Brassinosteroid-dependent phosphorylation of PHOSPHATE STARVATION RESPONSE2 reduces its DNA-binding ability in rice

Guoxia Zhang; Hongru Wang; Xiangle Ren; Yunhua Xiao; Dapu Liu; Wenjing Meng; Yahong Qiu; Bin Hu; Qingjun Xie; Chengcai Chu; Hongning Tong

doi:10.1093/plcell/koae063

Brassinosteroid-dependent phosphorylation of PHOSPHATE STARVATION RESPONSE2 reduces its DNA-binding ability in rice

Plant Cell. 2024 Feb 28:koae063. doi: 10.1093/plcell/koae063. Online ahead of print.

Authors

Guoxia Zhang^{1

2

3

4}, Hongru Wang⁵, Xiangle Ren⁶, Yunhua Xiao⁴, Dapu Liu⁷, Wenjing Meng⁷, Yahong Qiu⁴, Bin Hu^{1

2

3

4}, Qingjun Xie^{1

2

3}, Chengcai Chu^{1

2

3

4}, Hongning Tong⁷

Affiliations

¹ Guangdong Laboratory for Lingnan Modern Agriculture, and the State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, China.
² Key Laboratory for Enhancing Resource Use Efficiency of Crops in South China, Ministry of Agriculture and Rural Affairs, South China Agricultural University, Guangzhou, China.
³ Guangdong Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, China.
⁴ State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China.
⁵ Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China.
⁶ Howard Hughes Medical Institute, Program in Cellular and Molecular Medicine, Division of Hematology/Oncology, Department of Pediatrics, Boston Children's Hospital, Boston, MA USA.
⁷ State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China.

PMID: 38416876
DOI: 10.1093/plcell/koae063

Abstract

Brassinosteroids (BRs) are widely used as plant growth regulators in modern agriculture. Understanding how BRs regulate nutrient signaling is crucial for reducing fertilizer usage. Here we elucidate that the central BR signaling inhibitor GSK3/SHAGGY-LIKE KINASE2 (GSK2) interacts directly with and phosphorylates PHOSPHATE STARVATION RESPONSE2 (OsPHR2), the key regulator of phosphate (Pi) signaling, to suppress its transcription factor activity in rice (Oryza sativa). We identify a critical phosphorylation site at serine residue S269 of OsPHR2 and demonstrate that phosphorylation by GSK2 or phosphor-mimic mutation of S269 substantially impairs the DNA-binding activity of OsPHR2, and thus diminishes expression of OsPHR2-induced genes and reduces Pi levels. Like BRs, Pi starvation noticeably induces GSK2 instability. We further show that this site-specific phosphorylation event is conserved in Arabidopsis (Arabidopsis thaliana), but varies among the PHR-family members, being present only in most land plants. These results unveil a distinctive post-transcriptional regulatory mechanism in Pi signaling by which BRs promote Pi acquisition, with a potential contribution to the environmental adaptability of plants during their evolution.

Keywords: GSK2; OsPHR2; Phosphate; brassinosteroid; rice; signaling.