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Published on July 16, 2008; 10.1104/pp.108.124933

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Received June 17, 2008
Accepted July 10, 2008

Citrus chlorophyllase dynamics at ethylene-induced fruit color-break; a study of chlorophyllase expression, post-translational processing kinetics and in-situ intracellular localization

Tamar Azoulay Shemer , Smadar Harpaz-Saad , Eduard Belausov , Nicole Lovat , Oleg Krokhin , Victor Spicer , Kenneth G. Standing , Eliezer E. Goldschmidt , and Yoram Eyal *

Institute of Plant Sciences, The Volcani Center, Agricultural Research Organization, Bet-Dagan 50250, Israel; R.H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agriculture, Food, and Environmental Quality Sciences, Hebrew University of Jerusalem, Rehovot 76100, Israel; Manitoba Centre for Proteomics and Systems Biology, University of Manitoba 799 JBRC, 715 McDermot Avenue, Winnipeg, MB, R3E 3P4, Canada

* Corresponding author; email: eyalab{at}volcani.agri.gov.il.

Fruit color-break is the visual manifestation of the developmentally-regulated transition of chloroplasts to chromoplasts during fruit ripening and often involves biosynthesis of copious amounts of carotenoids concomitant with massive breakdown of chlorophyll. Regulation of chlorophyll breakdown at different physiological and developmental stages of the plant life cycle, particularly at fruit color-break, is still not well understood. Here we present the dynamics of native chlorophyllase and chlorophyll breakdown in Citrus limon fruit during ethylene induced color-break. We show, using in-situ immunofluorescence on ethylene treated fruit peel (flavedo) tissue, that citrus chlorophyllase is located in the plastid, in contrast to recent reports suggesting cytoplasmic localization of Arabidopsis chlorophyllases. At the intra-organellar level, chlorophyllase signal was found to overlap mostly with chlorophyll fluorescence, suggesting association of most of the chlorophyllase protein with the photosynthetic membranes. Confocal microscopy analysis showed that the kinetics of chlorophyll breakdown was not uniform in the flavedo cells. Chlorophyll quantity at the cellular level was negatively correlated with plastid chlorophyllase accumulation; plastids with reduced chlorophyll content were found by in-situ immunofluorescence to contain significant levels of chlorophyllase, while plastids containing still intact chlorophyll lacked any chlorophyllase signal. Immunoblot and protein-MS analyses were used to demonstrate that citrus chlorophyllase initially accumulates as a ~35-kDa precursor, which is subsequently N-terminally processed to ~33-kDa mature forms by cleavage at either of three consecutive amino acid positions. Chlorophyllase plastid localization, expression kinetics and the negative correlation with chlorophyll levels support the central role of the enzyme in chlorophyll breakdown during citrus fruit color-break.




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