Calcium-mediated apoptosis in a plant hypersensitive disease resistance response

Alex Levine, Roger I. Pennell, Maria E. Alvarez, Robert Palmer, Chris Lamb*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

501 Scopus citations

Abstract

Background: Avirulent pathogens elicit a battery of plant defenses, often accompanied by collapse of the challenged cells. In soybean cells, sustained accumulation of H2O2 from an oxidative burst cues localized host cell death. Such hypersensitive cell death appears to be an active process, but little is known about the mechanisms underlying cellular collapse. Results: We show that H2O2 stimulates a rapid influx of Ca2+ into soybean cells, which activates a physiological cell death program resulting in the generation of large (∼50 kb) DNA fragments and cell corpse morphology - including cell shrinkage, plasma membrane blebbing and nuclear condensation - characteristic of apoptosis. In contrast, H2O2 induction of the cellular protectant gene glutathione S-transferase is Ca2+-independent. Apoptosis in soybean cells and leaf tissue was induced by avirulent Pseudomonas syringae pv. glycinea but was not observed at comparable stages of the compatible interaction with the isogenic virulent strain, which fails to elicit a hypersensitive response. Apoptosis was also observed at the onset of the hypersensitive response in Arabidopsis leaves inoculated with avirulent P. syringae pv. tomato and in tobacco cells treated with the fungal peptide cryptogein, which is involved in the induction of non-host resistance to Phytophthora cryptogea. Conclusions: These observations establish a signal function for Ca2+ downstream of the oxidative burst in the activation of a physiological cell death program in soybean cells that is similar to apoptosis in animals. That the characteristic cell corpse morphology is also induced in Arabidopsis and tobacco by different avirulence signals suggests that apoptosis may prove to be a common, but not necessarily ubiquitous, feature of incompatible plant-pathogen interactions. Emerging similarities between facets of hypersensitive disease resistance and the mammalian native immune system indicate that apoptosis is a widespread defence mechanism in eukaryotes.

Original languageAmerican English
Pages (from-to)427-437
Number of pages11
JournalCurrent Biology
Volume6
Issue number4
DOIs
StatePublished - 1996
Externally publishedYes

Bibliographical note

Funding Information:
The first two authors contributed equally to this paper. We thank Cindy Doane for preparation of the manuscript, J. Chappell, N. Keen, J. Schroeder, D. Schubert, B. Staskawicz, I. Verma and L. Yu for biological materials or reagents. This work was supported by grants to C.L. from the Samuel Roberts Noble Foundation and to R.I.P. from The Royal Society. R.I.P. is a Royal Society University Fellow. A.L. was supported in part by a fellowship from the U.S.-Israel Binational Agricultural Research and Development Fund and M.E.A. by a fellowship from CONICET, Argentina. R.P. thanks Emmanuel College, Cambridge for a travel bursary.

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