The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death

Plant J. 2002 Nov;32(4):561-72. doi: 10.1046/j.1365-313x.2002.01444.x.

Abstract

The nectrotrophic fungus Alternaria alternata f.sp. lycopersici infects tomato plants of the genotype asc/asc by utilizing a host-selective toxin, AAL-toxin, that kills the host cells by inducing programmed cell death. Asc-1 is homologous to genes found in most eukaryotes from yeast to humans, suggesting a conserved function. A yeast strain with deletions in the homologous genes LAG1 and LAC1 was functionally complemented by Asc-1, indicating that Asc-1 functions in an analogous manner to the yeast homologues. Examination of the yeast sphingolipids, which are almost absent in the lag1Deltalac1Delta mutant, showed that Asc-1 was able to restore the synthesis of sphingolipids. We therefore examined the biosynthesis of sphingolipids in tomato by labeling leaf discs with l-[3-3H]serine. In the absence of AAL-toxin, there was no detectable difference in sphingolipid labeling between leaf discs from Asc/Asc or asc/asc leaves. In the presence of pathologically significant concentrations of AAL-toxin however, asc/asc leaf discs showed severely reduced labeling of sphingolipids and increased label in dihydrosphingosine (DHS) and 3-ketodihydrosphingosine (3-KDHS). Leaf discs from Asc/Asc leaves responded to AAL-toxin treatment by incorporating label into different sphingolipid species. The effects of AAL-toxin on asc/asc leaflets could be partially blocked by the simultaneous application of AAL-toxin and myriocin. Leaf discs simultaneously treated with AAL-toxin and myriocin showed no incorporation of label into sphingolipids or long-chain bases as expected. These results indicate that the presence of Asc-1 is able to relieve an AAL-toxin-induced block on sphingolipid synthesis that would otherwise lead to programmed cell death.

MeSH terms

  • Alternaria / physiology
  • Apoptosis / drug effects*
  • Gene Deletion
  • Genes, Fungal / genetics
  • Genes, Plant / genetics*
  • Genetic Complementation Test
  • Genetic Predisposition to Disease*
  • Lycopersicon esculentum / cytology*
  • Lycopersicon esculentum / drug effects
  • Lycopersicon esculentum / genetics
  • Lycopersicon esculentum / metabolism*
  • Molecular Sequence Data
  • Molecular Structure
  • Mycotoxins / toxicity*
  • Plant Diseases / genetics*
  • Plant Diseases / microbiology
  • Plants, Genetically Modified
  • Sphingolipids / metabolism*

Substances

  • Mycotoxins
  • Sphingolipids

Associated data

  • GENBANK/AJ312131
  • GENBANK/AJ416474