ORHis, a Natural Variant of OR, Specifically Interacts with Plastid Division Factor ARC3 to Regulate Chromoplast Number and Carotenoid Accumulation

Tianhu Sun; Hui Yuan; Cheng Chen; Deena K Kadirjan-Kalbach; Michael Mazourek; Katherine W Osteryoung; Li Li

doi:10.1016/j.molp.2020.03.007

OR^His, a Natural Variant of OR, Specifically Interacts with Plastid Division Factor ARC3 to Regulate Chromoplast Number and Carotenoid Accumulation

Mol Plant. 2020 Jun 1;13(6):864-878. doi: 10.1016/j.molp.2020.03.007. Epub 2020 Mar 25.

Authors

Tianhu Sun¹, Hui Yuan¹, Cheng Chen², Deena K Kadirjan-Kalbach², Michael Mazourek³, Katherine W Osteryoung², Li Li⁴

Affiliations

¹ Robert W. Holley Center for Agriculture and Health, USDA-ARS, Cornell University, Ithaca, NY 14853, USA; Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA.
² Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA.
³ Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA.
⁴ Robert W. Holley Center for Agriculture and Health, USDA-ARS, Cornell University, Ithaca, NY 14853, USA; Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA. Electronic address: ll37@cornell.edu.

PMID: 32222485
DOI: 10.1016/j.molp.2020.03.007

Abstract

Chromoplasts are colored plastids that synthesize and store massive amounts of carotenoids. Chromoplast number and size define the sink strength for carotenoid accumulation in plants. However, nothing is known about the mechanisms controlling chromoplast number. Previously, a natural allele of Orange (OR), OR^His, was found to promote carotenoid accumulation by activating chromoplast differentiation and increasing carotenoid biosynthesis, but cells in orange tissues in melon fruit and cauliflower OR mutant have only one or two enlarged chromoplasts. In this study, we investigated an OR^His variant of Arabidopsis OR, genetically mimicking the melon OR^His allele, and found that it also constrains chromoplast number in Arabidopsis calli. Both in vitro and in vivo experiments demonstrate that OR^His specifically interacts with the Membrane Occupation and Recognition Nexus domain of ACCUMULATION AND REPLICATION OF CHLOROPLASTS 3 (ARC3), a crucial regulator of chloroplast division. We further showed that OR^His interferes with the interaction between ARC3 and PARALOG OF ARC6 (PARC6), another key regulator of chloroplast division, suggesting a role of OR^His in competing with PARC6 for binding to ARC3 to restrict chromoplast number. Overexpression or knockout of ARC3 in Arabidopsis OR^His plants significantly alters total carotenoid levels. Moreover, overexpression of the plastid division factor PLASTID DIVISION 1 greatly enhances carotenoid accumulation. These division factors likely alter carotenoid levels via their influence on chromoplast number and/or size. Taken together, our findings provide novel mechanistic insights into the machinery controlling chromoplast number and highlight a potential new strategy for enhancing carotenoid accumulation and nutritional value in food crops.

Keywords: ARC3; OR(His); PARC6; PDV1; carotenoid; chromoplast number; plastid division.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Arabidopsis / genetics
Arabidopsis / metabolism*
Arabidopsis Proteins / metabolism*
Carotenoids / metabolism*
Gene Expression Regulation, Plant
Genes, Plant
HSP40 Heat-Shock Proteins / metabolism*
Models, Biological
Plastids / metabolism*
Protein Binding

Substances

ARC3 protein, Arabidopsis
Arabidopsis Proteins
HSP40 Heat-Shock Proteins
ORANGE protein, Arabidopsis
PARC6 protein, Arabidopsis
Carotenoids