Functional analysis of ZmG6PE reveals its role in responses to low-phosphorus stress and regulation of grain yield in maize

Hongkai Zhang; Bowen Luo; Jin Liu; Xinwu Jin; Haiying Zhang; Haixu Zhong; Binyang Li; Hongmei Hu; Yikai Wang; Asif Ali; Asad Riaz; Javed Hussain Sahito; Muhammad Zafar Iqbal; Xiao Zhang; Dan Liu; Ling Wu; Duojiang Gao; Shiqiang Gao; Shunzong Su; Shibin Gao

doi:10.3389/fpls.2023.1286699

Functional analysis of ZmG6PE reveals its role in responses to low-phosphorus stress and regulation of grain yield in maize

Front Plant Sci. 2023 Nov 9:14:1286699. doi: 10.3389/fpls.2023.1286699. eCollection 2023.

Authors

Hongkai Zhang^#^{1

2

3}, Bowen Luo^#^{1

2

3}, Jin Liu^{1

2

3}, Xinwu Jin^{1

2

3}, Haiying Zhang^{1

2

3}, Haixu Zhong^{1

2

3}, Binyang Li^{1

2

3}, Hongmei Hu^{1

2

3}, Yikai Wang^{1

2

3}, Asif Ali¹, Asad Riaz⁴, Javed Hussain Sahito^{2

5}, Muhammad Zafar Iqbal², Xiao Zhang^{1

2

3}, Dan Liu^{1

2

3}, Ling Wu^{1

2

3}, Duojiang Gao², Shiqiang Gao², Shunzong Su³, Shibin Gao^{1

2

3}

Affiliations

¹ State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, Sichuan, China.
² Maize Research Institute, Sichuan Agricultural University, Chengdu, Sichuan, China.
³ Key Laboratory of Biology and Genetic Improvement of Maize in Southwest Region, Ministry of Agriculture, Chengdu, Sichuan, China.
⁴ Centre of Excellence for Plant Success in Nature and Agriculture, The Queensland Alliance for Agriculture and Food Innovation (QAAFI), The University of Queensland, St. Lucia, Brisbane, QLD, Australia.
⁵ Key Laboratory of Wheat and Maize Crops Science, College of Agronomy, Henan Agricultural University, Zhengzhou, China.

^# Contributed equally.

Abstract

A previous metabolomic and genome-wide association analysis of maize screened a glucose-6-phosphate 1-epimerase (ZmG6PE) gene, which responds to low-phosphorus (LP) stress and regulates yield in maize's recombinant inbred lines (RILs). However, the relationship of ZmG6PE with phosphorus and yield remained elusive. This study aimed to elucidate the underlying response mechanism of the ZmG6PE gene to LP stress and its consequential impact on maize yield. The analysis indicated that ZmG6PE required the Aldose_epim conserved domain to maintain enzyme activity and localized in the nucleus and cell membrane. The zmg6pe mutants showed decreased biomass and sugar contents but had increased starch content in leaves under LP stress conditions. Combined transcriptome and metabolome analysis showed that LP stress activated plant immune regulation in response to the LP stress through carbon metabolism, amino acid metabolism, and fatty acid metabolism. Notably, LP stress significantly reduced the synthesis of glucose-1-phosphate, mannose-6-phosphate, and β-alanine-related metabolites and changed the expression of related genes. ZmG6PE regulates LP stress by mediating the expression of ZmSPX6 and ZmPHT1.13. Overall, this study revealed that ZmG6PE affected the number of grains per ear, ear thickness, and ear weight under LP stress, indicating that ZmG6PE participates in the phosphate signaling pathway and affects maize yield-related traits through balancing carbohydrates homeostasis.

Keywords: ZmG6PE; low-phosphorus stress; maize; metabonomics; transcriptomics.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was supported by the National Key Research and Development Program of China (grant no. 2021YFF1000500 and 2021YFD1200704), the Natural Science Foundation of China (grant no. 32101655), Sichuan Science and Technology Support Project (grant no. 2021YFYZ0027, 2021YFYZ0020) and the earmarked fund for China Agriculture Research System (grant no. CARS-02-09).