Misexpression of FATTY ACID ELONGATION1 in the Arabidopsis epidermis induces cell death and suggests a critical role for phospholipase A2 in this process.
Very-long-chain fatty acids (VLCFAs) are important functional components of various lipid classes, including cuticular lipids in the higher plant epidermis and lipid-derived second messengers. Here, we report the characterization of transgenic Arabidopsis thaliana plants that epidermally express FATTY ACID ELONGATION1 (FAE1), the seed-specific beta-ketoacyl-CoA synthase (KCS) catalyzing the first rate-limiting step in VLCFA biosynthesis. Misexpression of FAE1 changes the VLCFAs in different classes of lipids but surprisingly does not complement the KCS fiddlehead mutant. FAE1 misexpression plants are similar to the wild type but display an essentially glabrous phenotype, owing to the selective death of trichome cells. This cell death is accompanied by membrane damage, generation of reactive oxygen species, and callose deposition. We found that nuclei of arrested trichome cells in FAE1 misexpression plants cell-autonomously accumulate high levels of DNA damage, including double-strand breaks characteristic of lipoapoptosis. A chemical genetic screen revealed that inhibitors of KCS and phospholipase A2 (PLA2), but not inhibitors of de novo ceramide biosynthesis, rescue trichome cells from death. These results support the functional role of acyl chain length of fatty acids and PLA2 as determinants for programmed cell death, likely involving the exchange of VLCFAs between phospholipids and the acyl-CoA pool.
Reina-Pinto
José J
JJ
Max-Planck-Institut für Züchtungsforschung, 50829 Köln, Germany.
Voisin
Derry
D
Kurdyukov
Sergey
S
Faust
Andrea
A
Haslam
Richard P
RP
Michaelson
Louise V
LV
Efremova
Nadia
N
Franke
Benni
B
Schreiber
Lukas
L
Napier
Johnathan A
JA
Yephremov
Alexander
A
D000123:Acetyltransferases / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D017209:Apoptosis / Q000235:genetics / Q000502:physiology*; D017360:Arabidopsis / Q000166:cytology* / Q000254:growth & development / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000502:physiology*; D053903:DNA Breaks, Double-Stranded; D053904:DNA Breaks, Single-Stranded; D053938:DNA Fragmentation; D004260:DNA Repair / Q000235:genetics; D000081031:Fatty Acid Elongases; D018506:Gene Expression Regulation, Plant; D050356:Lipid Metabolism / Q000235:genetics; D013058:Mass Spectrometry; D008954:Models, Biological; D010641:Phenotype; D030821:Plants, Genetically Modified / Q000033:anatomy & histology / Q000254:growth & development / Q000378:metabolism; D011133:Polysaccharide-Lyases / Q000502:physiology*
D029681:Arabidopsis Proteins; D000123:Acetyltransferases; D000081031:Fatty Acid Elongases; D011133:Polysaccharide-Lyases; C513206:PLA2 protein, Arabidopsis