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

Plant Cell. 2013 May;25(5):1818-39. doi: 10.1105/tpc.113.111120. Epub 2013 May 14.

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 β-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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Biosynthetic Pathways / genetics
  • Biosynthetic Pathways / radiation effects
  • Chloroplasts / genetics
  • Chloroplasts / metabolism
  • Chloroplasts / radiation effects
  • Cyclopentanes / metabolism*
  • Electrophoresis, Polyacrylamide Gel
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Plant
  • Immunoblotting
  • Light
  • Mass Spectrometry / methods
  • Microscopy, Electron
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Mutation
  • Oxidative Stress / radiation effects
  • Oxylipins / metabolism*
  • Pigmentation / genetics
  • Pigmentation / radiation effects
  • Plant Leaves / genetics
  • Plant Leaves / metabolism
  • Plant Leaves / radiation effects
  • Protein Binding
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Proteomics / methods
  • Reverse Transcriptase Polymerase Chain Reaction
  • Thylakoids / genetics
  • Thylakoids / metabolism
  • Thylakoids / ultrastructure

Substances

  • Arabidopsis Proteins
  • Cyclopentanes
  • Multiprotein Complexes
  • Oxylipins
  • jasmonic acid
  • Protein Kinases
  • ABC1K1 protein, Arabidopsis