Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana

Plant Cell Physiol. 2009 Apr;50(4):719-29. doi: 10.1093/pcp/pcp035. Epub 2009 Mar 8.

Abstract

Tetrapyrroles are well-known photosensitizers. In plants, various intermediate molecules of tetrapyrrole metabolism have been reported to induce cell death in a light-dependent manner. In contrast to these reports, we found that pheophorbide a, a key intermediate of chlorophyll catabolism, causes cell death in complete darkness in a transgenic Arabidopsis plant, As-ACD1. In this plant, expression of mRNA for pheophorbide a oxygenase was suppressed by expression of Acd1 antisense RNA; thus, As-ACD1 accumulated an excessive amount of pheophorbide a when chlorophyll breakdown occurred. We observed that when senescence was induced by a continuous dark period, leaves of As-ACD1 plants became dehydrated. By measuring electrolyte leakage, we estimated that >50% of the leaf cells underwent cell death within a 5 d period of darkness. Light and electron microscopic observations indicated that the cellular structure had collapsed in a large population of cells. Partially covering a leaf with aluminum foil resulted in light-independent cell death in the covered region and induced bleaching in the uncovered regions. These results indicate that accumulation of pheophorbide a induces cell death under both darkness and illumination, but the mechanisms of cell death under these conditions may differ. We discuss the possible mechanism of light-independent cell death and the involvement of pheophorbide a in the signaling pathway for programmed cell death.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Arabidopsis / cytology*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Death*
  • Chlorophyll / analogs & derivatives*
  • Chlorophyll / metabolism
  • Darkness*
  • Gene Expression Regulation, Plant
  • Oxygenases / genetics
  • Oxygenases / metabolism
  • Plant Leaves / cytology
  • Plant Leaves / metabolism
  • Plants, Genetically Modified / cytology
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • RNA, Antisense

Substances

  • Apoptosis Regulatory Proteins
  • Arabidopsis Proteins
  • RNA, Antisense
  • Chlorophyll
  • ACD1 protein, Arabidopsis
  • Oxygenases
  • pheophorbide a