Nudix hydrolase 23 post-translationally regulates carotenoid biosynthesis in plants

Author:

Rao Sombir12ORCID,Cao Hongbo13ORCID,O’Hanna Franz Joseph1ORCID,Zhou Xuesong12ORCID,Lui Andy12ORCID,Wrightstone Emalee12ORCID,Fish Tara1ORCID,Yang Yong1ORCID,Thannhauser Theodore1ORCID,Cheng Lailiang4ORCID,Dudareva Natalia567ORCID,Li Li12ORCID

Affiliation:

1. Robert W. Holley Center for Agriculture and Health, USDA-ARS, Cornell University , Ithaca, NY 14853 , USA

2. Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University , Ithaca, NY 14853 , USA

3. College of Horticulture, Hebei Agricultural University , Baoding, Hebei 071000 , China

4. Horticulture Section, School of Integrative Plant Science, Cornell University , Ithaca, NY 14853 , USA

5. Department of Biochemistry, Purdue University , West Lafayette, IN 47907-2063 , USA

6. Department of Horticulture and Landscape Architecture, Purdue University , West Lafayette, IN 47907 , USA

7. Purdue Center for Plant Biology, Purdue University , West Lafayette, IN 47907 , USA

Abstract

Abstract Carotenoids are essential for photosynthesis and photoprotection. Plants must evolve multifaceted regulatory mechanisms to control carotenoid biosynthesis. However, the regulatory mechanisms and the regulators conserved among plant species remain elusive. Phytoene synthase (PSY) catalyzes the highly regulated step of carotenogenesis and geranylgeranyl diphosphate synthase (GGPPS) acts as a hub to interact with GGPP-utilizing enzymes for the synthesis of specific downstream isoprenoids. Here, we report a function of Nudix hydrolase 23 (NUDX23), a Nudix domain-containing protein, in post-translational regulation of PSY and GGPPS for carotenoid biosynthesis. NUDX23 expresses highly in Arabidopsis (Arabidopsis thaliana) leaves. Overexpression of NUDX23 significantly increases PSY and GGPPS protein levels and carotenoid production, whereas knockout of NUDX23 dramatically reduces their abundances and carotenoid accumulation in Arabidopsis. NUDX23 regulates carotenoid biosynthesis via direct interactions with PSY and GGPPS in chloroplasts, which enhances PSY and GGPPS protein stability in a large PSY–GGPPS enzyme complex. NUDX23 was found to co-migrate with PSY and GGPPS proteins and to be required for the enzyme complex assembly. Our findings uncover a regulatory mechanism underlying carotenoid biosynthesis in plants and offer promising genetic tools for developing carotenoid-enriched food crops.

Funder

USDA National Institute of Food and Agriculture

National Natural Science Foundation of China

Publisher

Oxford University Press (OUP)

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