The maize PLASTID TERMINAL OXIDASE (PTOX) gene controls carotenoid content of kernels

Authors: NIE, YONGXIN - Shandong Agricultural University; WANG, HUI - Sichuan Agricultural University; ZHANG, GUAN - Chinese Academy Of Agricultural Sciences; DING, HAIPING - Shandong Agricultural University; HAN, BEIBEI - Chinese Academy Of Agricultural Sciences; LIU, LEI - Huazhong Agricultural University; JIAN, SHI - Sichuan Agricultural University; DU, JIYUAN - Shandong Agricultural University; LI, XINZHENG - Shandong Academy Of Agricultural Sciences; ZHAO, YAJLIE - Shandong Agricultural University; ZHANG, XIAOCONG - Chinese Academy Of Agricultural Sciences; LIU, CHANGLIN - Chinese Academy Of Agricultural Sciences; WENG, JIANFNG - Chinese Academy Of Agricultural Sciences; LI, XINHAI - Chinese Academy Of Agricultural Sciences; LI, XIAOHU - Shandong Agricultural University; ZHANG, XIANSHENG - Shandong Agricultural University; ZHAO, ZIANGYU - Shandong Agricultural University; PAN, GUANGTANG - Sichuan Agricultural University; JACKSON, DAVID - Cold Spring Harbor Laboratory; Li, Qin-Bao; Stinard, Philip; ARP, JENNIFER - Bayer Cropscience; Sachs, Martin; MOOSE, STEPHEN - University Of Illinois; Hunter, Charles; WU, QINGYU - Chinese Academy Of Agricultural Sciences; ZHANG, ZHIMING - Shandong Agricultural University

Submitted to: The Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/20/2023
Publication Date: 1/10/2024
Citation: Nie, Y., Wang, H., Zhang, G., Ding, H., Han, B., Liu, L., Jian, S., Du, J., Li, X., Zhao, Y., Zhang, X., Liu, C., Weng, J., Li, X., Li, X., Zhang, X., Zhao, Z., Pan, G., Jackson, D., Li, Q., Stinard, P.S., Arp, J., Sachs, M.M., Moose, S., Hunter III, C.T., Wu, Q., Zhang, Z. 2024. The maize PLASTID TERMINAL OXIDASE (PTOX) gene controls carotenoid content of kernels. The Plant Journal. https://doi.org/10.1111/tpj.16618.
DOI: https://doi.org/10.1111/tpj.16618

Interpretive Summary: Carotenoids, which are compounds found in many plants that represent important nutrients for human health, being important sources of antioxidants and serving as precursors for vitamin A. The breeding of grains such as maize and rice to increase their nutritional value has received much attention for its potential to improve human health because much of the world suffers from vitamin A deficiency. Carotenoid biosynthesis involves a multi-step process involving numerous biochemical players, including the PTOX protein. ARS researchers at the Center for Medical, Agricultural, and Veterinary Entomology, in Gainesville FL, in collaboration with scientists in Chinese labs, Cold Spring Harbor Laboratories, University of Illinois, and ARS researchers in Urbana, IL, showed that the maize PTOX plays an important role in carotenoid production. Specifically, the scientists showed that disruption of the PTOX gene led to lower amounts of carotenoids while overexpression led to higher amounts of carotenoids. Their results demonstrated that the PTOX genes are good candidates for engineering or breeding of crops containing higher carotenoid content.

Technical Abstract: Carotenoids perform a broad range of important functions in humans; therefore, carotenoid biofortification of maize (Zea mays L.), one of the most highly produced cereal crops worldwide, would have a global impact on human health. PLASTID TERMINAL OXIDASE (PTOX) genes play an important role in carotenoid metabolism; however, the possible function of PTOX in carotenoid biosynthesis in maize has not yet been explored. In this study, we identified the maize PTOX gene ZmPTOX1 by forward genetic screening. While most higher plant species possess a single copy of the PTOX gene, maize carries two tandemly duplicated copies of ZmPTOX. Characterization of Zmptox1 mutants revealed that disrupting one copy of ZmPTOX1 was enough to impair carotenoid biosynthesis, indicating that ZmPTOX1 is essential for carotenoid biosynthesis in maize kernels. Remarkably, overexpression of ZmPTOX1 significantly improved the content of carotenoids, especially ß-carotene (provitamin A), which was increased by ~3-fold, in maize kernels. Overall, our study shows that ZmPTOX1 plays a crucial role in carotenoid biosynthesis in maize kernels and suggests that fine-tuning the expression of this gene could improve the nutritional value of cereal grains.