Cortical microtubule as a sensor and target of nitric oxide signal during the defence responses to Verticillium dahliae toxins in Arabidopsis

Plant, Cell and Environment

Volumn 32, Issue 4, 2009, Pages 428-438

  Shi, Fu Mei ^a,b   Yao, Lin Lin ^a   Pei, Bao Lei ^a   Zhou, Qun ^a   Li, Xiu Li ^a   Li, Yun ^a   Li, Ying Zhang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b LIAOCHENG UNIVERSITY   (China)

Author keywords

Cortical microtubules dynamics; Defence mechanisms; NO signal

Indexed keywords

ARABIDOPSIS PROTEIN; MYCOTOXIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NOA1 PROTEIN, ARABIDOPSIS; PLANT RNA;

ANGIOSPERM; DEFENSE MECHANISM; GENE EXPRESSION; GENETIC ANALYSIS; NITRIC OXIDE; SIGNAL; TOXIN;

ARABIDOPSIS; ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MICROTUBULE; MUTATION; PATHOGENICITY; PHYLLACHORALES; PLANT DISEASE; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; MICROTUBULES; MUTATION; MYCOTOXINS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHYLLACHORALES; PLANT DISEASES; RNA, PLANT; SIGNAL TRANSDUCTION;

ARABIDOPSIS; VERTICILLIUM DAHLIAE;

EID: 61649098842     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2009.01939.x     Document Type: Article

References (66)

1. de Almeida Engler J., Poucke K.V., Karimi M., Groodt R.D., Gheysen G., Engler G. Gheysen G. (2004) Dynamic cytoskeleton rearrangments in giant cells and syncytia of nematode-infected roots. The Plant Journal 38, 12 26.
2. Arasimowicz M. Floryszak-Wieczorek J. (2007) Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Science 172, 876 887.
3. Baluska F., Samaj J., Wojtaszek P., Volkmann D. Menzel D. (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiology 133, 482 491.
4. Berrocal-Lobo M. Molina A. (2007) Arabidopsis defense response against Fusarium oxysporum. Trends in Plant Science 13, 145 150.
5. Bhat R.G. Subbarao K.V. (1999) Host range specificity in Verticillium dahliae. Phytopathology 89, 1218 1225.
6. Binet M.N., Humbert C., Lecourieux D., Vantard M. Puginn A. (2001) Disruption of microtubular cytoskeleton induced by cryptogein, an elicitor of hypersensitive response in tobacco cells. Plant Physiology 125, 564 572.
7. Bonfoco E., Leist M., Zhivotovsky B., Orrenius S., Lipton S.A. Nicotera P. (1996) Cytoskeletal breakdown and apoptosis elicited by NO donors in cerebellar granule cells require NMDA receptor activation. Journal of Neurochemistry 67, 2484 2493.
8. 2 synthesis. The Plant Journal 45, 113 122.
9. Bruce T.J. Pickett J.A. (2007) Plant defence signaling induced by biotic attacks. Current Opinion in Plant Biology 10, 387 392.
10. 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 Pathology 51, 629 640.
11. Cameron R.K., Paiva N.L., Lamb C.J. Dixon R.A. (1999) Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiological and Molecular Plant Pathology 55, 121 130.
12. Crawford N.M., Galli M., Tischner R., Heimer Y.M., Okamoto M. Mack A. (2006) Response to Zemojtel et al.: plant nitric oxide synthase: back to square one. Trends in Plant Science 11, 526 527.
13. Delledonne M., Xia Y., Dixon R.A. Lamb C. (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585 588.
14. Delledonne M., Zeier J., Marocco A. Lamb C. (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive response. Proceedings of the National Academy of Sciences of the United States of America 98, 13454 13459.
15. Drøbak B.K., Franklin-Tong V.E. Staiger C.J. (2004) The role of the actin cytoskeleton in plant cell signaling. New Phytologist 163, 13 30.
16. Durner J. Klessig D. (1999) Nitric oxide as a signal in plants. Current Opinion in Plant Biology 2, 369 374.
17. Durner J., Wendehenne D. Klessig D.F. (1998) Defence gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceedings of the National Academy of Sciences of the United States of America 95, 10328 10333.
18. Flors V., Ton J., van Coorn R., Jakab G., Garcia-Agustin P. Mauch-Mani B. (2008) Interplay between JA, SA and ABA signaling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. The Plant Journal 54, 81 92.
19. Fradin E.F. Thomma B.P.H.J. (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Molecular Plant Pathology 7, 71 86.
20. Geitmann A., Snowmann B.N., Emons A.M. Franklin-tong V.E. (2000) Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas. The Plant Cell 12, 1239 1251.
21. Genre A. Bonfante P. (2002) Epidermal cells of a symbiosis-defective mutant of Lotus japonicus show altered cytoskeleton organization in the presence of a mycorrhizal fungus. Protoplasma 219, 43 50.
22. Grant M. Mansfield J. (1999) Early events in host-pathogen interactions. Current Opinion in Plant Biology 2, 312 317.
23. Grün S., Lindermayr C., Sell S. Durner J. (2006) Nitric oxide and gene regulation in plant. Journal of Experimental Botany 57, 507 516.
24. Guo F.Q., Okamoto M. Crawford N.M. (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signalling. Science 302, 100 103.
25. Hashimoto T. Kato T. (2006) Cortical control of plant microtubules. Current Opinion in Plant Biology 9, 5 11.
26. Hou Y.Y., Shi F.M. Li Y.Z. (2008) Verticillium dahliae toxins induce changes of a putative histone H2B and a pumilio/Puf RNA-binding protein gene expression in Arabidopsis thaliana. Journal of Plant Pathology 90, 117 120.
27. Huang X., Kiefer E., Rad U., Ernst D., Foissner I. Durner J. (2002) Nitric oxide burst and nitric oxide-dependent gene induction in plants. Plant Physiology and Biochemistry 40, 625 631.
28. 2 induced by Verticillium dahliae toxins and its influence on the expression of GST gene in cotton suspension cells. Chinese Science Bulletin 52, 1347 1354.
29. 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.
30. Kobayashi I., Kobayashi Y. Hardham A.R. (1994) Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195, 237 247.
31. Kobayashi I., Kobayashi Y., Funaki Y., Fujimoto S., Takemoto T. Kunoh H. (1997) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance response to flax rust infection. The Plant Journal 11, 525 537.
32. McGarry J.G., Klein-Nulend J. Prendergast P.J. (2005) The effect of cytoskeletal disruption on pulsatile fluid flow-induced nitric oxide and prostaglandin E2 release in osteocytes and osteoblasts. Biochemical and Biophysical Research Communications 330, 341 348.
33. MaFadden H.G., Chapple R., de Feyter R. Dennis E. (2001) Expression of pathogenesis-related genes in cotton stems in response to infection by Verticillium dahliae. Physiological and Molecular Plant Pathology 58, 119 132.
34. Mathur J. Hülskamp M. (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Current Biology 12, R669 R676.
35. 2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. The Plant Journal 29, 257 268.
36. Miklis M., Consonni C., Bhat R.A., Lipka V., Schulze-Lefert P. Panstruga R. (2007) Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiology 144, 1132 1143.
37. Mur L.A.J., Carver T.L.W. Prats E. (2006) NO way to live; the various roles of nitric oxide in plant-pathogen interactions. Journal of Experimental Botany 57, 489 505.
38. Murashige T. Skoog F. (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Physiologia Plantarum 15, 473 479.
39. Neill S.J., Desikan R. Hancock J.T. (2003) Nitric oxide signaling in plants. New Phytologist 159, 11 35.
40. Planchet E., Sonoda M., Zeier J. Kaiser W.M. (2006) Nitric oxide (NO) as an intermediate in the cryptogein-induced hypersensitive response - a critical re-evaluation. Plant, Cell & Environment 29, 59 69.
41. Polverari A., Molesini B., Pezzotti M., Buonaurio R., Marte M. Delledonne M. (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 16, 1094 1105.
42. Prats E., Mur L.A.J., Sanderson R. Carver T.L.W. (2005) Nitric oxide contributes both papilla-based resistance and the hypersensitive response in barley attacked by Blumeria graminis f. sp. hordei. Molecular Plant Pathology 6, 65 78.
43. Romero-Puertas M.C., Perazzolli M., Zago E.D. Delledonne M. (2004) Nitric oxide signaling functions in plant-pathogen interactions. Cellular Microbiology 6, 795 803.
44. Schmelzer E., Naton B., Freytag S., Rouhara I., Küster B. Hahlbrock K. (1995) Infection-induced rapid cell death in plants: a means of efficient pathogen defense. Canadian Journal of Botany-Revue Canadienne de Botanique 73, S426 S434.
45. Sedlářová M., Binarová P. Lebeda A. (2001) Changes in microtubular alignment in Lactuca spp. epidermal cells during early stages of infection by Bremia lactucae. Phyton 41, 21 34.
46. Shi F.M. Li Y.Z. (2008) Verticillium dahliae toxins-induced nitric oxide production in Arabidopsis is major dependent on nitrate reductase. Biochemistry and Molecular Biology Reports 41, 79 85.
47. Shibaoka H. (1994) Plant hormone-induced changes in the orientation of cortical microtubules. Annual Review of Plant Physiology and Plant Molecular Biology 45, 527 544.
48. Sivaguru M., Pike S., Gassmann W. Baskin T. (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant and Cell Physiology 44, 667 675.
49. Škalamera D. Heath M. (1998) Changes in the cytoskeleton accompanying infection-induced nuclear movements and the hypersensitive response in plant cells invaded by rust fungi. The Plant Journal 16, 191 200.
50. Takemoto D. Hardham A. (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiology 136, 3864 3876.
51. Takemoto D., Jones D.A. Hardham A.R. (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. The Plant Journal 33, 775 792.
52. Takemoto D., Jones D.A. Hardham A.R. (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. Molecular Plant Pathology 7, 553 563.
53. Taylor J.E., Hatcher P.E. Paul N.D. (2004) Crosstalk between plant responses to pathogens and herbivores: a view from the outside in. Journal of Experimental Botany 55, 159 168.
54. Thordal-Christensen H. (2003) Fresh insights into processes of nonhost resistance. Current Opinion in Plant Biology 6, 351 357.
55. Vandroux D., Schaeffer C., Tissier C., Lalande A., Bès S., Rochette L. Athiae P. (2004) Microtubule alteration is an early cellular reaction to the metabolic challenge in ischemic cardiomyocytes. Molecular and Cellular Biochemistry 258, 99 108.
56. Wang C., Li J. Yuan M. (2007) Salt tolerance requires cortical microtubule reorganization in Arabidopsis. Plant and Cell Physiology 48, 1534 1547.
57. Wasteneys G.O. Galway M.E. (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Annual Review of Plant Biology 54, 691 722.
58. Wasteneys G.O. Yang Z. (2004) The cytoskeleton becomes multidisciplinary. Plant Physiology 136, 3853 3854.
59. Webb J., Harvey M.W., Holden D.W. Evans T.J. (2001) Macrophage nitric oxide synthase associates with cortical actin but is not recruited to phagosomes. Infection Immunology 69, 6391 6400.
60. Williams J., Hall S.A., Hawkesford M.J., Beale M.H. Cooper R.M. (2002) Elemental sulfur and thiol accumulation in tomato and defense against a fungal vascular pathogen. Plant Physiology 128, 150 159.
61. Wilson I.D., Neill S.J. Hancock J.T. (2008) Nitric oxide synthesis and signaling in plants. Plant, Cell & Environment 31, 622 631.
62. Yuan H.Y., Jia Z.Q., Li Y. Li Y.Z. (2006) Verticillium dahliae toxin induced alterations of cytoskeletons and nucleoli in Arabidopsis suspension cells. Protoplasma 299, 75 82.
63. Yuan M., Shaw P.J., Warn R.M. Lloyd C.W. (1994) Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proceedings of the National Academy of Sciences of the United States of America 91, 6050 6053.
64. Zeier J., Delledonne M., Mishina T., Severi E., Sonoda M. Lamb C. (2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiology 136, 2875 2886.
65. Zhao M.G., Tian Q.Y. Zhang W.H. (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiology 144, 206 217.
66. Zhen X.H. Li Y.Z. (2004) Ultrastructural changes and location of β-1,3-glucanase in resistant and susceptible cotton callus cells in response to treatment with toxin of Verticillium dahliae and salicylic acid. Journal of Plant Physiology 161, 1367 1377.