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United States Department of Agriculture

Agricultural Research Service

Research Project: FUNGAL RESOURCES FOR BIOLOGICAL CONTROL AND HIGH-VALUE USES

Location: Biological Integrated Pest Management Unit

Title: Loss of plastoglobule kinases ABC1K1 and ABC1K3 causes conditional degreening, modified prenyl-lipids, and recruitment of the jasmonic acid pathway

Authors
item Lundquist, Peter -
item Poliakov, Anton -
item Giacomelli, Lisa -
item Friso, Giulia -
item Appel, Mason -
item Mcquinn, Ryan -
item Krasnoff, Stuart
item Rowland, Elden -
item Ponnala, Lalit -
item Sun, Qi -
item Van Wijka, Klaas -

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: April 25, 2013
Publication Date: May 14, 2013
Citation: Lundquist, P.K., Poliakov, A., Giacomelli, L., Friso, G., Appel, M., Mcquinn, R., Krasnoff, S., Rowland, E., Ponnala, L., Sun, Q., Van Wijka, K.J. 2013. Loss of plastoglobule kinases ABC1K1 and ABC1K3 causes conditional degreening, modified prenyl-lipids, and recruitment of the jasmonic acid pathway. The Plant Cell. 25:1818-1839.

Interpretive Summary: Plastoglobules are lipid-protein particles of chloroplasts that derive from the thylakoid membrane system, which houses the photosynthetic machinery of plants. The dynamic morphology and protein composition of plastoglobules suggests contributions to proper plant function and the synthesis of molecular compounds important to human health. To unravel the nature of these contributions, we have examined the function of two plastoglobule-localized protein kinases of Arabidopsis chloroplasts. Our results indicate that these kinases are regulators of multiple metabolic pathways, potentially including vitamin A and E metabolism. Loss of either of these kinases in null mutants impairs the plant’s ability to cope with several abiotic stresses. Notably, recruitment of jasmonic acid synthesis and chlorophyll degradation to the plastoglobule are found specifically in the mutant plants under moderate light stress treatment. We conclude that the plastoglobule functions as a specialized microdomain within the thylakoid membrane system to recruit specific sets of metabolites and proteins into spatial proximity. This likely facilitates the regulation of metabolic pathways and turnover of thylakoid membrane components under stress conditions through enhanced metabolic channeling and flux. Our results support a model in which the plastoglobule serves as a crossroads of numerous metabolic pathways.

Technical Abstract: Plastoglobules (PGs) are plastid lipid-protein particles. This study examines the function of PG-localized kinases ABC1K1 and ABC1K3 in Arabidopsis thaliana. Several lines of evidence suggested that ABC1K1 and ABC1K3 form a protein complex. Null mutants for both genes (abc1k1 and abc1k3) and the double mutant (k1 k3) displayed rapid chlorosis upon high light stress. Also, k1 k3 showed a slower, but irreversible, senescence-like phenotype during moderate light stress that was phenocopied by drought and nitrogen limitation, but not cold stress. This senescence-like phenotype involved degradation of the photosystem II core and upregulation of chlorophyll degradation. The senescence-like phenotype was independent of the EXECUTER pathway that mediates genetically controlled cell death from the chloroplast and correlated with increased levels of the singlet oxygen–derived carotenoid b-cyclocitral, a retrograde plastid signal. Total PG volume increased during light stress in wild type and k1 k3 plants, but with different size distributions. Isolated PGs from k1 k3 showed a modified prenyl- lipid composition, suggesting reduced activity of PG-localized tocopherol cyclase (VTE1), and was consistent with loss of carotenoid cleavage dioxygenase 4. Plastid jasmonate biosynthesis enzymes were recruited to the k1 k3 PGs but not wild- type PGs, while pheophytinase, which is involved in chlorophyll degradation, was induced in k1 k3 and not wild-type plants and was localized to PGs. Thus, the ABC1K1/3 complex contributes to PG function in prenyl-lipid metabolism, stress response, and thylakoid remodeling.

Last Modified: 10/25/2014
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