ZmPTOX1, a plastid terminal oxidase, contributes to redox homeostasis during seed development and germination

Author:

Peng Yixuan1,Liang Zhi1,Cai Minghao1,Wang Jie1,Li Delin2,Chen Quanquan1,Du Xuemei1,Gu Riliang1ORCID,Wang Guoying2,Schnable Patrick S.3,Wang Jianhua1,Li Li14ORCID

Affiliation:

1. State Key Laboratory of Maize Bio‐Breeding, Key Laboratory of Crop Heterosis Utilization, Ministry of Education Beijing Innovation Center for Crop Seed Technology (MOA), College of Agronomy and Biotechnology, China Agricultural University Beijing 100193 P. R. China

2. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences Beijing 100081 P. R. China

3. Department of Agronomy Iowa State University 2035 Roy J. Carver Co‐Lab Ames 50011‐3650 Iowa USA

4. Sanya Institute of China Agricultural University Sanya 572025 China

Abstract

SUMMARYMaize plastid terminal oxidase1 (ZmPTOX1) plays a pivotal role in seed development by upholding redox balance within seed plastids. This study focuses on characterizing the white kernel mutant 3735 (wk3735) mutant, which yields pale‐yellow seeds characterized by heightened protein but reduced carotenoid levels, along with delayed germination compared to wild‐type (WT) seeds. We successfully cloned and identified the target gene ZmPTOX1, responsible for encoding maize PTOX—a versatile plastoquinol oxidase and redox sensor located in plastid membranes. While PTOX's established role involves regulating redox states and participating in carotenoid metabolism in Arabidopsis leaves and tomato fruits, our investigation marks the first exploration of its function in storage organs lacking a photosynthetic system. Through our research, we validated the existence of plastid‐localized ZmPTOX1, existing as a homomultimer, and established its interaction with ferredoxin‐NADP+ oxidoreductase 1 (ZmFNR1), a crucial component of the electron transport chain (ETC). This interaction contributes to the maintenance of redox equilibrium within plastids. Our findings indicate a propensity for excessive accumulation of reactive oxygen species (ROS) in wk3735 seeds. Beyond its known role in carotenoids' antioxidant properties, ZmPTOX1 also impacts ROS homeostasis owing to its oxidizing function. Altogether, our results underscore the critical involvement of ZmPTOX1 in governing seed development and germination by preserving redox balance within the seed plastids.

Funder

Beijing Municipal Natural Science Foundation

National Natural Science Foundation of China

National Key Transform Program

Publisher

Wiley

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