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review Plant Signaling & Behavior 5:12, 1568-1570; December 2010; ©2010 Landes Bioscience Two vacuole-mediated defense strategies in plants Noriyuki Hatsugai1,2 and Ikuko Hara-Nishimura1,* Graduate School of Science; Kyoto University; Sakyo-ku, Kyoto; 2Research Center for Cooperative Projects; Hokkaido University; Kita-ku, Sapporo, Japan 1 Key words: plant-pathogen interaction, vacuole, hypersensitive cell death, caspase activity, vacuolar processing enzyme, proteasome As plants lack immune cells, each cell has to defend itself against invading pathogens. Plant cells have a large central vacuole that accumulates a variety of hydrolytic enzymes and antimicrobial compounds, raising the possibility that vacuoles play a role in plant defense. However, how plants use vacuoles to protect against invading pathogens is poorly understood. Recently, we characterized two vacuole-mediated defense strategies associated with programmed cell death (PCD). In one strategy, vacuolar processing enzyme (VPE) mediated the disruption of the vacuolar membrane, resulting in the release of vacuolar contents into the cytoplasm in response to viral infection. In the other strategy, proteasome-dependent fusion of the central vacuole with the plasma membrane caused the discharge of vacuolar antibacterial protease and cell deathpromoting contents from the cell in response to bacterial infection. Intriguingly, both strategies relied on enzymes with caspase-like activities: the vacuolar membrane-collapse system required VPE, which has caspase-1-like activity and the membrane-fusion system required a proteasome that has caspase-3-like activity. Thus, plants may have evolved a cellular immune system that involves vacuolar membrane collapse to prevent the systemic spread of viral pathogens and membrane fusion to inhibit the proliferation of bacterial pathogens. Introduction Plant defense systems against pathogen invasion consist of multiple layers.1 The first line of defense involves physical barriers, such as the cuticle and cell wall, and constitutively produced antimicrobial compounds (i.e., phytoanticipins). This provides resistance against attack by a wide range of pathogens. However, some pathogens circumvent these barriers and compounds, and attempt to colonize the host tissue. Only certain host plants implement a second line of defense that inhibits pathogen proliferation and spread. This second defense system, which is enhanced by the inherited ability to recognize certain pathogens, includes the generation of reactive oxygen species and antimicrobial compounds *Correspondence to: Ikuko Hara-Nishimura; Email: [email protected] Submitted: 08/13/10; Accepted: 08/13/10 Previously published online: www.landesbioscience.com/journals/psb/article/13319 DOI: 10.4161/psb.5.12.13319 1568 (i.e., phytoalexins). Many of these induced defense responses are linked to the hypersensitive response (HR), which is accompanied by rapid and localized programmed cell death (PCD) known as hypersensitive cell death. The HR is controlled by multiple signal transduction pathways that are initiated upon recognition of a pathogen avirulence (Avr) factor by a plant resistance (R) gene product.2 Although the components of the signaling pathways that lead to hypersensitive cell death have been well-documented,1 little is known about how cell death is brought about, or whether plants share cell death mechanisms with animals. The Role of the Vacuole in Plant Defense Most mature cells from the vegetative tissues of plants have one large central vacuole that occupies up to 90% of the cell volume and has a significant impact on the physiology of the organism. The vacuole has numerous functions, including the maintenance of turgor pressure, protoplasmic homeostasis, storage of metabolic products, sequestration of xenobiotics and digestion of cytoplasmic constituents. In addition to its roles in development and metabolic adjustment, the vacuole is believed to be involved in plant defense against microbial pathogens and herbivores.3 In healthy plants, some phytoanticipins, such as cyanogenic glycosides and glucosinolates, are commonly stored in the vacuole as inactive precursors, but are readily converted into biologically active antibiotics by plant enzymes in response to pathogen infection or herbivore damage. Since the plant enzymes that activate these phytoanticipins are already present in healthy plant tissue, but are separated from their substrates by compartmentalization, these phytoanticipins can be rapidly activated without requiring the transcription of new gene products.4,5 On the other hand, pathogenesis-related (PR) proteins and phytoalexins are not present in healthy plants, but are synthesized in response to pathogen invasion and stored in vacuoles both at the site of infection and in uninfected (systemic) tissues, in preparation of secondary infection.4 How these vacuolar-sequestered compounds attack invading pathogens in the cytoplasm or intercellular space remained elusive until recently. A Vacuolar Membrane-collapse System for Plant Immunity Nicotiana plants that carry the resistance gene to tobacco mosaic virus (TMV) induce the HR in leaves infected with TMV. An Plant Signaling & BehaviorVolume 5 Issue 12 REVIEW review ultrastructural analysis and a viability assay of TMV-infected leaves showed that disruption of vacuolar membranes occurs prior to cell death.6-8 The disruption of vacuolar membranes releases the vacuolar contents, including hydrolytic enzymes, directly into the cytoplasm and leads to hypersensitive cell death, thereby preventing viral proliferation. Vacuolar membrane collapse followed by cell death is suppressed in VPE-deficient plants.6-8 This observation demonstrated that VPE is a key molecule in the immune system that is associated with vacuolar membrane collapse. VPE was originally identified as a processing enzyme that is responsible for the maturation of seed storage proteins.9 Studies indicate that VPE is responsible for the maturation or activation of vacuolar proteins in plants,10-14 and of lysosomal proteins in mouse.15 We discussed the pleiotropic functions of VPE family members in a previous review.16 VPE-mediated membranecollapse is also involved in the PCD triggered by mycotoxins. Some necrotrophic pathogens secrete toxins to kill host cells, and thereby promote their own growth.17 Fumonisin B1 (FB1), a mycotoxin produced by Fusarium moniliforme, induces PCD in host plants.18 FB1-induced cell death is completely abolished in the Arabidopsis VPE-null mutant, which lacks all four VPE genes.19 Hypersensitive cell death is a plant defense strategy against invading pathogens, whereas mycotoxin-induced host cell death is an infection strategy of necrotrophic pathogens to overcome plant defense. While these two processes appear to differ from each other, they both involve VPE-mediated vacuolar membrane collapse. A Membrane Fusion System for Plant Immunity Phytopathogenic bacteria do not enter plant host cells, but proliferate in the intracellular space. Recently, we established how vacuolar antibacterial proteases reach the intercellular space.20 In response to infection by avirulent bacterial strains of Pseudomonas syringae and prior to cell death, the large central vacuole of Arabidopsis plants fused to the plasma membrane,20 resulting in the discharge of vacuolar antibacterial protease and cell death-promoting agents from the cells. These molecules suppressed bacterial growth and caused hypersensitive cell death of the surrounding tissues. A defect in proteasome function abolished the membrane fusion associated with both disease resistance and PCD in response to the bacteria.20 The proteasome is a large protein complex that consists of three catalytic subunits (ß1, ß2 and ß5), and is responsible for the processing and degradation of intracellular proteins.21 Whereas some studies support the involvement of the ubiquitination pathway in cell death and disease resistance in plants,22,23 there is no direct evidence that the proteasome itself is involved in plant immunity. Our findings demonstrate that proteasome function is required for the activation of the immune response that is associated with vacuolar membrane fusion. Thus, the proteasome-regulated fusion of vacuolar and plasma membranes References 1. Jones JD, Dangl JL. The plant immune system. Nature 2006; 444:323-9. 2. Dangl JL, Jones JD. Plant pathogens and integrated defence responses to infection. Nature 2001; 411:826-33. www.landesbioscience.com provides plants with a mechanism for attacking intercellular bacterial pathogens. Two Types of Caspase-like Activities in Plant Cell Death Interestingly, both PCD-associated defense systems use enzymes that have activities similar to those of caspases, the executors of animal apoptosis. Accumulating evidence suggests that plant and animal PCD have features in common, including caspase-like activity.24-27 Although no caspase homologues have been identified in plants, at least eight distinct caspase-like activities have been detected in plants.24 We previously demonstrated that VPE is responsible for caspase-1-like (YVADase) activity in Nicotiana tabacum (tobacco) 6 and Arabidopsis.19 Despite having limited sequence identity, both VPE and caspase-1 share several structural properties.8 Whereas caspases are endopeptidases that have a substrate specificity for aspartic acids,28 VPE exhibits activity toward the aspartic acids of some peptide substrates,29 but was originally regarded as an asparaginyl endopeptidase.30,31 Recently, we showed that the proteasome ß1 subunit PBA1 was responsible for caspase-3-like (DEVDase) activity in Arabidopsis.20 This result is consistent with the finding that the amino acid sequence of the substrate pocket of the yeast ß1 subunit (ScPRE3),32 which cleaves a peptide bond at the C-terminal side of either glutamic acid or aspartic acid,33,34 is conserved in PBA1.20 Concluding Remarks We now have a good understanding of vacuole-mediated plant defense strategies. Plants have evolved immune systems that protect them from invading pathogens. The central vacuole triggers PCD, rather than just playing a supporting role as a provider of the proteolytic enzymes that facilitate cell death. Whereas caspase-1-like activity is conferred by VPE in plants, caspase-3-like activity is conferred by proteasome PBA1. The identification of potential substrates of both proteases in plant cells would help to unravel the molecular mechanisms underlying vacuole-mediated cell death. The plant immune response has become the focus of intense research due to predicted food and energy shortages in the near future. Acknowledgements This work was supported by PREST and CREST of the Japan Science and Technology Corporation, by Grants-in-Aid for Scientific Research (nos. 16085203, 17107002 and 21687003) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan, and by the Global Center of Excellence Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of MEXT. 3. Iglesias AFM Jr. Vacuoles and plant defense. In: Robinson ADG, Rogers JC, Eds. Vacuolar Compartments in Plants. London, UK: Sheffield Academic Press 2000; 112-32. 4. Morrissey JP, Osbourn AE. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 1999; 63:708-24. Plant Signaling & Behavior 5. Bednarek P, Osbourn A. Plant-microbe interactions: chemical diversity in plant defense. Science 2009; 324:746-8. 6. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 2004; 305:855-8. 1569 7. Hara-Nishimura I, Hatsugai N, Kuroyanagi M, Nakaune S, Nishimura M. Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 2005; 8:404-8. 8. Hatsugai N, Kuroyanagi M, Nishimura M, HaraNishimura I. A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 2006; 11:905-11. 9. Hara-Nishimura I, Inoue K, Nishimura M. A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms. FEBS Lett 1991; 294:89-93. 10. Yamada K, Shimada T, Kondo M, Nishimura M, Hara-Nishimura I. Multiple functional proteins are produced by cleaving Asn-Gln bonds of a single precursor by vacuolar processing enzyme. J Biol Chem 1999; 274:2563-70. 11. Shimada T, Yamada K, Kataoka M, Nakaune S, Koumoto Y, Kuroyanagi M, et al. Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J Biol Chem 2003; 278:32292-9. 12. Hiraiwa N, Takeuchi Y, Nishimura M, Hara-Nishimura I. A vacuolar processing enzyme in maturing and germinating seeds: Its distribution and associated changes during development. Plant Cell Physiol 1993; 34:1197-204. 13. Hara-Nishimura I, Shimada T, Hiraiwa N, Nishimura M. Vacuolar processing enzyme responsible for maturation of seed proteins. J Plant Physiol 1995; 145:632-40. 14. Hara-Nishimura I, Maeshima M. Vacuolar processing enzymes and auqaporins. In: Robinson ADG, Rogers JC, Eds. Vacuolar Compartments in Plants. London, UK: Sheffield Academic Press 2000; 20-42. 15.Shirahama-Noda K, Yamamoto A, Sugihara K, Hashimoto N, Asano M, Nishimura M, et al. Biosynthetic processing of cathepsins and lysosomal degradation are abolished in asparaginyl endopeptidase-deficient mice. J Biol Chem 2003; 278:33194-9. 1570 16. Yamada K, Shimada T, Nishimura M, Hara-Nishimura I. A VPE family supporting various vacuolar functions in plants. Physiol Plant, Special Issue 2005; 123:369-75. 17. Walton JD. Host-selective toxins: agents of compatibility. Plant Cell 1996; 8:1723-33. 18. Gilchrist DG. Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 1998; 36:393-414. 19. Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I. VPE is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J Biol Chem 2005; 280:32914-20. 20. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, et al. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 2009; 23:2496-506. 21. Smalle J, Vierstra RD. The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 2004; 55:555-90. 22. Dreher K, Callis J. Ubiquitin, hormones and biotic stress in plants. Ann Bot (Lond) 2007; 99:787-822. 23. Craig A, Ewan R, Mesmar J, Gudipati V, Sadanandom A. E3 ubiquitin ligases and plant innate immunity. J Exp Bot 2009; 60:1123-32. 24. Bonneau L, Ge Y, Drury GE, Gallois P. What happened to plant caspases? J Exp Bot 2008; 59:491-9. 25. Lam E, del Pozo O. Caspase-like protease involvement in the control of plant cell death. Plant Mol Biol 2000; 44:417-28. 26. Woltering EJ. Death proteases come alive. Trends Plant Sci 2004; 9:469-72. 27. Woltering EJ, van der Bent A, Hoeberichts FA. Do plant caspases exist? Plant Physiol 2002; 130:1764-9. 28.Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates and functions during apoptosis. Annu Rev Biochem 1999; 68:383-424. 29. Hara-Nishimura I, Kinoshita T, Hiraiwa N, Nishimura M. Vacuolar processing enzymes in protein-storage vacuoles and lytic vacuoles. J Plant Physiol 1998; 152:668-74. 30. Becker C, Shutov AD, Nong VH, Senyuk VI, Jung R, Horstmann C, et al. Purification, cDNA cloning and characterization of proteinase B, an asparagine-specific endopeptidase from germinating vetch (Vicia sativa L.) seeds. Eur J Biochem 1995; 228:456-62. 31. Hiraiwa N, Nishimura M, Hara-Nishimura I. Vacuolar processing enzyme is self-catalytically activated by sequential removal of the C-terminal and N-terminal propeptides. FEBS Lett 1999; 447:213-6. 32. Fu H, Doelling JH, Arendt CS, Hochstrasser M, Vierstra RD. Molecular organization of the 20S proteasome gene family from Arabidopsis thaliana. Genetics 1998; 149:677-92. 33. Kisselev AF, Akopian TN, Castillo V, Goldberg AL. Proteasome active sites allosterically regulate each other, suggesting a cyclical bite-chew mechanism for protein breakdown. Mol Cell 1999; 4:395-402. 34. Kisselev AF, Garcia-Calvo M, Overkleeft HS, Peterson E, Pennington MW, Ploegh HL, et al. The caspaselike sites of proteasomes, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites. J Biol Chem 2003; 278:35869-77. Plant Signaling & BehaviorVolume 5 Issue 12