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The Aegilops ventricosa 2NvS segment in bread wheat: cytology, genomics and breeding.
Theor Appl Genet. 2021 Feb; 134(2):529-542.TA

Abstract

KEY MESSAGE

The first cytological characterization of the 2NvS segment in hexaploid wheat; complete de novo assembly and annotation of 2NvS segment; 2NvS frequency is increasing 2NvS and is associated with higher yield. The Aegilops ventricosa 2NvS translocation segment has been utilized in breeding disease-resistant wheat crops since the early 1990s. This segment is known to possess several important resistance genes against multiple wheat diseases including root knot nematode, stripe rust, leaf rust and stem rust. More recently, this segment has been associated with resistance to wheat blast, an emerging and devastating wheat disease in South America and Asia. To date, full characterization of the segment including its size, gene content and its association with grain yield is lacking. Here, we present a complete cytological and physical characterization of this agronomically important translocation in bread wheat. We de novo assembled the 2NvS segment in two wheat varieties, 'Jagger' and 'CDC Stanley,' and delineated the segment to be approximately 33 Mb. A total of 535 high-confidence genes were annotated within the 2NvS region, with > 10% belonging to the nucleotide-binding leucine-rich repeat (NLR) gene families. Identification of groups of NLR genes that are potentially N genome-specific and expressed in specific tissues can fast-track testing of candidate genes playing roles in various disease resistances. We also show the increasing frequency of 2NvS among spring and winter wheat breeding programs over two and a half decades, and the positive impact of 2NvS on wheat grain yield based on historical datasets. The significance of the 2NvS segment in wheat breeding due to resistance to multiple diseases and a positive impact on yield highlights the importance of understanding and characterizing the wheat pan-genome for better insights into molecular breeding for wheat improvement.

Authors+Show Affiliations

Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), El Batan, 56237, Texcoco, CP, Mexico.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Department of Agronomy, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Plant Genome and Systems Biology (PGSB), Helmholtz Center Munich, Ingolstaedter Landstr. 1, 85764, Neuherberg, Germany.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA. United States Department of Agriculture Agricultural Research Service, 1701 Centre Avenue, Fort Collins, CO, 80526, USA.Department of Agronomy, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA. Programa de Cultivos de Secano, Instituto Nacional de Investigación Agropecuaria (INIA), Estación Experimental La Estanzuela, Ruta 50, km 11.5, 70006, Colonia, Uruguay.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Plant Genome and Systems Biology (PGSB), Helmholtz Center Munich, Ingolstaedter Landstr. 1, 85764, Neuherberg, Germany.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, Corrensstr. 3, 06466, Seeland, Germany.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.John Innes Centre, Computational and Systems Biology, Norwich Research Park, Norwich, NR47UH, UK.Department of Agronomy and Plant Genetics, University of Minnesota, 1991 Upper Buford Circle, 411 Borlaug Hall, Saint Paul, MN, 55108, USA.Crop Development Centre, University of Saskatchewan, Agriculture Building, 51 Campus Drive, Saskatoon, SK, S7N 5A8, Canada. Grain Research Laboratory, Canadian Grain Commission, Winnipeg, MB, Canada.Crop Development Centre, University of Saskatchewan, Agriculture Building, 51 Campus Drive, Saskatoon, SK, S7N 5A8, Canada.Global Wheat Program, International Maize and Wheat Improvement Center (CIMMYT), El Batan, 56237, Texcoco, CP, Mexico.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, Corrensstr. 3, 06466, Seeland, Germany. Center for Integrated Breeding Research (CiBreed), Georg-August-University Göttingen, 37073, Göttingen, Germany.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, Corrensstr. 3, 06466, Seeland, Germany. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, 04103, Leipzig, Germany.Department of Agronomy, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA.Department of Plant Pathology and Wheat Genetics Resource Center, Kansas State University, 1712 Claflin Road, Manhattan, KS, 66506, USA. jpoland@ksu.edu.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

33184704

Citation

Gao, Liangliang, et al. "The Aegilops Ventricosa 2NvS Segment in Bread Wheat: Cytology, Genomics and Breeding." TAG. Theoretical and Applied Genetics. Theoretische Und Angewandte Genetik, vol. 134, no. 2, 2021, pp. 529-542.
Gao L, Koo DH, Juliana P, et al. The Aegilops ventricosa 2NvS segment in bread wheat: cytology, genomics and breeding. Theor Appl Genet. 2021;134(2):529-542.
Gao, L., Koo, D. H., Juliana, P., Rife, T., Singh, D., Lemes da Silva, C., Lux, T., Dorn, K. M., Clinesmith, M., Silva, P., Wang, X., Spannagl, M., Monat, C., Friebe, B., Steuernagel, B., Muehlbauer, G. J., Walkowiak, S., Pozniak, C., Singh, R., ... Poland, J. (2021). The Aegilops ventricosa 2NvS segment in bread wheat: cytology, genomics and breeding. TAG. Theoretical and Applied Genetics. Theoretische Und Angewandte Genetik, 134(2), 529-542. https://doi.org/10.1007/s00122-020-03712-y
Gao L, et al. The Aegilops Ventricosa 2NvS Segment in Bread Wheat: Cytology, Genomics and Breeding. Theor Appl Genet. 2021;134(2):529-542. PubMed PMID: 33184704.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The Aegilops ventricosa 2NvS segment in bread wheat: cytology, genomics and breeding. AU - Gao,Liangliang, AU - Koo,Dal-Hoe, AU - Juliana,Philomin, AU - Rife,Trevor, AU - Singh,Daljit, AU - Lemes da Silva,Cristiano, AU - Lux,Thomas, AU - Dorn,Kevin M, AU - Clinesmith,Marshall, AU - Silva,Paula, AU - Wang,Xu, AU - Spannagl,Manuel, AU - Monat,Cecile, AU - Friebe,Bernd, AU - Steuernagel,Burkhard, AU - Muehlbauer,Gary J, AU - Walkowiak,Sean, AU - Pozniak,Curtis, AU - Singh,Ravi, AU - Stein,Nils, AU - Mascher,Martin, AU - Fritz,Allan, AU - Poland,Jesse, Y1 - 2020/11/12/ PY - 2020/06/22/received PY - 2020/10/17/accepted PY - 2020/11/14/pubmed PY - 2021/7/3/medline PY - 2020/11/13/entrez SP - 529 EP - 542 JF - TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik JO - Theor Appl Genet VL - 134 IS - 2 N2 - KEY MESSAGE: The first cytological characterization of the 2NvS segment in hexaploid wheat; complete de novo assembly and annotation of 2NvS segment; 2NvS frequency is increasing 2NvS and is associated with higher yield. The Aegilops ventricosa 2NvS translocation segment has been utilized in breeding disease-resistant wheat crops since the early 1990s. This segment is known to possess several important resistance genes against multiple wheat diseases including root knot nematode, stripe rust, leaf rust and stem rust. More recently, this segment has been associated with resistance to wheat blast, an emerging and devastating wheat disease in South America and Asia. To date, full characterization of the segment including its size, gene content and its association with grain yield is lacking. Here, we present a complete cytological and physical characterization of this agronomically important translocation in bread wheat. We de novo assembled the 2NvS segment in two wheat varieties, 'Jagger' and 'CDC Stanley,' and delineated the segment to be approximately 33 Mb. A total of 535 high-confidence genes were annotated within the 2NvS region, with > 10% belonging to the nucleotide-binding leucine-rich repeat (NLR) gene families. Identification of groups of NLR genes that are potentially N genome-specific and expressed in specific tissues can fast-track testing of candidate genes playing roles in various disease resistances. We also show the increasing frequency of 2NvS among spring and winter wheat breeding programs over two and a half decades, and the positive impact of 2NvS on wheat grain yield based on historical datasets. The significance of the 2NvS segment in wheat breeding due to resistance to multiple diseases and a positive impact on yield highlights the importance of understanding and characterizing the wheat pan-genome for better insights into molecular breeding for wheat improvement. SN - 1432-2242 UR - https://www.unboundmedicine.com/medline/citation/33184704/The_Aegilops_ventricosa_2NvS_segment_in_bread_wheat:_cytology_genomics_and_breeding_ L2 - https://dx.doi.org/10.1007/s00122-020-03712-y DB - PRIME DP - Unbound Medicine ER -