Multi-omics analyses reveal the crosstalk between the circadian clock and the response to herbicide application in Oryza sativa

Ke Chen; Xiao Su; Haona Yang; Yajun Peng; Lamei Wu; Zhenghong Zhao; Tao Lin; Lianyang Bai; Lifeng Wang

doi:10.3389/fpls.2023.1155258

Multi-omics analyses reveal the crosstalk between the circadian clock and the response to herbicide application in Oryza sativa

Front Plant Sci. 2023 Mar 24:14:1155258. doi: 10.3389/fpls.2023.1155258. eCollection 2023.

Authors

Ke Chen^{1

2

3}, Xiao Su⁴, Haona Yang^{1

3}, Yajun Peng^{1

3}, Lamei Wu^{1

3}, Zhenghong Zhao^{1

2

3}, Tao Lin⁴, Lianyang Bai^{1

2

3}, Lifeng Wang^{1

2

3}

Affiliations

¹ Longping Branch, College of Biology, Hunan University, Changsha, China.
² Key Laboratory of Indica Rice Genetics and Breeding in the Middle and Lower Reaches of Yangtze River Valley, Ministry of Agriculture and Rural Affairs, Hunan Rice Research Institute, Hunan Academy of Agricultural Sciences, Changsha, China.
³ Huangpu Research Institute of Longping Agricultural Science and Technology, Guangzhou, China.
⁴ State Key Laboratory of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural University, Beijing, China.

Abstract

Plants have evolved circadian clock systems that enable biological processes to occur in tandem with periodic changes in the environment. However, it is largely unknown whether crosstalk occurs between the circadian clock and the response to herbicide in rice. We identified 19 conserved rhythmic metabolites which were response to pesticide application and their metabolic abundance peaked mainly at ZT2 or ZT14-ZT18. We found a series of glyphosate, s-Metolachlor, fenclorim, metcamifen and GA3 response genes were expressed following stable circadian rhythms. In order to determine the patterns of their temporal expression, co-expression network analysis was done on 10,467 genes that were periodically expressed throughout a 24-hour period. Next, we identified 4,031 potential direct target genes of OsCCA1 in using DAP-seq data for OsCCA1. Of these, 339, 22, 53, 53 and 63 genes showed a response to glyphosate, s-Metolachlor, fenclorim, metcamifen and GA3 application, respectively. And they were mainly phased from dusk to midnight. Interestingly, we identified significant OsCCA1 binding peaks in the promoter regions of four herbicide resistance genes, including OsCYP81A12, OsCYP81E22, OsCYP76C2, and OsCYP76C4. Finally, we found that herbicide application could affects the expression of some of the central oscillator genes of the rice circadian clock. Here, we used multi-omics data to reveal the crosstalk between the circadian clock and herbicide response processes at the epigenomics, transcriptome, and metabolome levels in rice. This work will serve as a theoretical guide for identifying rhythmic herbicide targets, leading to the creation of new herbicides or the breeding of crops resistant to herbicides.

Keywords: Oryza sativa L.; RNA-seq; circadian clock; herbicides; metabolome.

Grants and funding

This research was supported by grants from the National Natural Science Foundation of China (No. 32272564 and No. 32001923), the National Key R&D Program of China (No. 2021YFD1700101), the science and Technology Innovation Program of Hunan Province (No. 2020WK2014 and No. 2020WK2023), the Training Program for Excellent Young Innovators of Changsha (kq2106079), and the China Agriculture Research System of MOF and MARA (CARS-16-E19).