Die and let live - Programmed cell death in plants

Current Opinion in Plant Biology

Volumn 2, Issue 6, 1999, Pages 502-507

  Lam, Eric ^a   Pontier, Dominique ^a   Del Pozo, Olga ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0033485272     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(99)00026-6     Document Type: Review

References (49)

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4. Groover A., Jones A.M. Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol. 119:1999;375-384. In vitro differentiation of tracheary element (TE) was studied. The heterotrimeric G-protein activator mastoparan and a calcium ionophore were found to accelerate hormone-dependent programmed cell death. Vacuole collapse and cessation of cytoplasmic streaming preceded nuclear DNA fragmentation, suggestive of an autolytic process of programmed cell death. Interestingly, these authors found that addition of 1% (w/v) trypsin activated vacuole collapse and nuclear DNA fragmentation in a calcium-dependent manner whereas exogenous soybean trypsin inhibitor has the opposite effect of inhibiting TE differentiation. A 40 kDa secreted protease that can be inhibited with soybean trypsin inhibitor was found to correlate with TE differentiation.
5. Bethke P.C., Lonsdale J.E., Fath A., Jones R.L. Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell. 11:1999;1033-1045. This paper describes the careful microscopic analysis of gibberellic acid induced aleurone cell death with isolated protoplasts. Cell death is preceded by an abrupt loss of membrane integrity and vacuolization of cytoplasmic vesicles. Signaling by cGMP is suggested by the effects of LY83583, a guanylyl cyclase inhibitor, on DNA degradation and programmed cell death of aleurone cells. The authors concluded that gibberellic acid activated aleurone cell death is likely to occur via autolysis rather than apoptosis.
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14. Navarre D.A., Wolpert T.J. Victorin induction of an apoptotic/senescence-like response in oats. Plant J. 11:1999;237-249. Cell death induction by the host-selective fungal toxin victorin in susceptible oat leaves resulted in chromosomal laddering, similar to those previously reported for Alternaria alternate toxin and tomato. Victorin interacts with subunits of the photorespiratory enzyme glycine decarboxylase (GDC) and effectively inhibits this mitochondrial enzyme in vivo. Parallels between victorin induced cell death and senescence are drawn. An interesting phenotype is the cleavage of the 14 amino-terminal amino acid residues from the large subunit of ribulose 1,5-bisphosphate carboxylase (LSU) and its inhibition by a variety of treatments, including cysteine protease inhibitors such as E-64 and calpeptin. This work suggests the plant mitochondria may be the site where an apoptotic signal can be activated by victorin inhibition of photorespiration through the GDC. Ethylene also appears to be required for victorin induced cell death and LSU cleavage.
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19. Shah J., Kachroo P., Klessig D.F. The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell. 11:1999;191-206. The authors describe a semidominant mutant of Arabidopsis that constitutively expresses PR genes in an NPR1 independent manner. Spontaneous HR-like cell death lesions are observed and the phenotypes are SA dependent as revealed through NahG expression. This work suggests that SA is required, although not sufficient, to induce HR cell death.
20. Rate D.N., Cuenca J.V., Bowman G.R., Guttman D.S., Greenberg J.T. A gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses and cell growth. Plant Cell. 11:1999;191-206. This report documents the characterization of a new lesion mimic mutant in Arabidopsis, acd6. It is caused by a dominant mutation that activates cell death and resistance to bacterial pathogen; however, the plant is unable to respond with an HR upon challenge with an avirulent bacteria and phytoalexin synthesis is not activated. Interestingly, the phenotype of acd6 is SA dependent, as it can be reversed by NahG expression, but is partially NPR1 independent. A novel phenotype of the acd6 mutant in comparison to other previously described lesion mimics is the observation of abnormal cell growth and enlargement that is SA dependent. A model is presented whereby SA potentiates both cell death and cell growth and/or proliferation and the acd6 mutation effectively decreases the threshold of response for SA signaling to these processes.
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22. He Z.H., He D., Kohorn B.D. Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J. 14:1998;55-63. Suppression of a cell wall associated receptor kinase by antisense technology and a dominant-negative mutant resulted in heightened sensitivity to 2,2-dichloroisonicotinic acid (INA) whereas overexpression of this kinase resulted in higher tolerance for SA treatment.
23. Heo W.D., Lee S.H., Kim M.C., Kim J.C., Chung W.S., Chun H.J., Lee K.J., Park C.Y., Park H.C., Choi J.Y., Cho M.J. Involvement of specific calmodulin isoforms in salicylic acid-independent activation of plant disease resistance responses. Proc Natl Acad Sci USA. 96:1999;766-771. The expression of two isoforms encoded by SCaM4 and SCaM5 of the calmodulin gene family from soybean was found to respond to pathogen and fungal elicitors. Overexpression of these genes in transgenic tobacco resulted in the appearance of hypersensitive-response-like phenotypes including spontaneous cell death in older mature leaves, pathogen-related gene expression and broad spectrum resistance to various types of pathogens. Surprisingly, salicylic acid (SA) levels are not affected by these transgenes suggesting that they act via SA-independent pathways to induce lesions and resistance. This work provides evidence that intracellular calcium levels can play important roles in the control of cell death activation in plants via specific calmodulin isoforms that are transcriptionally regulated. Moreover, it clearly demonstrates the existence of SA-independent cell death and resistance pathways.
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28. 2. These responses were shown to be systemic and the induction of cell death can be uncoupled from disease resistance and defense markers, with sublethal levels of ROS (reactive oxygen species) inducing pathogenesis-related gene expression and resistance without concomitant cell death.
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31. Kawasaki T., Henmi K., Ono E., Hatakeyama S., Iwano M., Satoh H., Shimamoto K. The small GTP-binding protein Rac is a regulator of cell death in plants. Proc Natl Acad Sci USA. 96:1999;10922-10926. The role of the small GTP-binding protein OsRac1 was examined by expression of its constitutively active or dominant-negative mutations in transgenic rice cell cultures and plants. Expression of the transgene encoding the constitutively active mutant of OsRac1 resulted in ROS (reactive oxygen species) production and programmed cell death which correlated with TUNEL (terminal deoxynucleotidyl transferase-mediated dUTP nick end-labeling) staining. Involvement of the NADPH oxidase is suggested by inhibition of these phenotypes by diphenylene iodonium. Conversely, transgenic expression of a dominant-negative variant of OsRac1 in a rice lesion mimic mutant resulted in suppression of ROS generation and cell death induction by a rice blast fungus and calyculin A, a protein phosphatase I inhibitor. This work provides the first clear evidence for the involvement of Rac in the regulation of plant NADPH oxidase in ROS generation and cell death induction. It complements nicely the identification of multiple plant genes encoding the large subunit of the plant NADPH oxidase and suggests that analogous to the neutrophil NADPH oxidase, the plant enzyme is also regulated by Rac and phosphorylation.
32. Reichheld J.P., Vernoux T., Lardon F., Van Montagu M, Inze D. Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J. 17:1999;647-656.
33. Tamagnone L., Merida A., Stacey N., Plaskitt K., Parr A., Chang C.F., Lynn D., Dow M.J., Roberts K., Martin C. Inhibition of phenolic acid metabolism results in precocious cell death and altered cell morphology in leaves of transgenic tobacco plants. Plant Cell. 10:1998;1801-1816. An extensive study characterizing the phenotypic defects resulting from downregulation of phenolic acid metabolism in transgenic tobacco through the transgenic expression of the gene encoding the transcription factor AmMYB308. Concomitant with the decrease of phenolic compounds, abnormal development of the leaf palisade layer is correlated with premature programmed cell death as detected by TUNEL staining. This 'early senescence' phenotype could be rescued in cell cultures by supplying exogenous phenolic precursors. Interestingly, the hypersensitive response is activated much faster in these transgenic plants and this response correlated with a heightened level of lipid peroxidation. These and earlier results suggest that phenolic compounds act as important buffers against the effects of ROS (reactive oxygen species) in plants.
34. Aravind L., Dixit V.M., Koonin E.V. The domains of death: evolution of the apoptosis machinery. Trends Biochem Sci. 24:1999;47-53. A thorough and provocative review of the various types of cell death regulators that have been defined in animal systems. Interesting comparisons between molecules that are or may be involved in cell death regulation from plants, animals and prokaryotes are presented and the evolutionary implications summarized.
35. Wolf B.B., Green D.R. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem. 274:1999;20049-20052. A well-written and comprehensive summary of the state-of-the-art knowledge on the structure, function and regulation of caspases, the growing family of cysteine proteases that specializes in controlling cell death activation.
36. del Pozo O., Lam E. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol. 8:1998;1129-1132. This work showed that synthetic peptide inhibitors of animal caspases can suppress hypersensitive response (HR) cell death induced by avirulent bacteria when co-infiltrated into tobacco leaves. The induction of two HR cell death gene markers was inhibited whereas pathogenesis-related gene induction was not affected by these inhibitors, thus showing that plant-pathogen signaling remains intact and that defense gene activation can be uncoupled from cell death. Transient induction of caspase-like proteolytic activity was detected in extracts from leaf tissues during tobacco mosaic virus (TMV)-induced HR that was synchronized by temperature shift. This work constitutes the first report of caspase-like protease activities in plants and provided evidence for their participation in HR cell death activation.
37. L and Ced-9 from animal systems can delay cell death induced by ultraviolet light, paraquat and pathogen challenge. Although the mechanism responsible for these observations is unclear at present, the results suggest that these regulators may suppress one or more evolutionarily conserved cell death switches in plants.
38. Lacomme C., Santa Cruz S. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc Natl Acad Sci USA. 96:1999;7956-7961. The gene encoding the pro-apoptotic regulator Bax from mammalian systems is expressed in tobacco by a tobacco mosaic virus (TMV) viral vector and found to induce hypersensitive-response-like phenotypes such as cell death and pathogenesis-related gene expression. Mutational analyses show that the likely target site of Bax in plants is the mitochondria and that domains required for Bax dimerization are required for optimal cell death induction. This work provides evidence that plant mitochondria can be the site of origin for signals leading to hypersensitive-response-like phenomena.
39. Solomon M., Belenghi B., Delledonne M., Menachem E., Levine A. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell. 11:1999;431-444. Cell death induction in soybean cells by oxidative stress or avirulent bacterial pathogen was shown to depend on protein synthesis and multiple proteases are induced. Ectopic expression of the soybean cysteine protease inhibitor cystatin resulted in suppression of programmed cell death. This work showed that a cysteine protease or proteases that can interact with cystatin may be good candidates for activities that are required to execute the death signal upon oxidative stress and during the HR in this system.
40. Yano A., Suzuki K., Shinshi H.A. signaling pathway, independent of the oxidative burst, that leads to hypersensitive cell death in cultured tobacco cells includes a serine protease. Plant J. 18:1999;105-109.
41. Shimizu S., Narita M., Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature. 399:1999;483-487.
42. Shaham S., Shuman M.A., Herskowitz I. Death-defying yeast identify novel apoptosis genes. Cell. 92:1998;425-427.
43. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M.et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:1999;441-445. A flavoprotein that has homology to bacterial oxidoreductases was purified from mouse liver mitochondria. It is a mitochondrial protein that is released by the transition pore which can be regulated by Bcl-2. Purified apoptosis inducing factor (AIF) can induce apoptotic phenotypes in isolated nuclei as well as activate cytochrome c release from mitochondria in whole cells with subsequent caspase activation. AIF thus may function directly in inducing nuclear events as well as serving to amplify cell death signals. It may be involved in caspase-independent cell death signaling as AIF activity in microinjected cells is insensitive to the broad range inhibitor Z-VAD-fmk. (Z-Val-Ala-fluoromethylketone).
44. Okuno S., Shimizu S., Ito T., Nomura M., Hamada E., Tsujimoto Y., Matsuda H. Bcl-2 prevents caspase-independent cell death. J Biol Chem. 273:1998;34272-34277.
45. Maxwell D.P., Wang Y., McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA. 96:1999;8271-8276. Using a transgenic strategy, the level of the alternative oxidase (AOX) enzyme was increased or decreased in tobacco plants using sense or antisense transcript expression, respectively. In the absence of stress, plants deficient in AOX show detectable levels of ROS (reactive oxygen species) in their mitochondria and expression of PR-1. These plants are also hypersensitive to treatment with antimycin A (AA) - a specific inhibitor of Complex III of the oxidative electron transport chain - and rapid cell death is activated concomitant with production of dramatic levels of ROS in the mitochondria. Overexpression of AOX suppresses induction of ROS by AA treatment as well as suppressing basal levels of PR-1 expression. This work provides the first evidence that interference with electron transport in plant mitochondria can lead to significant ROS generation and this process is regulated by AOX. Furthermore, ROS generated from plant mitochondria can activate cell death and defense gene markers coordinately, analogous to that observed during the hypersensitive response.
46. Chivasa S., Carr J.P. Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. Plant Cell. 10:1998;1489-1498. Antimycin A and cyanide treatments were found to induce expression of AOX to the same level as salicylic acid (SA) and its analog 2,2-dichloroisonicotinic acid (INA) in tobacco. Cyanide treatment can reverse the effects of NahG expression by inhibiting tobacco mosaic virus (TMV) cell-to-cell movement and lesion proliferation, as well as virus replication. Interestingly, the effect of cyanide can be reversed by treatment with SHAM (salicylhydroxamic acid), an inhibitor of AOX. Treatment with SHAM alone can block SA-dependent resistance to TMV, induce PR-1 in an SA-dependent manner, but does not affect resistance to bacterial or fungal pathogens. This work provided evidence that SA-mediated cell death activation that is required for optimal virus restriction probably involves AOX. However, the effects of SHAM and cyanide on resistance may be more complex to interpret at present.
47. Hu G., Yalpani N., Briggs S.P., Johal G.S.A. porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell. 10:1998;1095-1105.
48. Molina A., Volrath S., Guyer D., Maleck K., Ryals J., Ward E. Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance. Plant J. 17:1999;667-678.
49. Simons B.H., Millenaar F.F., Mulder L., Van Loon L.C., Lambers H. Enhanced expression and activation of the alternative oxidase during infection of Arabidopsis with Pseudomonas syringae pv tomato. Plant Physiol. 120:1999;529-538. AOX (alternative oxidase) expression was found to be induced rapidly in the infected leaves by challenge with avirulent, but more slowly with virulent, bacterial pathogens in Arabidopsis. In addition, the rapid but not the slower rise in AOX is dependent on salicylic acid but independent of NPR1. Furthermore, ethylene sensing through ETR1 is absolutely required for AOX induction. This work suggests that the local induction of AOX involves ethylene production during the hypersensitive response HR and that AOX could serve as a protectant for ROS (reactive oxygen species) damage to the cells at or near the infection site.