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Tuesday, 13 December 2016

Suppression of OsVPE3 Enhances Salt Tolerance by Attenuating Vacuole Rupture during Programmed Cell Death and Affects Stomata Development in Rice

Published Date
AccessOriginal article
First Online: 
29 November 2016
DOI: 10.1186/s12284-016-0138-x


Cite this article as: 
Lu, W., Deng, M., Guo, F. et al. Rice (2016) 9: 65. doi:10.1186/s12284-016-0138-x


Author 

  • Wenyun Lu
  • Minjuan Deng
  • Fu Guo
  • Mingqiang Wang
  • Zhanghui Zeng
  • Ning Han
  • Yinong Yang
  • Muyuan Zhu
  • Hongwu Bian
Abstract 

Background

Vacuolar processing enzymes (VPEs) are cysteine proteinases that act as crucial mediators of programmed cell death (PCD) in plants. In rice, however, the role of VPEs in abiotic stress-induced PCD remains largely unknown. In this study, we generated OsVPE3 overexpression and suppression transgenic lines to elucidate the function of this gene in rice.

Results

Survival rate and chlorophyll retention analyses showed that suppression of OsVPE3 clearly enhanced salt stress tolerance in transgenic rice compared with wild type. Furthermore, fragmentation of genomic DNA was inhibited in plants with down-regulated OsVPE3. Vital staining studies indicated that vacuole rupture occurred prior to plasma membrane collapse during salt-induced PCD. Notably, overexpression of OsVPE3 promoted vacuole rupture, whereas suppression of OsVPE3 attenuated or delayed the disintegration of vacuolar membranes. Moreover, we found that suppression of OsVPE3 caused decreased leaf width and guard cell length in rice.

Conclusions

Taken together, these results indicated that suppression of OsVPE3 enhances salt tolerance by attenuating vacuole rupture during PCD. Therefore, we concluded that OsVPE3 plays a crucial role in vacuole-mediated PCD and in stomatal development in rice.

Keywords

OsVPE3Programmed cell deathRiceSalt stressStomataVacuolar processing enzyme

Abbreviations

BCECF-AM
2’,7’-bis-(2-carboxyethyl)-5-(and-6)-carboxyfluorescein-acetoxymethyl
BCL-2
B-cell lymphoma-2
GFP
Green fluorescent protein
MPK6
Mitogen-activated protein kinase 6
PCD
Programmed cell death
qRT-PCR
Real time quantitative polymerase chain reaction
ROS
Reactive oxygen species
SOS
Salt-overly-sensitive
VPE
Vacuolar processing enzymes




References 
  1. Albertini A, Simeoni F, Galbiati M, Bauer H, Tonelli C, Cominelli E (2014) Involvement of the vacuolar processing enzyme gamma VPE in response of Arabidopsis thaliana to water stress. Biol Plantarum 58:531–538CrossRefGoogle Scholar
  2. Assmann SM (1993) Signal-Transduction in Guard-Cells. Annu Rev Cell Biol 9:345–375CrossRefPubMedGoogle Scholar
  3. Azeez A, Sane AP, Bhatnagar D, Nath P (2007) Enhanced expression of serine proteases during floral senescence in Gladiolus. Phytochemistry 68:1352–1357CrossRefPubMedGoogle Scholar
  4. Bai Y, Han N, Wu J, Yang Y, Wang J, Zhu M, Bian H (2014) A transient gene expression system using barley protoplasts to evaluate microRNAs for post-transcriptional regulation of their target genes. Plant Cell Tissue Organ Cult 119:211–219CrossRefGoogle Scholar
  5. Balcerowicz M, Hoecker U (2014) Auxin - a novel regulator of stomata differentiation. Trends Plant Sci 19:747–749CrossRefPubMedGoogle Scholar
  6. Boller T, Wiemken A (1986) Dynamics of Vacuolar Compartmentation. Annu Rev Plant Phys 37:137–164CrossRefGoogle Scholar
  7. De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant, Cell Environ 35:234–244CrossRefGoogle Scholar
  8. Deng MJ, Bian HW, Xie YK, Kim Y, Wang WZ, Lin EP, Zeng ZH, Guo F, Pan JW, Han N, Wang JH, Qian Q, Zhu MY (2011) Bcl-2 suppresses hydrogen peroxide-induced programmed cell death via OsVPE2 and OsVPE3, but not via OsVPE1 and OsVPE4, in rice. Febs Journal 278:4797–4810CrossRefPubMedGoogle Scholar
  9. Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9CrossRefGoogle Scholar
  10. Gao JP, Chao DY, Lin HX (2007) Understanding abiotic stress tolerance mechanisms: Recent studies on stress response in rice. J Integr Plant Biol 49:742–750CrossRefGoogle Scholar
  11. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101CrossRefPubMedGoogle Scholar
  12. Geisler M, Nadeau J, Sack FD (2000) Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–2086CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hara-Nishimura I, Hatsugai N (2011) The role of vacuole in plant cell death. Cell Death Differ 18:1298–1304CrossRefPubMedPubMedCentralGoogle Scholar
  14. Haranishimura I, Inoue K, Nishimura M (1991) A Unique Vacuolar Processing Enzyme Responsible for Conversion of Several Proprotein Precursors into the Mature Forms. FEBS Lett 294:89–93CrossRefGoogle Scholar
  15. Haranishimura I, Takeuchi Y, Nishimura M (1993) Molecular Characterization of a Vacuolar Processing Enzyme Related to a Putative Cysteine Proteinase of Schistosoma-Mansoni. Plant Cell 5:1651–1659CrossRefGoogle Scholar
  16. Hara-Nishimura I, Kinoshita T, Hiraiwa N, Nishimura M (1998) Vacuolar processing enzymes in protein-storage vacuoles and lytic vacuoles. J Plant Physiol 152:668–674CrossRefGoogle Scholar
  17. Hara-Nishimura I, Hatsugai N, Nakaune S, Kuroyanagi M, Nishimura M (2005) Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 8:404–408CrossRefPubMedGoogle Scholar
  18. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Hara-Nishimura I, Nishimura M (2004a) Vacuolar processing enzyme exhibiting caspase-1-like activity is involved in TMV-induced hypersensitive cell death in tobacco. Plant and Cell Physiology 45, S143-S143
  19. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004b) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305, 855–858
  20. Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11:905–911CrossRefPubMedGoogle Scholar
  21. Hatsugai N, Yamada K, Yamada S, Hara-Nishimura I (2015) Vacuolar processing enzyme in plant programmed cell death. Front Plant Sci 6:234CrossRefPubMedPubMedCentralGoogle Scholar
  22. Higaki T, Kurusu T, Hasezawa S, Kuchitsu K (2011) Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants. J Plant Res 124:315–324CrossRefPubMedGoogle Scholar
  23. Hiraiwa N, Takeuchi Y, Nishimura M, Haranishimura I (1993) A Vacuolar Processing Enzyme in Maturing and Germinating-Seeds - Its Distribution and Associated Changes during Development. Plant Cell Physiol 34:1197–1204Google Scholar
  24. Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: An overview with the central focus on rice plant. Rice 5:11CrossRefPubMedGoogle Scholar
  25. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29:649–659CrossRefPubMedGoogle Scholar
  26. Jiang AL, Cheng YW, Li JY, Zhang W (2008) A zinc-dependent nuclear endonuclease is responsible for DNA laddering during salt-induced programmed cell death in root tip cells of rice. J Plant Physiol 165:1134–1141CrossRefPubMedGoogle Scholar
  27. Kagan ML, Novoplansky N, Sachs T (1992) Variable Cell Lineages Form the Functional Pea Epidermis. Ann Bot 69:303–312Google Scholar
  28. Kariya K, Demiral T, Sasaki T, Tsuchiya Y, Turkan I, Sano T, Hasezawa S, Yamamoto Y (2013) A novel mechanism of aluminium-induced cell death involving vacuolar processing enzyme and vacuolar collapse in tobacco cell line BY-2. J Inorg Biochem 128:196–201CrossRefPubMedGoogle Scholar
  29. Khatun S, Flowers TJ (1995) Effects of Salinity on Seed Set in Rice. Plant, Cell Environ 18:61–67CrossRefGoogle Scholar
  30. Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M, Blajecka K, Herrfurth C, Feussner I, Apel K (2012) Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. Plant Cell 24:3026–3039CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kim YH, Wang MQ, Bai Y, Zeng ZH, Guo F, Han N, Bian HW, Wang JH, Pan JW, Zhu MY (2014) Bcl-2 suppresses activation of VPEs by inhibiting cytosolic Ca2+ level with elevated K+ efflux in NaCl-induced PCD in rice. Plant Physiol Bioch 80:168–175CrossRefGoogle Scholar
  32. Kinoshita T, Yamada K, Hiraiwa N, Kondo M, Nishimura M, Hara-Nishimura I (1999) Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J 19:43–53CrossRefPubMedGoogle Scholar
  33. Krishnan HB, Okita TW (1986) Structural Relationship among the Rice Glutelin Polypeptides. Plant Physiol 81:748–753CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kudla J, Batistic O, Hashimoto K (2010) Calcium Signals: The Lead Currency of Plant Information Processing. Plant Cell 22:541–563CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I (2005) Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J Biol Chem 280:32914–32920CrossRefPubMedGoogle Scholar
  36. Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Bio 5:305–315CrossRefGoogle Scholar
  37. Li JY, Jiang AL, Zhang W (2007) Salt stress-induced programmed cell death in rice root tip cells. J Integr Plant Biol 49:481–486CrossRefGoogle Scholar
  38. Li Z, Yue HY, Xing D (2012) MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytol 195:85–96CrossRefPubMedGoogle Scholar
  39. Lin JS, Wang Y, Wang GX (2006) Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status. J Plant Physiol 163:731–739CrossRefPubMedGoogle Scholar
  40. Liu T, Ohashi-Ito K, Bergmann DC (2009) Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development 136:2265–2276CrossRefPubMedGoogle Scholar
  41. Menezes-Benavente L, Teixeira FK, Kamei CLA, Margis-Pinheiro M (2004) Salt stress induces altered expression of genes encoding antioxidant enzymes in seedlings of a Brazilian indica rice (Oryza sativa L.). Plant Sci 166:323–331CrossRefGoogle Scholar
  42. Mino M, Murata N, Date S, Inoue M (2006) Collapse of vacuole is a direct factor of cell death in the seedling of interspecific hybrid of Nicotiana gossei x N-tabacum. Plant Cell Physiol 47:S182–S182Google Scholar
  43. Mittler R, Simon L, Lam E (1997) Pathogen-induced programmed cell death in tobacco. J Cell Sci 110:1333–1344PubMedGoogle Scholar
  44. Neuhaus JM, Sticher L, Meins F, Boller T (1991) A Short C-Terminal Sequence Is Necessary and Sufficient for the Targeting of Chitinases to the Plant Vacuole. Proc Natl Acad Sci U S A 88:10362–10366CrossRefPubMedPubMedCentralGoogle Scholar
  45. Nicholson DW (1999) Caspase structure, proteolytic substrates, and functionduring apoptotic cell death. Cell Death Differ 6:1028–1042CrossRefPubMedGoogle Scholar
  46. Obara K, Kuriyama H, Fukuda H (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125:615–626CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pan JW, Ye D, Wang LL, Hua J, Zhao GF, Pan WH, Han N, Zhu MY (2004) Root border cell development is a temperature-insensitive and Al-sensitive process in barley. Plant Cell Physiol 45, 751–760.CrossRefPubMedGoogle Scholar
  48. Rea PA, Sanders D (1987) Tonoplast Energization - 2 H+ Pumps, One Membrane. Physiol Plantarum 71:131–141CrossRefGoogle Scholar
  49. Rojo E, Zouhar J, Carter C, Kovaleva V, Raikhel NV (2003) A unique mechanism for protein processing and degradation in Arabidopsis thaliana. Proc Natl Acad Sci U S A 100:7389–7394CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sahi C, Singh A, Kumar K, Blumwald E, Grover A (2006) Salt stress response in rice: genetics, molecular biology, and comparative genomics. Funct Integr Genomics 6:263–284CrossRefPubMedGoogle Scholar
  51. Samuilov VD, Lagunova EM, Gostimsky SA, Timofeev KN, Gusev MV (2003) Role of chloroplast photosystems II and I in appoptosis of pea guard cells. Biochemistry-Moscow 68:912–917CrossRefPubMedGoogle Scholar
  52. Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404CrossRefPubMedGoogle Scholar
  53. Shabala S (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 60:709–711CrossRefPubMedGoogle Scholar
  54. Swanson SJ, Jones RL (1996) Gibberellic acid induces vacuolar acidification in barley aleurone. Plant Cell 8:2211–2221CrossRefPubMedPubMedCentralGoogle Scholar
  55. Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The Rice Mutant esp2 Greatly Accumulates the Glutelin Precursor and Deletes the Protein Disulfide Isomerase. Plant Physiology 128(4):1212–1222.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Tamura K, Shimada T, Ono E, Tanaka Y, Nagatani A, Higashi S, Watanabe M, Nishimura M, Hara-Nishimura I (2003) Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants. Plant J 35:545–555CrossRefPubMedGoogle Scholar
  57. Tang RJ, Liu H, Yang Y, Yang L, Gao XS, Garcia VJ, Luan S, Zhang HX (2012) Tonoplast calcium sensors CBL2 and CBL3 control plant growth and ion homeostasis through regulating V-ATPase activity in Arabidopsis. Cell Res 22:1650–1665CrossRefPubMedPubMedCentralGoogle Scholar
  58. van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761CrossRefPubMedGoogle Scholar
  59. Wang YH, Zhu SS, Liu SJ, Jiang L, Chen LM, Ren YL, Han XH, Liu F, Ji SL, Liu X, Wan JM (2009) The vacuolar processing enzyme OsVPE1 is required for efficient glutelin processing in rice. Plant J 58:606–617CrossRefPubMedGoogle Scholar
  60. Williams B, Dickman M (2008) Plant programmed cell death: can't live with it; can't live without it. Mol Plant Pathol 9:531–544CrossRefPubMedGoogle Scholar
  61. Wituszynska W, Szechynska-Hebda M, Sobczak M, Rusaczonek A, Kozlowska-Makulska A, Witon D, Karpinski S (2015) LESION SIMULATING DISEASE 1 and ENHANCED DISEASE SUSCEPTIBILITY 1 differentially regulate UV-C-induced photooxidative stress signalling and programmed cell death in Arabidopsis thaliana. Plant, Cell Environ 38:315–330CrossRefGoogle Scholar
  62. Yamada K, Matsushima R, Nishimura M, Hara-Nishimura I (2001) A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing arabidopsis leaves. Plant Physiol 127:1626–1634CrossRefPubMedPubMedCentralGoogle Scholar
  63. Yamagata H, Sugimoto T, Tanaka K, Kasai Z (1982) Biosynthesis of Storage Proteins in Developing Rice Seeds. Plant Physiol 70:1094–1100CrossRefPubMedPubMedCentralGoogle Scholar
  64. Yoshida S, Forno D, Cock J, Gomez K (1976) Laboratory Manual for Physiological Studies of Rice, 3rd edn. International Rice Research Institute, Manila, PhilippinesGoogle Scholar
  65. Yu XJ, Li GX, Xu D, Dong XL, Qi XX, Deng YQ (2006) An improvement of cucumber cotyledon greening bioassay for cytokinins. Acta Physiol Plant 28:9–11CrossRefGoogle Scholar
  66. Zhang KW, Xia XY, Zhang YY, Gan SS (2012) An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J 69:667–678CrossRefPubMedGoogle Scholar
  67. Zhang HY, Niu XL, Liu J, Xiao FM, Cao SQ, Liu YS (2013a) RNAi-Directed Downregulation of Vacuolar H+−ATPase Subunit A Results in Enhanced Stomatal Aperture and Density in Rice. PloS one 8 (7) e69046
  68. Zhang J, Li QF, Huang WW, Xu XY, Zhang XL, Hui MX, Zhang MK, Zhang LG (2013b) A Vacuolar Processing Enzyme RsVPE1 Gene of Radish Is Involved in Floral Bud Abortion under Heat Stress. International journal of molecular sciences 14, 13346–13359
  69. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar
  70. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445CrossRefPubMedGoogle Scholar

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