Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants

Journal of Plant Research

Volumn 124, Issue 3, 2011, Pages 315-324

  Higaki, Takumi ^a,b   Kurusu, Takamitsu ^b   Hasezawa, Seiichiro ^a   Kuchitsu, Kazuyuki ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Actin microfilament; Elicitor; Innate immunity; Microtubule; Programmed cell death; Vacuole

Indexed keywords

ACTIN; CALCIUM; REACTIVE OXYGEN METABOLITE; VEGETABLE PROTEIN;

CELL DEATH; CELL VACUOLE; CELL WALL; CYTOLOGY; CYTOPLASM; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; INTRACELLULAR MEMBRANE; METABOLISM; MICROBIOLOGY; MICROFILAMENT; PHYSIOLOGY; PLANT; PLANT DISEASE; REVIEW;

ACTINS; CALCIUM; CELL DEATH; CELL WALL; CYTOPLASM; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTRACELLULAR MEMBRANES; MICROFILAMENTS; PLANT DISEASES; PLANT PROTEINS; PLANTS; REACTIVE OXYGEN SPECIES; VACUOLES;

EID: 79955373336     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10265-011-0408-z     Document Type: Review

References (83)

1. Aist JR (1976) Papillae and related wound plugs of plant cells. Annu Rev Phytopathol 14: 145-163.
2. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15: 5118-5129.
3. Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323: 101-106.
4. Binet MN, Humbert C, Lecourieux D, Vantard M, Pugin A (2001) Disruption of microtubular cytoskeleton induced by cryptogein, an elicitor of hypersensitive response in tobacco cells. Plant Physiol 125: 564-572.
5. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15: 441-447.
6. Cahill D, Rookes J, Michalczyk A, McDonald K, Drake A (2002) Microtubule dynamics in compatible and incompatible interactions of soybean hypocotyls cells with Phytophthora sojae. Plant Pathol 51: 629-640.
7. Choi Y, Lee Y, Jeon BW, Staiger CJ, Lee Y (2008) Phosphatidylinositol 3- and 4-phosphate modulate actin filament reorganization in guard cells of day flower. Plant Cell Environ 31: 366-377.
8. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95-101.
9. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973-977.
10. Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka K (2003) High-throughput vital expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 15: 1507-1523.
11. Franklin-Tong VE, Gourlay CW (2008) A role for actin in regulating apoptosis/programmed cell death: evidence spanning yeast, plants and animals. Biochem J 413: 389-404.
12. Gross P, Julius C, Schmelzer E, Hahlbrock K (1993) Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defence gene activation in infected, cultured parsley cells. EMBO J 12: 1735-1744.
13. Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, Yang Z (2005) A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 169: 127-138.
14. Gunawardena AH, Greenwood JS, Dengler NG (2004) Programmed cell death remodels lace plant leaf shape during development. Plant Cell 16: 60-73.
15. Guo WJ, Ho TH (2008) An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiol 147: 1710-1722.
16. Hardham AR, Takemoto D, White RG (2008) Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8: 63.
17. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305: 855-858.
18. Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11: 905-911.
19. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, Nishimura M, Hara-Nishimura I (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23: 2496-2506.
20. Hazen BE, Bushnell WR (1983) Inhibition of the hypersensitive reaction in barley to powdery mildew by heat shock and cytochalasin B. Physiol Plant Pathol 23: 421-438.
21. Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44: 321-334.
22. Higaki T, Kutsuna N, Okubo E, Sano T, Hasezawa S (2006) Actin microfilaments regulate vacuolar structures and dynamics: dual observation of actin microfilaments and vacuolar membrane in living tobacco BY-2 cells. Plant Cell Physiol 47: 839-852.
23. Higaki T, Goh T, Hayashi T, Kutsuna N, Kadota Y, Hasezawa S, Sano T, Kuchitsu K (2007) Elicitor-induced cytoskeletal rearrangement relates to vacuolar dynamics and execution of cell death: in vivo imaging of hypersensitive cell death in tobacco BY-2 cells. Plant Cell Physiol 48: 1414-1425.
24. Higaki T, Kadota Y, Goh T, Hayashi T, Kutsuna N, Sano T, Hasezawa S, Kuchitsu K (2008) Vacuolar and cytoskeletal dynamics during elicitor-induced programmed cell death in tobacco BY-2 cells. Plant Signal Behav 3: 700-703.
25. Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125: 94-97.
26. 2+ channels and cell cycle in tobacco BY-2 cells. In: Nagata T, Matsuoka K, Inze D (eds) Biotechnology in agriculture and forestry 58 Tobacco BY-2 cells: from cellular dynamics to omics. Springer, Berlin, pp 207-221.
27. 2+ transients and defense responses in tobacco BY-2 cells. Biochem Biophys Res Commun 317: 823-830.
28. 2+ transients, anion efflux and production of reactive oxygen species. Plant Cell Physiol 45: 160-170.
29. Kadota Y, Watanabe T, Fujii S, Higashi K, Sano T, Nagata T, Hasezawa S, Kuchitsu K (2004c) Crosstalk between elicitor-induced cell death and cell cycle regulation in tobacco BY-2 cells. Plant J 40: 131-142.
30. Kadota Y, Watanabe T, Fujii S, Maeda Y, Ohno R, Higashi K, Sano T, Muto S, Hasezawa S, Kuchitsu K (2005) Cell cycle dependence of elicitor-induced signal transduction in tobacco BY-2 cells. Plant Cell Physiol 46: 156-165.
31. Kadota Y, Fujii S, Ogasawara Y, Maeda Y, Higashi K, Kuchitsu K (2006) Continuous recognition of the elicitor signal for several hours is prerequisite for induction of cell death and prolonged activation of signaling events in tobacco BY-2 cells. Plant Cell Physiol 47: 1337-1342.
32. Kobayashi I, Hakuno H (2003) Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta 217: 340-345.
33. Kobayashi I, Kobayashi Y, Yamaoka N, Kunoh H (1992) Recognition of a pathogen and a nonpathogen by barley coleoptile cells. III. Response of microtubules and actin filaments in barley coleoptile cells to penetration attempts. Can J Bot 70: 1815-1823.
34. Kobayashi I, Kobayashi Y, Hardham AR (1994) Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195: 237-247.
35. Kobayashi I, Kobayashi Y, Hardham AR (1997a) Inhibition of rust-induced hypersensitive response in flax cells by the microtubule inhibitor oryzalin. Aust J Plant Physiol 24: 733-740.
36. Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T, Kunoh H (1997b) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J 11: 525-537.
37. Koh S, Andre A, Edwards H, Ehrhardt D, Someville S (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44: 516-529.
38. Kumagai F, Yoneda A, Tomida T, Sano T, Nagata T, Hasezawa S (2001) Fate of nascent microtubules organized at the M/G1 interface, as visualized by synchronized tobacco BY-2 cells stably expressing GFP-tubulin: time-sequence observations of the reorganization of cortical microtubules in living plant cells. Plant Cell Physiol 42: 723-732.
39. Kuriyama H (1999) Loss of tonoplast integrity programmed in tracheary element differentiation. Plant Physiol 121: 763-774.
40. 2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J 42: 798-809.
41. 2+ transients by protein phosphorylation. J Plant Res. doi: 10. 1007/s10265-010-0388-4.
42. Kutsuna N, Hasezawa S (2002) Dynamic organization of vacuolar and microtubule structures during cell cycle progression in synchronized tobacco BY-2 cells. Plant Cell Physiol 43: 965-973.
43. Kutsuna N, Hasezawa S (2005) Morphometrical study of plant vacuolar dynamics in single cells using three-dimensional reconstruction form optical sections. Microsc Res Tech 68: 296-306.
44. Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jürgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451: 835-840.
45. Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14: 2627-2641.
46. Lee YJ, Szumlanski A, Nielsen E, Yang Z (2008) Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J Cell Biol 181: 1155-1168.
47. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183.
48. Marty F (1999) Plant vacuoles. Plant Cell 11: 587-600.
49. Meyer D, Pajonk S, Micali C, O'Connell R, Schulze-Lefert P (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57: 986-999.
50. Miklis M, Consonni C, Bhat RA, Lipka V, Schulze-Lefert P, Panstruga R (2007) Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiol 144: 1132-1143.
51. Mongrand S, Stanislas T, Bayer EM, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends Plant Sci 15: 656-663.
52. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59: 501-520.
53. Nakaune S, Yamada K, Kondo M, Kato T, Tabata S, Nishimura M, Hara-Nishimura I (2005) A vacuolar processing enzyme, δVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17: 876-887.
54. 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: 615-626.
55. 2+ and phosphorylation. J Biol Chem 283: 8885-8892.
56. Pajerowska-Mukhtar K, Dong X (2009) A kiss of death-proteasome-mediated membrane fusion and programmed cell death in plant defense against bacterial infection. Genes Dev 23: 2449-2454.
57. Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9: 1157-1168.
58. Poulter NS, Vatovec S, Franklin-Tong VE (2008) Microtubules are a target for self-incompatibility signaling in Papaver pollen. Plant Physiol 146: 1358-1367.
59. Reape TJ, McCabe PF (2010) Apoptotic-like regulation of programmed cell death in plants. Apoptosis 15: 249-256.
60. Reisen D, Marty F, Leborgne-Castel N (2005) New insights into the tonoplast architecture of plant vacuoles and vacuolar dynamics during osmotic stress. BMC Plant Biol 5: 13.
61. Saito SY, Watabe S, Ozaki H, Kobayashi M, Suzuki T, Kobayashi H, Fusetani N, Karaki H (1998) Actin-depolymerizing effect of dimeric macrolides, bistheonellide A and swinholide A. J Biochem 123: 571-578.
62. Saito C, Ueda T, Abe H, Wada Y, Kuroiwa T, Hisada A, Furuya M, Nakano A (2002) A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29: 245-255.
63. Samaj J, Ovecka M, Hlavacka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bögre L, Baluska F, Hirt H (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. EMBO J 21: 3296-3306.
64. Sano T, Higaki T, Oda Y, Hayashi T, Hasezawa S (2005) Appearance of actin microfilament 'twin peaks' in mitosis and their function in cell plate formation, as visualized in tobacco BY-2 cells expressing GFP-fimbrin. Plant J 44: 595-605.
65. Schreiber K, Ckurshumova W, Peek J, Desveaux D (2008) A high-throughput chemical screen for resistance to Pseudomonas syringae in Arabidopsis. Plant J 54: 522-531.
66. Schütz I, Gus-Mayer S, Schmelzer E (2006) Profilin and Rop GTPases are localized at infection sites of plant cells. Protoplasma 227: 229-235.
67. Shimada C, Lipka V, O'Connell R, Okuno T, Schulze-Lefert P, Takano Y (2006) Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Mol Plant Microbe Interact 19: 270-279.
68. Skalamera D, Heath MC (1995) Changes in the plant endomembrane system associated with callose synthesis during the interaction between cowpea (Vigna unguiculata) and the cowpea fungus (Uromyces vignae). Can J Bot 73: 1731-1738.
69. Skalamera D, Heath MC (1996) Cellular mechanisms of callose deposition in response to fungal infection or chemical damage. Can J Bot 74: 1236-1242.
70. Skalamera D, Heath MC (1998) Changes in the cytoskeleton accompanying infection-induced nuclear movements and the hypersensitive response in plant cells invaded by rust fungi. Plant J 16: 191-200.
71. Skalamera D, Jibodh S, Heath MC (1997) Callose deposition during the interaction between cowpea (Vigna unguiculata) and the monokaryotic stage of the cowpea fungus (Uromyces vignae). New Phytol 136: 511-524.
72. Smertenko AP, Bozhkov PV, Filonova LH, von Arnold S, Hussey PJ (2003) Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos. Plant J 33: 813-824.
73. Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18: 731-746.
74. Takemoto D, Maeda H, Yoshioka H, Doke N, Kawakita K (1999) Effect of cytochalasin D on defense responses of potato tuber discs treated with hyphal wall components of Phytophthora infestans. Plant Sci 141: 219-226.
75. Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33: 775-792.
76. Takemoto D, Jones DA, Hardham AR (2006) Re-organization of the cytoskeleton and endoplasmic reticulum in the Arabidopsis pen1-1 mutant inoculated with the non-adapted powdery mildew pathogen, Blumeria graminis f. sp. hordei. Mol Plant Pathol 7: 553-563.
77. Tang X, Lancelle SA, Hepler PK (1989) Fluorescence microscopic localization of actin in pollen tubes: comparison of actin antibody and phalloidin staining. Cell Motil Cytoskelet 12: 216-224.
78. Thomas SG, Huang S, Li S, Staiger CJ, Franklin-Tong VE (2006) Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. J Cell Biol 174: 221-229.
79. Tian M, Chaudhry F, Ruzicka DR, Meagher RB, Staiger CJ, Day B (2009) Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol 150: 815-824.
80. Tomiyama K, Sato K, Doke N (1982) Effect of cytochalasin B and colchicines on hypersensitive death of potato cells infected by incompatible race of Phytophthora infestans. Ann Phytopathol Soc Jpn 48: 228-230.
81. Uemura T, Yoshimura SH, Takeyasu K, Sato MH (2002) Vacuolar membrane dynamics revealed by GFP-AtVam3 fusion protein. Genes Cells 7: 743-753.
82. Wright H, van Doorn WG, Gunawardena AH (2009) In vivo study of developmental programmed cell death using the lace plant (Aponogeton madagascariensis; Aponogetonaceae) leaf model system. Am J Bot 96: 865-876.
83. Yun BW, Atkinson HA, Gaborit C, Greenland A, Read ND, Pallas JA, Loake GJ (2003) Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. Plant J 34: 768-777.