Chromosome-length genome assemblies of six legume species provide insights into genome organization, evolution, and agronomic traits for crop improvement

Vanika Garg; Olga Dudchenko; Jinpeng Wang; Aamir W Khan; Saurabh Gupta; Parwinder Kaur; Kai Han; Rachit K Saxena; Sandip M Kale; Melanie Pham; Jigao Yu; Annapurna Chitikineni; Zhikang Zhang; Guangyi Fan; Christopher Lui; Vinodkumar Valluri; Fanbo Meng; Aditi Bhandari; Xiaochuan Liu; Tao Yang; Hua Chen; Babu Valliyodan; Manish Roorkiwal; Chengcheng Shi; Hong Bin Yang; Neva C Durand; Manish K Pandey; Guowei Li; Rutwik Barmukh; Xingjun Wang; Xiaoping Chen; Hon-Ming Lam; Huifang Jiang; Xuxiao Zong; Xuanqiang Liang; Xin Liu; Boshou Liao; Baozhu Guo; Scott Jackson; Henry T Nguyen; Weijian Zhuang; Wan Shubo; Xiyin Wang; Erez Lieberman Aiden; Jeffrey L Bennetzen; Rajeev K Varshney

doi:10.1016/j.jare.2021.10.009

Chromosome-length genome assemblies of six legume species provide insights into genome organization, evolution, and agronomic traits for crop improvement

J Adv Res. 2022 Dec:42:315-329. doi: 10.1016/j.jare.2021.10.009. Epub 2021 Nov 3.

Authors

Vanika Garg¹, Olga Dudchenko², Jinpeng Wang³, Aamir W Khan¹, Saurabh Gupta⁴, Parwinder Kaur⁵, Kai Han⁶, Rachit K Saxena¹, Sandip M Kale⁷, Melanie Pham⁸, Jigao Yu³, Annapurna Chitikineni¹, Zhikang Zhang³, Guangyi Fan⁹, Christopher Lui⁸, Vinodkumar Valluri¹, Fanbo Meng³, Aditi Bhandari¹, Xiaochuan Liu⁶, Tao Yang¹⁰, Hua Chen¹¹, Babu Valliyodan¹², Manish Roorkiwal¹, Chengcheng Shi⁶, Hong Bin Yang¹³, Neva C Durand², Manish K Pandey¹⁴, Guowei Li¹⁵, Rutwik Barmukh¹, Xingjun Wang¹⁵, Xiaoping Chen¹³, Hon-Ming Lam¹⁶, Huifang Jiang¹⁷, Xuxiao Zong¹⁰, Xuanqiang Liang¹³, Xin Liu¹⁸, Boshou Liao¹⁷, Baozhu Guo¹⁹, Scott Jackson²⁰, Henry T Nguyen²¹, Weijian Zhuang¹¹, Wan Shubo²², Xiyin Wang²³, Erez Lieberman Aiden²⁴, Jeffrey L Bennetzen²⁵, Rajeev K Varshney²⁶

Affiliations

¹ Center of Excellence in Genomics and Systems Biology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, India.
² The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA; Center for Theoretical Biological Physics, Rice University, Houston, TX, USA.
³ School of Life Sciences, North China University of Science and Technology, Tangshan, China.
⁴ Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany.
⁵ UWA School of Agriculture and Environment, University of Western Australia, Perth, Australia.
⁶ BGI-Qingdao, BGI-Shenzhen, Qingdao 266555, China.
⁷ The Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany.
⁸ The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.
⁹ BGI-Qingdao, BGI-Shenzhen, Qingdao 266555, China; BGI-Shenzhen, Shenzhen 518083, China.
¹⁰ National Key Facility for Crop Gene Resources and Genetic Improvement/Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China.
¹¹ Institute of Oil Crops, Center of Legume Oil Crop Genetics and Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, China.
¹² Department of Agriculture and Environmental Sciences, Lincoln University, Jefferson City, MO, USA.
¹³ Crops Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China.
¹⁴ Center of Excellence in Genomics and Systems Biology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, India; Shandong Peanut Research Institute, Shandong Academy of Agricultural Sciences, Qingdao, China.
¹⁵ Biotechnology Research Center, Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Shandong Academy of Agricultural Sciences, Ji'nan, China.
¹⁶ Center of Soybean Research of the State Key Laboratory of Agrobiotechnology and School of Life Sciences, The Chinese University of Hong Kong, Hong Kong.
¹⁷ Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, Oil Crops Research Institute of Chinese Academy of Agricultural Sciences, Wuhan, China.
¹⁸ BGI-Qingdao, BGI-Shenzhen, Qingdao 266555, China; BGI-Shenzhen, Shenzhen 518083, China; China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China.
¹⁹ Crop Genetics and Breeding Research Unit, USDA-ARS, Tifton, GA, USA.
²⁰ Bayer Crop Sciences, Chesterfield, MO, USA.
²¹ Division of Plant Sciences and National Center for Soybean Biotechnology, University of Missouri, Columbia, MO, USA.
²² Biotechnology Research Center, Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Shandong Academy of Agricultural Sciences, Ji'nan, China. Electronic address: [email protected].
²³ School of Life Sciences, North China University of Science and Technology, Tangshan, China. Electronic address: [email protected].
²⁴ The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA; Center for Theoretical Biological Physics, Rice University, Houston, TX, USA; UWA School of Agriculture and Environment, University of Western Australia, Perth, Australia; Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech, Pudong, China; Broad Institute of MIT and Harvard, Cambridge, MA, USA. Electronic address: [email protected].
²⁵ Department of Genetics, University of Georgia, Athens, GA, USA. Electronic address: [email protected].
²⁶ Center of Excellence in Genomics and Systems Biology, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, India; Institute of Oil Crops, Center of Legume Oil Crop Genetics and Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, China; Shandong Peanut Research Institute, Shandong Academy of Agricultural Sciences, Qingdao, China; State Agricultural Biotechnology Centre, Centre for Crop and Food Innovation, Food Futures Institute, Murdoch University, Murdoch, Western Australia, Australia; The UWA Institute of Agriculture, University of Western Australia, Perth, Australia. Electronic address: [email protected].

Abstract

Introduction: Legume crops are an important source of protein and oil for human health and in fixing atmospheric N₂ for soil enrichment. With an objective to accelerate much-needed genetic analyses and breeding applications, draft genome assemblies were generated in several legume crops; many of them are not high quality because they are mainly based on short reads. However, the superior quality of genome assembly is crucial for a detailed understanding of genomic architecture, genome evolution, and crop improvement.

Objectives: Present study was undertaken with an objective of developing improved chromosome-length genome assemblies in six different legumes followed by their systematic investigation to unravel different aspects of genome organization and legume evolution.

Methods: We employed in situ Hi-C data to improve the existing draft genomes and performed different evolutionary and comparative analyses using improved genome assemblies.

Results: We have developed chromosome-length genome assemblies in chickpea, pigeonpea, soybean, subterranean clover, and two wild progenitor species of cultivated groundnut (A. duranensis and A. ipaensis). A comprehensive comparative analysis of these genome assemblies offered improved insights into various evolutionary events that shaped the present-day legume species. We highlighted the expansion of gene families contributing to unique traits such as nodulation in legumes, gravitropism in groundnut, and oil biosynthesis in oilseed legume crops such as groundnut and soybean. As examples, we have demonstrated the utility of improved genome assemblies for enhancing the resolution of "QTL-hotspot" identification for drought tolerance in chickpea and marker-trait associations for agronomic traits in pigeonpea through genome-wide association study. Genomic resources developed in this study are publicly available through an online repository, 'Legumepedia'.

Conclusion: This study reports chromosome-length genome assemblies of six legume species and demonstrates the utility of these assemblies in crop improvement. The genomic resources developed here will have significant role in accelerating genetic improvement applications of legume crops.

Keywords: Evolution; GWAS; Legumes; Nodulation; Plant genomes; QTL.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Chromosome Mapping
Chromosomes
Cicer* / genetics
Crops, Agricultural / genetics
Fabaceae* / genetics
Genome, Plant
Genome-Wide Association Study
Glycine max / genetics
Humans
Plant Breeding

Abstract

Publication types

MeSH terms

Grants and funding