A natural variant of COOL1 gene enhances cold tolerance for high-latitude adaptation in maize

Rong Zeng; Yiting Shi; Li Guo; Diyi Fu; Minze Li; Xiaoyan Zhang; Zhuoyang Li; Junhong Zhuang; Xiaohong Yang; Jianru Zuo; Zhizhong Gong; Feng Tian; Shuhua Yang

doi:10.1016/j.cell.2024.12.018

A natural variant of COOL1 gene enhances cold tolerance for high-latitude adaptation in maize

Cell. 2025 Jan 13:S0092-8674(24)01431-4. doi: 10.1016/j.cell.2024.12.018. Online ahead of print.

Authors

Rong Zeng¹, Yiting Shi¹, Li Guo², Diyi Fu¹, Minze Li¹, Xiaoyan Zhang¹, Zhuoyang Li¹, Junhong Zhuang¹, Xiaohong Yang², Jianru Zuo³, Zhizhong Gong¹, Feng Tian², Shuhua Yang⁴

Affiliations

¹ State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
² State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, National Maize Improvement Center, Key Laboratory of Biology and Genetic Improvement of Maize (MOA), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China.
³ State Key Laboratory of Plant Genomics and National Plant Gene Research Center, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
⁴ State Key Laboratory of Plant Environmental Resilience, Frontiers Science Center for Molecular Design Breeding, College of Biological Sciences, China Agricultural University, Beijing 100193, China. Electronic address: [email protected].

PMID: 39842436
DOI: 10.1016/j.cell.2024.12.018

Abstract

Low temperature severely limits the growth, yield, and geographical distribution of maize (Zea mays L.). How maize adapts to cold climates remains largely unclear. Here, we identify a basic helix-loop-helix (bHLH) transcription factor, COLD-RESPONSIVE OPERATION LOCUS 1 (COOL1), as a crucial regulator of maize cold tolerance through genome-wide association studies. Natural variations in the COOL1 promoter affect the binding affinity of ELONGATED HYPOCOTYL5 (HY5), a transcriptional factor repressing COOL1 transcription. COOL1, in turn, negatively regulates downstream cold-responsive genes, thereby modulating cold tolerance. Moreover, calcium-dependent protein kinase CPK17 translocates to the nucleus and stabilizes COOL1 in response to cold stress. Intriguingly, the cold-tolerant allele of COOL1 is predominantly distributed in northern high latitudes with cold climates. This study defines a previously unknown pathway by which the COOL1-centered module regulates cold tolerance for high latitudinal adaptation in maize.

Keywords: COOL1; cold tolerance; latitudinal adaptation; maize; natural variation.