Vacuolar processing system responsible for programmed cell death in plants

2009 Fiscal Year Final Research Report

• Project/Area Number: 17107002
• Research Category: Grant-in-Aid for Scientific Research (S)
• Allocation Type: Single-year Grants
• Research Field: 植物生理・分子
• Research Institution: Kyoto University
• Principal Investigator: NISHIMURA Ikuko Kyoto University, 大学院・理学研究科, 教授 (00241232)
• Project Period (FY): 2005 – 2009
• Keywords: 液胞 / 液胞プロセシング酵素 / 植物免疫 / 過敏感細胞死 / 外環境応答

Research Abstract

Almost all plant cells have large vacuoles that contain both hydrolytic enzymes and a variety of defense proteins. We found that plants use vacuoles and vacuolar contents for programmed cell death (PCD) in two different ways: for a destructive way and for a non-destructive way. Destruction is caused by vacuolar membrane collapse followed by the release of vacuolar hydrolytic enzymes into the cytosol, resulting in rapid and direct cell death. This way is effective in the digestion of viruses, in susceptible cell death, and in developmental cell death of integuments. On the other hand, the non-destructive way involves fusion of the vacuolar and the plasma membrane, which allows vacuolar defense proteins to be discharged into the extracellular space where the bacteria proliferate. Membrane fusion, which is normally suppressed, was triggered in a proteasome-dependent manner. Intriguingly, both ways use enzymes with caspase-like activity as animal PCD : the membrane-fusion system uses proteasome subunit PBA1 with caspase-3-like activity and the vacuolar-collapse system uses VPE with caspase-1-like activity, although vacuole-mediated plant cell death differs from animal apoptotic cell death.

Research Products

• [Journal Article] Stomagen positively regulates stomatal density in Arabidopsis. (2010)
  • Author(s): Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I.
  • Journal Title: Nature(evaluated by Faculty of 1000 Biology) 463 Pages: 241-244
  • Peer Reviewed
• [Journal Article] Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. (2010)
  • Author(s): Ueda H, Yokota E, Kutsuna N, Shimada T, Tamura K, Shimmen T, Hasezawa S, Dolja VV, Hara-Nishimura I.
  • Journal Title: Proc Natl Acad Sci USA 107 Pages: 6594-6599
  • Peer Reviewed
• [Journal Article] Identification and Characterization of Nuclear Pore Complex Components in Arabidopsis thaliana. (2010)
  • Author(s): Tamura K, Fukao Y, Iwamoto M, Haraguchi T, Hara-Nishimura I.
  • Journal Title: Plant Cell(evaluated by Faculty of 1000 Biology) 22 Pages: 4084-4097
  • Peer Reviewed
• [Journal Article] A rapid and non-destructive scree screecrescrecrecrere2010) A rapid and non-destructive screfying transformed seeds of Arabidopsis thaliana. (2010)
  • Author(s): Shimada TL, Shimada T, Hara-Nishimura I.
  • Journal Title: Plant J.(evaluated by Faculty of 1000 Biology) 61 Pages: 519-528
  • Peer Reviewed
• [Journal Article] Ectopic expression of an esterase, which is a candidate for the unidentified plant cutinase, causes cuticular defects in Arabidopsis thaliana. (2010)
  • Author(s): Takahashi K, Shimada T, Kondo M, Tamai A, Mori M, Nishimura M, Hara-Nishimura I.
  • Journal Title: Plant Cell Physiol.(evaluated by Faculty of 1000 Biology) 51 Pages: 123-131
  • Peer Reviewed
• [Journal Article] Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development. (2010)
  • Author(s): Shirakawa M, Ueda H, Shimada T, Koumoto Y, Shimada TL, Kondo M, Takahashi T, Okuyama Y, Nishimura M, Hara-Nishimura I.
  • Journal Title: Plant J. 64 Pages: 926-935
  • Peer Reviewed
• [Journal Article] MAG4/Atp115 is a Golgi-localized tethering factor that mediates efficient anterograde transport in Arabidopsis. (2010)
  • Author(s): Takahashi H, Tamura K, Takagi J, Koumoto Y, Hara-Nishimura I, Shimada T.
  • Journal Title: Plant Cell Physiol. 51 Pages: 1777-1787
  • Peer Reviewed
• [Journal Article] Two vacuole-mediated defense strategies in plants. (2010)
  • Author(s): Hatsugai N, Hara-Nishimura I
  • Journal Title: Plant Sinal Behav 5 Pages: 1568-1570
  • Peer Reviewed
• [Journal Article] The cystatin M/E-cathepsin L balance is essential for tissue homeostasis in epidermis, hair follicles, and cornea. (2010)
  • Author(s): Zeeuwen PL, van Vlijmen-Willems IM, Cheng T, Rodijk-Olthuis D, Hitomi K, Hara-Nishimura I, John S, Smyth N, Reinheckel T, Hendriks WJ, Schalkwijk J.
  • Journal Title: FASEB J. 24 Pages: 3744-3755
  • Peer Reviewed
• [Journal Article] A novel membrane fusion-mediated plant immunity against bacterial pathogens. (2009)
  • Author(s): Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, Nishimura M, Hara-Nishimura I.
  • Journal Title: Genes Dev.(selected as an F1000 paper) 23 Pages: 2496-2506
  • Peer Reviewed
• [Journal Article] GNOM-LIKE1/ERMO1 and SEC24a/ERMO2 Are Required for Maintenance of Endoplasmic Reticulum Morphology in Arabidopsis thaliana. (2009)
  • Author(s): Nakano RT, Matsushima R, Ueda H, Tamura K, Shimada T, Li L, Hayashi Y, Kondo M, Nishimura M, Hara-Nishimura I.
  • Journal Title: Plant Cell 21 Pages: 3672-3685
  • Peer Reviewed
• [Journal Article] Mice lacking asparaginyl endopeptidase develop disorders resembling hemophagocytic syndrome. (2009)
  • Author(s): Chan CB, Abe M, Hashimoto N, Hao C, Williams IR, Liu X, Nakao S, Yamamoto A, Li SY, Hara-Nishimura I, Asano M, Ye K.
  • Journal Title: Proc Natl Acad Sci USA 106 Pages: 468-473
  • Peer Reviewed
• [Journal Article] Quantitative Analysis of ER Body Morphology in an Arabidopsis Mutant. (2009)
  • Author(s): Nagano AJ, Maekawa A, Nakano RT, Miyahara M, Higaki T, Kutsuna N, Hasezawa S, Hara-Nishimura I.
  • Journal Title: Plant Cell Physiol. 50 Pages: 2015-2022
  • Peer Reviewed
• [Journal Article] Vacuolar SNAREs function in the formation of the leaf vascular network by regulating auxin distribution. (2009)
  • Author(s): Shirakawa M, Ueda H, Shimada T, Nishiyama C, Hara-Nishimura I.
  • Journal Title: Plant Cell Physiol. 50 Pages: 1319-1328
  • Peer Reviewed
• [Journal Article] Neuroprotective actions of PIKE-L by inhibition of SET proteolytic degradation by asparagine endopeptidase. (2008)
  • Author(s): Liu Z, Jang SW, Liu X, Cheng D, Peng J, Yepes M, Li XJ, Matthews S, Watts C, Asano M, Hara-Nishimura I, Luo HR, Ye K.
  • Journal Title: Mol Cell 29 Pages: 665-678
  • Peer Reviewed
• [Journal Article] NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. (2008)
  • Author(s): Kunieda T, Mitsuda N, Ohme-Takagi M, Takeda S, Aida M, Tasaka M, Kondo M, Nishimura M, Hara-Nishimura I.
  • Journal Title: Plant Cell 20 Pages: 2631-2642
  • Peer Reviewed
• [Journal Article] A novel role of oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. (2008)
  • Author(s): Shimada TL, Shimada T, Takahashi H, Fukao Y, Hara-Nishimura I.
  • Journal Title: Plant J. 55 Pages: 798-809
  • Peer Reviewed
• [Journal Article] NAI2 is an endoplasmic reticulum body component that enables ER body formation in Arabidopsis thaliana. (2008)
  • Author(s): Yamada K, Nagano AJ, Nishina M, Hara-Nishimura I, Nishimura M.
  • Journal Title: Plant Cell 20 Pages: 2529-2540
  • Peer Reviewed
• [Journal Article] AtMap1 : a DNA microarray for genomic deletion mapping in Arabidopsis thaliana. (2008)
  • Author(s): Nagano AJ, Fukazawa M, Hayashi M, Ikeuchi M, Tsukaya H, Nishimura M, Hara-Nishimura I.
  • Journal Title: Plant J. 56 Pages: 1058-1065
  • Peer Reviewed
• [Journal Article] Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence. (2008)
  • Author(s): Yamazaki M, Shimada T, Takahashi H, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I.
  • Journal Title: Plant Cell Physiol. 49 Pages: 142-156
  • Peer Reviewed
• [Journal Article] Antagonistic jacalin-related lectins regulate the size of ER body-type beta-glucosidase complexes in Arabidopsis thaliana. (2008)
  • Author(s): Nagano AJ, Fukao Y, Fujiwara M, Nishimura M, Hara-Nishimura I.
  • Journal Title: Plant Cell Physiol. 49 Pages: 969-980
  • Peer Reviewed
• [Journal Article] Arabidopsis vacuolar-sorting mutants (green-fluorescent seed) can be identified efficiently by secretion of vacuole-targeted green-fluorescent protein in their seeds. (2007)
  • Author(s): Fuji, K, Shimada, T, Takahashi, H, Koumoto, Y, Utsumi, S, Nishizawa, K, Maruyama, N, Hara-Nishimura, I.
  • Journal Title: Plant Cell 19 Pages: 597-609
  • Peer Reviewed
• [Journal Article] Arabidopsis KAM2/GRV2 Is required for proper endosome formation and functions in vacuolar sorting and determination of the embryo growth axis. (2007)
  • Author(s): Tamura, K, Takahashi, H, Kunieda, T, Fuji, K, Shimada, T, Hara-Nishimura, I.
  • Journal Title: Plant Cell 19 Pages: 320-332
  • Peer Reviewed
• [Journal Article] An asparaginyl endopeptidase mediates in vivo protein backbone cyclization. (2007)
  • Author(s): Saska, I, Gillon, AD, Hatsugai, N, Dietzgen, RG, Hara-Nishimura, I, Anderson, MA, Craik, DJ.
  • Journal Title: J.Biol.Chem. 282 Pages: 29721-29728
  • Peer Reviewed
• [Journal Article] A cellular suicide strategy of plants : vacuole-mediated cell death. (2006)
  • Author(s): Hatsugai, N, Kuroyanagi, M, Nishimura, M, Hara-Nishimura, I.
  • Journal Title: Apoptosis 11 Pages: 905-911
  • Peer Reviewed
• [Journal Article] AtVAM3 is required for normal specification of idioblasts, myrosin cells. (2006)
  • Author(s): Ueda, H, Nishiyama, C, Shimada, T, Koumoto, Y, Hayashi, Y, Kondo, M, Takahashi, T, Ohtomo, I, Nishimura, M, Hara-Nishimura, I.
  • Journal Title: Plant Cell Physiol. 47 Pages: 164-175
  • Peer Reviewed
• [Journal Article] MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana. (2006)
  • Author(s): Li, L, Shimada, T, Takahashi, H, Ueda, H, Fukao, Y, Kondo, M, Nishimura, M, Hara-Nishimura, I.
  • Journal Title: Plant Cell 18 Pages: 3535-3547
  • Peer Reviewed
• [Journal Article] Vacuolar processing enzyme, a key molecule in both pathogen-induced and phytotoxin-induced cell death in higher plants. (2006)
  • Author(s): Kuroyanagi, M, Hara-Nishimura, I, Hatsugai, N, Nishimura, M.
  • Journal Title: Mol.Plant Microbe Interaction Vol.5 Pages: 208-214
  • Peer Reviewed
• [Journal Article] AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins. (2006)
  • Author(s): Shimada, T, Koumoto, Y, Li, L, Yamazaki, M, Kondo, M, Nishimura, M, Hara-Nishimura, I.
  • Journal Title: Plant Cell Physiol. 47 Pages: 1187-1194
  • Peer Reviewed
• [Journal Article] Vacuolar Processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. (2005)
  • Author(s): Kuroyanagi, M, Yamada, K, Hatsugai, N, Kondo, M, Nishimura, M, Hara-Nishimura, I.
  • Journal Title: J.Biol.Chem. 280 Pages: 32914-32920
  • Peer Reviewed
• [Journal Article] KATAMARI1/MUR3 is a novel Golgi membrane protein that is required for endomembrane organization in Arabidopsis. (2005)
  • Author(s): Tamura, K, Shimada, T, Kondo, M, Nishimura, M, Hara-Nishimura, I.
  • Journal Title: Plant Cell 17 Pages: 1764-1776
  • Peer Reviewed
• [Journal Article] A VPE family supporting various vacuolar functions in plants. (2005)
  • Author(s): Yamada, K, Shimada, T, Nishimura, M, Hara-Nishimura, I.
  • Journal Title: Physiol.Plant, Special Issue 123 Pages: 369-375
  • Peer Reviewed
• [Journal Article] Vacuolar processing enzyme : an executor of plant cell death. (2005)
  • Author(s): Hara-Nishimura, I, Hatsugai, N, Kuroyanagi, M, Nakaune, S, Nishimura, M.
  • Journal Title: Curr.Opinon Plant Biol. 8 Pages: 404-408
  • Peer Reviewed
• [Journal Article] Asparagine endopeptidase is not essential for class II MHC antigen presentation but is required for processing of cathepsin L in mice. (2005)
  • Author(s): Maehr, R, Hang, HC, Mintern, JD, Kim, Y-M, Culvillier, A, Nishimura, M, Yamada, K, Shiramama-Noda, K, Hara-Nishimura, I, Ploegh, HL.
  • Journal Title: J.Immunol. 174 Pages: 7066-7074
  • Peer Reviewed
• [Journal Article] Activation of an ER-body-localized β-glucosidase via a cytosolic binding partner in damaged tissues of Arabidopsis thaliana. (2005)
  • Author(s): Nagano, JA, Matsushima, R, Hara-Nishimura, I.
  • Journal Title: Plant Cell Physiol. 46 Pages: 1140-1148
  • Peer Reviewed
• [Presentation] Plants use two types of vacuole-mediated plant immunity : Proteasome-dependent membrane fusion and VPE-dependent vacuolar collapse. (2010)
  • Author(s): Hara-Nishimura I.
  • Organizer: The 2010 Cold Spring Harbor Asia Conference
  • Place of Presentation: Suzhou, China(招待講演)
  • Year and Date: 20101025-20101029
• [Presentation] Two types of vacuole-mediated plant immunity : proteasome-dependent membrane fusion and VPE-dependent vacuolar collapse. (2010)
  • Author(s): Hara-Nishimura I.
  • Organizer: Frontiers in Developmental Cell Biology. Plants & Beyond
  • Place of Presentation: Lausanne, Switzerland(招待講演)
  • Year and Date: 20100907-20100908
• [Presentation] A membrane fusion-mediated plant defense strategy against bacterial pathogens. (2010)
  • Author(s): Hara-Nishimura I.
  • Organizer: 21st International Conference on Arabidopsis Research 2010.
  • Place of Presentation: Yokohama Pacifico Yokohama(招待講演)
  • Year and Date: 20100606-20100610
• [Presentation] A novel membrane fusion-mediated plant immunity against bacterial pathogens. (2010)
  • Author(s): Hara-Nishimura I.
  • Organizer: 2010 International Symposium : Development and Defense
  • Place of Presentation: Seoul, Korea(招待講演)
  • Year and Date: 2010-08-20
• [Presentation] Plant Defense Strategies Using Vacuoles and Endomembranes. (2009)
  • Author(s): Hara-Nishimura, I.
  • Organizer: Premium International Symposium Nagoya Univ.
  • Place of Presentation: Nagoya(招待講演)
  • Year and Date: 2009-03-24
• [Presentation] Different Vacuole-Mediated-Defense Strategies Against Invading Viral and Bacterial Pathogens. (2008)
  • Author(s): Hara-Nishimura, I.
  • Organizer: The 55th NIBB Conference "Frontiers of Plant Science in the 21st Century"
  • Place of Presentation: NIBB, Okazaki(招待講演)
  • Year and Date: 20080913-20080915
• [Presentation] Vacuolar sorting and vacuolar processing systems in higher plants. (2007)
  • Author(s): Hara-Nishimura, I., Shimada, T., Fuji, K., Li, L., Takahashi, H.
  • Organizer: Plant Cell Biology Conference
  • Place of Presentation: Max-Planck-Institute, Cologne, Germany(招待講演)
  • Year and Date: 20070904-20070906
• [Presentation] Vacuolar sorting mechanism in plants. (2007)
  • Author(s): Hara-Nishimura, I., Shimada, T., Fuji, K., Li, L., Takahashi, H.
  • Organizer: 19th FAOBMB Conference
  • Place of Presentation: Seoul, Korea(招待講演)
  • Year and Date: 20070528-20070530
• [Presentation] Vacuolar sorting and vacuolar processing of seed storage proteins. (2006)
  • Author(s): Hara-Nishimura, I.
  • Organizer: International Symposium of Plant Molecular Biology
  • Place of Presentation: Adelaide, Australia(招待講演)
  • Year and Date: 20060820-20060825
• [Presentation] Vacuolar processing enzyme (VPE) : an executor of vacuole-mediated cell death in plants. (2006)
  • Author(s): Hara-Nishimura, I., Hatsugai, N., Kuroyanagi, M., Nakaune, S., Kunieda, T., Takahashi, K., Nishimura, M.
  • Organizer: 20th IUBMB International Congress of Biochemistry and Molecular Biology and 11th FAOBMB Congress
  • Place of Presentation: Kyoto International Conference Center, Kyoto(招待講演)
  • Year and Date: 20060618-20060623
• [Presentation] Involvement of vacuolar processing enzyme (VPE) in plant cell death. (2006)
  • Author(s): Hara-Nishimura, I., Hatsugai, N, Kuroyanagi, M., Nakaune, S., Kunieda, T., Takahashi, K., Nishimura, M.
  • Organizer: The 53rd NIBB Conference "Dynamic Organelles in Plants"
  • Place of Presentation: NIBB, Okazaki(招待講演)
  • Year and Date: 20060614-20060617
• [Presentation] Vacuolar processing enzyme responsible for programmed cell death in plants. (2006)
  • Author(s): Hara-Nishimura, I.
  • Organizer: The NAIST COE Symposium "Frontiers in Plant Immunity Research"
  • Place of Presentation: NAIST, Nara(招待講演)
  • Year and Date: 2006-06-24
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  • Industrial Property Rights Holder: 京都大学
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• [Patent(Industrial Property Rights)] 新規選択マーカー遺伝子およびその利用 (2010)
  • Inventor(s): 島田貴士, 嶋田知生, 西村いくこ
  • Industrial Property Rights Holder: 京都大学
  • Industrial Property Number: PTC/JP2009/059592
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• [Patent(Industrial Property Rights)] ポリペプチド,気孔増加剤,植物における気孔の数および/または密度の増加方法ならびに植物 (2009)
  • Inventor(s): 菅野茂夫, 嶋田知生, 西村いくこ
  • Industrial Property Rights Holder: 京都大学
  • Industrial Property Number: 特願2009-278065
  • Filing Date: 2009-12-07
• [Patent(Industrial Property Rights)] VPE欠損モデル (2009)
  • Inventor(s): 西村いくこ, 野田佳苗, 浅野雅秀, 西村幹夫
  • Industrial Property Rights Holder: 独立行政法人科学技術振興機構
  • Industrial Property Number: 特願2003-117686
  • Acquisition Date: 2009-09-18
• [Patent(Industrial Property Rights)] 新規選択マーカー遺伝子およびその利用 (2008)
  • Inventor(s): 島田貴士, 嶋田知生, 西村いくこ
  • Industrial Property Rights Holder: 京都大学
  • Industrial Property Number: 特願2008-140083
  • Filing Date: 2008-05-28