISH - South Dakota State University; Fiedler, Jason; CHOULET, FREDERIC - Inrae; ACEVEDO, MARICELIS - Cornell University; GILL, UPINDER - North Dakota State University; WANG, MEINAN - Washington State University

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/26/2024
Publication Date: 9/18/2024
Citation: Singh, J., Gudi, S., Maughan, P. J., Liu, Z., Kolmer, J.A., Wang, M., Chen, X., Rouse, M.N., Lasserre-Zuber, P., Rimbert, H., Sehgal, S., Fiedler, J.D., Choulet, F., Acevedo, M., Gupta, R., Gill, U. 2024. Genomes of Aegilops umbellulata provide new insights into unique structural variations and genetic diversity in the U-genome for wheat improvement. Nature Genetics. 22(12): 3505-3519. https://doi.org/10.1111/pbi.14470.
DOI: https://doi.org/10.1111/pbi.14470

Interpretive Summary: Wild grasses that are relatives of wheat, can be used to improve harvest yields in modern wheat since these plants have genes for resistance to drought, diseases and other stresses. In this study, DNA of one selection of the wild wheat relative Aegilops umbellulata (AE), was fully sequenced using an advanced technique and compared with the DNA sequences of an additional 20 selections of AE that had been previously sequenced. The sequences were assembled into seven chromosomes, that had a large majority of highly repetitive DNA. The 20 lines could be placed into three genetically different groups that are found in the Fertile Crescent region where wheat and its relatives originated from. These lines also varied for different forms of the leaf rust resistance gene Lr9. Many of the AE accessions were highly resistant to all of the current predominant leaf rust races present in the United States. In addition the accessions had resistance to important races of stem rust and stripe rust. These AE accessions can be used to improve the disease resistance of U.S. wheat cultivars. The DNA sequence information will allow wheat breeders to add these new resistance genes to the current wheat cultivars.

Technical Abstract: Aegilops spp. serve as an important reservoir for novel biotic and abiotic stress tolerance. To harness this reservoir, we have generated a platinum standard chromosome-level genome assembly of an accession “PI 554389” of Aegilops umbellulata using a combination of PacBio HiFi, Oxford nanopore, and chromosome conformation capture (Hi-C) sequencing technologies and resequenced 20 Ae. umbellulata genomes using Illumina sequencing. Our platinum standard U-genome assembled into 4.20 Gb genome spanned over seven chromosomes, rich in repetitive elements (~84%), achieving a QV of 59.54 with 98.14% completeness. The phylogenetic analysis places the U-genome with D-lineage but major and distinct rearrangements were revealed in the U-genome by the comparative genomics analysis. Unique transposable elements landscape and complex chromosomal rearrangements, most prominently in 4U and 6U chromosomes, of diploid U-genome uncovered a distinct evolutionary trajectory of Ae. umbellulata. Additionally, the resequencing of geographically and morphologically diverse Ae. umbellulata accessions revealed high genetic diversity distributed in three sub-populations. Resequencing also identified six new haplotypes for Lr9, the first leaf rust resistance gene introgressed and cloned from Ae. umbellulata. These genomics resources along with high levels of resistance in the resequenced accessions against five devastating wheat diseases presented in this study affirmed the genetic potential of Ae. umbellulata for wheat improvement.