Pangenomic analysis identifies structural variation associated with heat tolerance in pearl millet

Haidong Yan; Min Sun; Zhongren Zhang; Yarong Jin; Ailing Zhang; Chuang Lin; Bingchao Wu; Min He; Bin Xu; Jing Wang; Peng Qin; John Pablo Mendieta; Gang Nie; Jianping Wang; Chris S Jones; Guangyan Feng; Rakesh K Srivastava; Xinquan Zhang; Aureliano Bombarely; Dan Luo; Long Jin; Yuanying Peng; Xiaoshan Wang; Yang Ji; Shilin Tian; Linkai Huang

doi:10.1038/s41588-023-01302-4

Pangenomic analysis identifies structural variation associated with heat tolerance in pearl millet

Nat Genet. 2023 Mar;55(3):507-518. doi: 10.1038/s41588-023-01302-4. Epub 2023 Mar 2.

Authors

Haidong Yan^#^{1

2

3}, Min Sun^#¹, Zhongren Zhang^#⁴, Yarong Jin^#¹, Ailing Zhang¹, Chuang Lin¹, Bingchao Wu¹, Min He⁵, Bin Xu⁶, Jing Wang⁷, Peng Qin⁸, John Pablo Mendieta³, Gang Nie¹, Jianping Wang⁹, Chris S Jones¹⁰, Guangyan Feng¹, Rakesh K Srivastava¹¹, Xinquan Zhang¹, Aureliano Bombarely¹², Dan Luo¹, Long Jin¹³, Yuanying Peng¹⁴, Xiaoshan Wang¹, Yang Ji¹⁵, Shilin Tian^{16

17}, Linkai Huang^{18

19}

Affiliations

¹ College of Grassland Science and Technology, Sichuan Agricultural University, Chengdu, China.
² School of Plant and Environmental Sciences, Virginia Tech, Blacksburg, VA, USA.
³ Department of Genetics, University of Georgia, Athens, GA, USA.
⁴ Novogene Bioinformatics Institute, Beijing, China.
⁵ State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, China.
⁶ College of Grassland Science, Nanjing Agricultural University, Nanjing, China.
⁷ Key Laboratory of Bio-Source and Environmental Conservation, School of Life Science, Sichuan University, Chengdu, China.
⁸ Rice Research Institute, Sichuan Agricultural University, Chengdu, China.
⁹ Agronomy Department, University of Florida, Gainesville, FL, USA.
¹⁰ Feed and Forage Development, International Livestock Research Institute, Nairobi, Kenya.
¹¹ International Crops Research Institute for the Semi-Arid Tropics, Hyderabad, India.
¹² Instituto de Biologia Molecular y Celular de Plantas, UPV-CSIC, Valencia, Spain.
¹³ College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, China.
¹⁴ Triticeae Research Institute, Sichuan Agricultural University, Chengdu, China.
¹⁵ Sichuan Animal Science Academy, Chengdu, China.
¹⁶ Novogene Bioinformatics Institute, Beijing, China. tianshilin@novogene.com.
¹⁷ Department of Ecology, Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan, China. tianshilin@novogene.com.
¹⁸ College of Grassland Science and Technology, Sichuan Agricultural University, Chengdu, China. huanglinkai@sicau.edu.cn.
¹⁹ State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, China. huanglinkai@sicau.edu.cn.

^# Contributed equally.

Abstract

Pearl millet is an important cereal crop worldwide and shows superior heat tolerance. Here, we developed a graph-based pan-genome by assembling ten chromosomal genomes with one existing assembly adapted to different climates worldwide and captured 424,085 genomic structural variations (SVs). Comparative genomics and transcriptomics analyses revealed the expansion of the RWP-RK transcription factor family and the involvement of endoplasmic reticulum (ER)-related genes in heat tolerance. The overexpression of one RWP-RK gene led to enhanced plant heat tolerance and transactivated ER-related genes quickly, supporting the important roles of RWP-RK transcription factors and ER system in heat tolerance. Furthermore, we found that some SVs affected the gene expression associated with heat tolerance and SVs surrounding ER-related genes shaped adaptation to heat tolerance during domestication in the population. Our study provides a comprehensive genomic resource revealing insights into heat tolerance and laying a foundation for generating more robust crops under the changing climate.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adaptation, Physiological / genetics
Gene Expression Profiling
Genomics
Pennisetum* / genetics
Thermotolerance* / genetics