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Contributed by Diter von Wettstein, December 31, 2015 (sent for review December 13, 2015; reviewed by Klaus van Leyen and Daichang Yang)
Significance
Mammals including humans use highly specific pathways for tissue differentiation. One such pathway is operative in reticulocytes and involves the programmed destruction of the cell’s organellar complement by 15-lipoxygenase (15-LOX), which oxygenates polyunsaturated membrane fatty acids and provokes organelle leakage. As we report here, plants make use of a similar LOX pathway to degrade their chloroplasts during leaf senescence. The enzyme involved is a 13-LOX with unique positional specificity and molecular terms. Because 15-LOX and 13-LOX pathway products likewise operate in biological defense, a mechanism of cross-kingdom conservation of pathway regulation and function was uncovered for multicellular eukaryotes.
Abstract
Leaf senescence is the terminal stage in the development of perennial plants. Massive physiological changes occur that lead to the shut down of photosynthesis and a cessation of growth. Leaf senescence involves the selective destruction of the chloroplast as the site of photosynthesis. Here, we show that 13-lipoxygenase (13-LOX) accomplishes a key role in the destruction of chloroplasts in senescing plants and propose a critical role of its NH2-terminal chloroplast transit peptide. The 13-LOX enzyme identified here accumulated in the plastid envelope and catalyzed the dioxygenation of unsaturated membrane fatty acids, leading to a selective destruction of the chloroplast and the release of stromal constituents. Because 13-LOX pathway products comprise compounds involved in insect deterrence and pathogen defense (volatile aldehydes and oxylipins), a mechanism of unmolested nitrogen and carbon relocation is suggested that occurs from leaves to seeds and roots during fall.
Footnotes
- ↵1To whom correspondence may be addressed. Email: diter{at}wsu.edu or sreinbot{at}ujf-grenoble.fr.
Author contributions: A.S., D.v.W., and S. Reinbothe designed research; A.S., C.K., S. Rustgi, C.R., S.P., and S. Reinbothe performed research; A.S., C.K., S. Rustgi, C.R., S.P., and S. Reinbothe analyzed data; and A.S., C.K., S. Rustgi, D.v.W., C.R., S.P., and S. Reinbothe wrote the paper.
Reviewers: K.v.L., Harvard Medical School; and D.Y., Wuhan University.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1525747113/-/DCSupplemental.
13-LOX and leaf senescence
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