Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence

Plant Cell. 2010 May;22(5):1463-82. doi: 10.1105/tpc.110.075333. Epub 2010 May 4.

Abstract

In Arabidopsis thaliana, a family of six genes (ACBP1 to ACBP6) encodes acyl-CoA binding proteins (ACBPs). Investigations on ACBP3 reported here show its upregulation upon dark treatment and in senescing rosettes. Transgenic Arabidopsis overexpressing ACBP3 (ACBP3-OEs) displayed accelerated leaf senescence, whereas an acbp3 T-DNA insertional mutant and ACBP3 RNA interference transgenic Arabidopsis lines were delayed in dark-induced leaf senescence. Acyl-CoA and lipid profiling revealed that the overexpression of ACBP3 led to an increase in acyl-CoA and phosphatidylethanolamine (PE) levels, whereas ACBP3 downregulation reduced PE content. Moreover, significant losses in phosphatidylcholine (PC) and phosphatidylinositol, and gains in phosphatidic acid (PA), lysophospholipids, and oxylipin-containing galactolipids (arabidopsides) were evident in 3-week-old dark-treated and 6-week-old premature senescing ACBP3-OEs. Such accumulation of PA and arabidopsides (A, B, D, E, and G) resulting from lipid peroxidation in ACBP3-OEs likely promoted leaf senescence. The N-terminal signal sequence/transmembrane domain in ACBP3 was shown to be essential in ACBP3-green fluorescent protein targeting and in promoting senescence. Observations that recombinant ACBP3 binds PC, PE, and unsaturated acyl-CoAs in vitro and that ACBP3 overexpression enhances degradation of the autophagy (ATG)-related protein ATG8 and disrupts autophagosome formation suggest a role for ACBP3 as a phospholipid binding protein involved in the regulation of leaf senescence by modulating membrane phospholipid metabolism and ATG8 stability in Arabidopsis. Accelerated senescence in ACBP3-OEs is dependent on salicylic acid but not jasmonic acid signaling.

Publication types

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

MeSH terms

  • Acyl Coenzyme A / metabolism
  • Arabidopsis / cytology*
  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cellular Senescence* / drug effects
  • Cellular Senescence* / genetics
  • DNA, Bacterial / genetics
  • Darkness
  • Down-Regulation / drug effects
  • Esters / metabolism
  • Gene Expression Regulation, Plant / drug effects
  • Green Fluorescent Proteins / metabolism
  • Membrane Lipids / metabolism
  • Mutagenesis, Insertional / genetics
  • Oxidation-Reduction / drug effects
  • Phagosomes / drug effects
  • Phagosomes / metabolism
  • Phenotype
  • Phosphatidylcholines / metabolism
  • Phosphatidylethanolamines / metabolism
  • Plant Leaves / cytology*
  • Plant Leaves / drug effects
  • Plant Leaves / genetics
  • Plant Leaves / growth & development*
  • Plants, Genetically Modified
  • Protein Binding / drug effects
  • Protein Processing, Post-Translational / drug effects
  • RNA Interference / drug effects
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Recombinant Fusion Proteins / metabolism
  • Salicylic Acid / pharmacology

Substances

  • ACBP3 protein, Arabidopsis
  • Acyl Coenzyme A
  • Arabidopsis Proteins
  • Carrier Proteins
  • DNA, Bacterial
  • Esters
  • Membrane Lipids
  • Phosphatidylcholines
  • Phosphatidylethanolamines
  • RNA, Messenger
  • Recombinant Fusion Proteins
  • T-DNA
  • Green Fluorescent Proteins
  • phosphatidylethanolamine
  • Salicylic Acid

Associated data

  • RefSeq/NM_111436
  • RefSeq/NM_112443
  • RefSeq/NM_117255
  • RefSeq/NM_118556
  • RefSeq/NM_119743
  • RefSeq/NM_119745
  • RefSeq/NM_121497
  • RefSeq/NM_123957
  • RefSeq/NM_124726
  • RefSeq/NM_129765
  • RefSeq/NM_180100