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SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION

An Evaluation of the Basis and Consequences of a Stay-Green Mutation in the navel negra Citrus Mutant Using Transcriptomic and Proteomic Profiling and Metabolite Analysis^1,[W]

Instituto Valenciano de Investigaciones Agrarias, Centro de Genómica, 46113 Moncada, Valencia, Spain (E.A., D.J.I., M.T., M.C.); Chemistry and Biochemistry Pigments Group, Food Biotechnology Department, Instituto de la Grasa, Consejo Superior de Investigaciones Científicas, 41012 Sevilla, Spain (M.R., M.I.M.-M.); Department of Plant Biology, Cornell University, Ithaca, New York 14853 (C.M.B.D., J.K.C.R.); and U.S. Department of Agriculture Plant, Soil, and Nutrition Laboratory, Cornell University, Ithaca, New York 14853 (T.W.T.)

A Citrus sinensis spontaneous mutant, navel negra (nan), produces fruit with an abnormal brown-colored flavedo during ripening. Analysis of pigment composition in the wild-type and nan flavedo suggested that typical ripening-related chlorophyll (Chl) degradation, but not carotenoid biosynthesis, was impaired in the mutant, identifying nan as a type C stay-green mutant. nan exhibited normal expression of Chl biosynthetic and catabolic genes and chlorophyllase activity but no accumulation of dephytylated Chl compounds during ripening, suggesting that the mutation is not related to a lesion in any of the principal enzymatic steps in Chl catabolism. Transcript profiling using a citrus microarray indicated that a citrus ortholog of a number of SGR (for STAY-GREEN) genes was expressed at substantially lower levels in nan, both prior to and during ripening. However, the pattern of catabolite accumulation and SGR sequence analysis suggested that the nan mutation is distinct from those in previously described stay-green mutants and is associated with an upstream regulatory step, rather than directly influencing a specific component of Chl catabolism. Transcriptomic and comparative proteomic profiling further indicated that the nan mutation resulted in the suppressed expression of numerous photosynthesis-related genes and in the induction of genes that are associated with oxidative stress. These data, along with metabolite analyses, suggest that nan fruit employ a number of molecular mechanisms to compensate for the elevated Chl levels and associated photooxidative stress.

² Present address: Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Manuel Talón (talon_man{at}gva.es).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.119917

^* Corresponding author; e-mail talon_man{at}gva.es.

Received March 27, 2008; accepted May 5, 2008; published May 8, 2008.