Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene content in arabidopsis seeds

Sabrina Gonzalez-Jorge, Sun Hwa Ha, Maria Magallanes-Lundback, Laura Ullrich Gilliland, Ailing Zhou, Alexander E. Lipka, Yen Nhu Nguyen, Ruthie Angelovici, Haining Lin, Jason Cepela, Holly Little, C. Robin Buell, Michael A. Gore, Dean DellaPenna

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Abstract

Experimental approaches targeting carotenoid biosynthetic enzymes have successfully increased the seed β-carotene content of crops. However, linkage analysis of seed carotenoids in Arabidopsis thaliana recombinant inbred populations showed that only 21% of quantitative trait loci, including those for β-carotene, encode carotenoid biosynthetic enzymes in their intervals. Thus, numerous loci remain uncharacterized and underutilized in biofortification approaches. Linkage mapping and genome-wide association studies of Arabidopsis seed carotenoids identified CAROTENOID CLEAVAGE DIOXYGENASE4 (CCD4) as a major negative regulator of seed carotenoid content, especially β-carotene. Loss of CCD4 function did not affect carotenoid homeostasis during seed development but greatly reduced carotenoid degradation during seed desiccation, increasing β-carotene content 8.4-fold relative to the wild type. Allelic complementation of a ccd4 null mutant demonstrated that single-nucleotide polymorphisms and insertions and deletions at the locus affect dry seed carotenoid content, due at least partly to differences in CCD4 expression. CCD4 also plays a major role in carotenoid turnover during dark-induced leaf senescence, with β-carotene accumulation again most strongly affected in the ccd4 mutant. These results demonstrate that CCD4 plays a major role in β-carotene degradation in drying seeds and senescing leaves and suggest that CCD4 orthologs would be promising targets for stabilizing and increasing the level of provitamin A carotenoids in seeds of major food crops.

Original languageEnglish (US)
Pages (from-to)4812-4826
Number of pages15
JournalPlant Cell
Volume25
Issue number12
DOIs
StatePublished - Dec 1 2013

All Science Journal Classification (ASJC) codes

  • Plant Science
  • Cell Biology

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    Gonzalez-Jorge, S., Ha, S. H., Magallanes-Lundback, M., Gilliland, L. U., Zhou, A., Lipka, A. E., Nguyen, Y. N., Angelovici, R., Lin, H., Cepela, J., Little, H., Buell, C. R., Gore, M. A., & DellaPenna, D. (2013). Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene content in arabidopsis seeds. Plant Cell, 25(12), 4812-4826. https://doi.org/10.1105/tpc.113.119677