Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance

Plant Cell

Volumn 19, Issue 3, 2007, Pages 890-903

  Hernández Blanco, Camilo ^a   Feng, Dong Xin ^b,e   Hu, Jian ^b,f   Sánchez Vallet, Andrea ^a   Deslandes, Laurent ^b   Llorente, Francisco ^a   Berrocal Lobo, Marta ^c,g   Keller, Harald ^b   Barlet, Xavier ^b   Sánchez Rodríguez, Clara ^a   Anderson, Lisa K ^d   Somerville, Shauna ^c   Marco, Yves ^b   Molinaa, Antonio ^a  

^a Electrotechnical Section   (Spain)

^b CNRS   (France)

^c GEOPHYSICAL LABORATORY   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e INSTITUTE OF PLANT PROTECTION   (China)

^f CHINA AGRICULTURAL UNIVERSITY   (China)

^g UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DISEASES; SYNTHESIS (CHEMICAL);

CELL WALL; CELLULOSE SYNTHASES; DEFENSE PATHWAYS;

CELLULOSE;

CELLS; CELLULOSE; DISEASES; SYNTHESIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); FUNGI; PLECTOSPHAERELLA CUCUMERINA; RALSTONIA SOLANACEARUM;

EID: 34250762011     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.106.048058     Document Type: Article

References (75)

1. AbuQamar, S., Chen, X., Dhawan, R., Bluhm, B., Salmeron, J., Lam, S., Dietrich, R.A., and Mengiste, T. (2006). Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J. 48: 28-44.
2. Aldon, D., Brito, B., Boucher, C., and Genin, S. (2000). A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes. EMBO J. 10: 2304-2314.
3. Anderson, J.P., Badruzsaufari, E., Schenk, P.M., Manners, J.M., Desmond, O.J., Ehlert, C., Maclean, D.J., Ebert, P.R., and Kazan, K. (2004). Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16: 3460-3479.
4. Audenaert, K., De Meyer, G.B., and Hofte, M.M. (2002). Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128: 491-501.
5. Bartsch, M., Gobbato, E., Bednarek, P., Debey, S., Schultze, J.L., Bautor, J., and Parker, J.E. (2006). Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18: 1038-1051.
6. Baudoin, N., Serizet, C., Gosti, F., and Giraudat, J. (2000). Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12: 1103-1115.
7. Berrocal-Lobo, M., Molina, A., and Solano, R. (2002a). Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 29: 23-32.
8. Berrocal-Lobo, M., Segura, A., Moreno, M., Lopez, G., Garcia-Olmedo, F., and Molina, A. (2002b). Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol. 128: 951-961.
9. Boucher, C.A., Barberis, P.A., Trigalet, A.P., and Demery, D.A.J. (1985). Transposon mutagenesis of Pseudomonas solanacearum: Isolation of Tn5-induced virulent mutants. J. Gen. Microbiol. 131: 2449-2457.
10. Brown, D.M., Zeef, L.A., Ellis, J., Goodacre, R., and Turner, S.R. (2005). Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17: 2281-2295.
11. Cao, H., Bowling, S.A., Gordon, A.S., and Dong, X. (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592.
12. Capella, A.N., Menossi, M., Arruda, P., and Benedetti, C.E. (2001). COI1 affects myrosinase activity and controls the expression of two flower-specific myrosinase-binding protein homologues in Arabidopsis. Planta 213: 691-699.
13. Carpita, N.C., and McCann, M. (2000). The cell wall. In Biochemistry and Molecular Biology of Plants, B. Buchanan, W. Gruissem, and R.L. Jones, eds (Rockville, MD: American Society of Plant Physiologists), pp. 52-108.
14. Celenza, J.L., Quiel, J.A., Smolen, G.A., Merrikh, H., Silvestro, A.R., Normanly, J., and Bender, J. (2005). The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol. 137: 253-262.
15. Chen, Z., Hong, X., Zhang, H., Wang, Y., Li, X., Zhu, J.K., and Gong, Z. (2005). Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J. 43: 273-283.
16. Dangl, J.L., Ritter, C., Gibbon, M.J., Mur, L.A., Wood, J.R., Gross, S., Mansfield, J., and Taylor, J.D. (1992). Functional homologs of the Arabidopsis RPM1 disease resistance gene in bean and pea. Plant Cell 4: 1359-1369.
17. Deslandes, L., Olivier, J., Peeters, N., Feng, D.X., Khounlotham, M., Boucher, C., Somssich, I., Genin, S., and Marco, Y. (2003). Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. USA 100: 8024-8029.
18. Deslandes, L., Pileur, F., Liaubet, L., Camut, S., Can, C., Williams, K., Holub, E, Beynon, J., Arlat, M., and Marco, Y. (1998). Genetic characterization of RRS1, a recessive locus in Arabidopsis thaliana that confers resistance to the bacterial soilborne pathogen Ralstonia solanacearum. Mol. Plant Microbe Interact. 11: 659-667.
19. Desprez, T., Vernhettes, S., Fagard, M., Refregier, G., Desnos, T., Aletti, E., Py, H., Pelletier, S., and Hofte, H. (2002). Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol. 128: 482-490.
20. Ellis, C., Karafyllidis, I., Wasternack, C., and Turner, J.G. (2002). The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14: 1557-1566.
21. Epple, P., Apel, K., and Bohlmann, H. (1997). Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell 9: 509-520.
22. Facchini, P.J., and St-Pierre, B. (2005). Synthesis and trafficking of alkaloid biosynthetic enzymes. Curr. Opin. Plant Biol. 8: 657-666.
23. Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S., and Hofte, H. (2000). PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12: 2409-2424.
24. Feys, B., Benedetti, C.E., Penfold, C.N., and Turner, J.G. (1994). Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751-759.
25. García-Olmedo, F., Molina, A., Alamillo, J.M., and Rodriguez-Palenzuela, P. (1998). Plant defense peptides. Biopolymers 47: 479-491.
26. Glazebrook, J. (2001). Genes controlling expression of defense responses in Arabidopsis. Curr. Opin. Plant Biol. 4: 301-308.
27. Godiard, L., Sauviac, L., Torii, K.U., Grenon, O.,Mangin, B., Grimsley, N.L., and Marco, Y. (2004). ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J. 36: 353-365.
28. Gosti, F., Beaudoin, N., Serizet, C., Webb, A.A., Vartanian, N., and Giraudat, J. (1999). ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11: 1897-1910.
29. Grubb, C.D., and Abel, S. (2006). Glucosinolate metabolism and its control. Trends Plant Sci. 11: 89-100.
30. Hirsch, J., Deslandes, L., Feng, D.X., Balagué, C., and Marco, Y. (2002). Delayed symptom development in ein2-1, an Arabidopsis ethylene-insensitive mutant, in response to bacterial wilt caused by Ralstonia solanacearum. Phytopathology 92: 1142-1148.
31. Hu, X., and Reddy, A.S. (1997). Cloning and expression of a PR5-like protein from Arabidopsis: Inhibition of fungal growth by bacterially expressed protein. Plant Mol. Biol. 34: 949-959.
32. Jorda, L., Coego, A., Conejero, V., and Vera, P. (1999). A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. J. Biol. Chem. 274: 2360-2365.
33. Kappers, I.F., Aharoni, A., van Herpen, T.W., Luckerhoff, L.L., Dicke, M., and Bouwmeester, H.J. (2005). Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309: 2070-2072.
34. Kliebenstein, D.J., Kroymann, J., and Mitchell-Olds, T. (2005). The glucosinolate-myrosinase system in an ecological and evolutionary context. Curr. Opin. Plant Biol. 8: 264-271.
35. Kliebenstein, D.J., Rowe, H.C., and Denby, K.J. (2005). Secondary metabolites influence Arabidopsis/Botrytis interactions: Variation in host production and pathogen sensitivity. Plant J. 44: 25-36.
36. Lawton, K., Weymann, K., Friedrich, L., Vernooij, B., Uknes, S., and Ryals, J. (1995). Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol. Plant Microbe Interact. 8: 863-870.
37. Lipka, V., et al. (2005). Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183.
38. Llorente, F., Alonso-Blanco, C., Sanchez-Rodriguez, C., Jorda, L., and Molina, A. (2005). ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J. 43: 165-180.
39. Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., and Solano, R. (2004). JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938-1950.
40. Lukowitz, W., Gillmor, C.S., and Scheible, W.R. (2000). Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 123: 795-805.
41. Lummerzheim, M., Kroj, T., Ferreira, M., Tronchet, M., Godard, F., Van Montagu, M., and Roby, D. (2004). An Arabidopsis mutant with altered hypersensitive response to Xanthomonas campestris pv. campestris, hxc1, displays a complex pathophenotype. Mol. Plant Pathol. 5: 453-464.
42. Mauch-Mani, B., and Mauch, F. (2005). The role of abscisic acid in plant-pathogen interactions. Curr. Opin. Plant Biol. 8: 409-414.
43. Melotto, M., Underwood, W., Koczan, J., Nomura, K., and He, S.Y. (2006). Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980.
44. Mengiste, T., Chen, X., Salmeron, J., and Dietrich, R. (2003). The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15: 2551-2565.
45. Merchan, S., Bernal, D., Serrano, R., and Yenush, L. (2004). Response of the Saccharomyces cerevisiae Mpk1 mitogen-activated protein kinase pathway to increases in internal turgor pressure caused by loss of Ppz protein phosphatases. Eukaryot. Cell 3: 100-107.
46. Molina, A., Ahl-Goy, P., Fraile, A., Sanchez-Monge, R., and Garcia-Olmedo, F. (1993a). Inhibition of bacterial and fungal plant pathogens by thionins of types I and II. Plant Sci. 92: 169-177.
47. Molina, A., and García-Olmedo, F. (1997). Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J. 12: 669-675.
48. Molina, A., Segura, A., and García-Olmedo, F. (1993b). Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett. 316: 119-122.
49. Niyogi, K.K., and Fink, G.R. (1992). Two anthranilate synthase genes in Arabidopsis: Defense-related regulation of the tryptophan pathway. Plant Cell 4: 721-733.
50. Niyogi, K.K., Grossman, A.R., and Bjorkman, O. (1998). Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134.
51. Pandey, S., Chen, J.G., Jones, A.M., and Assmann, S.M. (2006). G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol. 141: 243-256.
52. Park, J.M., Park, C.-H., Lee, S.-B., Hamd, B.-K., Shin, R., and Paek, K.-H. (2001). Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13: 1035-1046.
53. Persson, S., Wei, H., Milne, J., Page, G.P., and Somerville, C.R. (2005). Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc. Natl. Acad. Sci. USA 102: 8633-8638.
54. Philip, B., and Levin, D.E. (2001). Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol. Cell. Biol. 21: 271-280.
55. Roman, G., Lubarsky, B., Kieber, J.J., Rothenberg, M., and Ecker, J.R. (1995). Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: Five novel mutant loci integrated into a stress response pathway. Genetics 139: 1393-1409.
56. Scheible, W.R., Eshed, R., Richmond, T., Delmer, D., and Somervillle, C.R. (2001). Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis ixr1 mutants. Proc. Natl. Acad. Sci. USA 98: 10079-10084.
57. Schulze-Lefert, P. (2004). Knocking on the heaven's wall: Pathogenesis of and resistance to biotrophic fungi at the cell wall. Curr. Opin. Plant Biol. 7: 377-383.
58. Segura, A., Moreno, M., and Garcia-Olmedo, F. (1993). Purification and antipathogenic activity of lipid transfer proteins (LTPs) from the leaves of Arabidopsis and spinach. FEBS Lett. 332: 243-246.
59. Shinozaki, K., Yamaguchi-Shinozaki, K., and Seki, M. (2003). Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol. 6: 410-417.
60. Somerville, C.R., et al. (2004). Toward a systems approach to understanding plant cell walls. Science 306: 2206-2211.
61. Staswick, P.E., Su, W., and Howell, S.H. (1992). Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. USA 89: 6837-6840.
62. Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B.H., Molina, A., Schulze-Lefert, P., Lipka, V., and 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.
63. Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K., and Turner, S.R. (2003). Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl. Acad. Sci. USA 100: 1450-1455.
64. Titarenko, E., Lopez-Solanilla, E., Garcia-Olmedo, F., and Rodriguez-Palenzuela, P. (1997). Mutants of Ralstonia (Pseudomonas) solanacearum sensitive to antimicrobial peptides are altered in their lipopolysaccharide structure and are avirulent in tobacco. J. Bacteriol. 179: 6699-6704.
65. Ton, J., Jakab, G., Toquin, V., Flors, V., Iavicoli, A., Maeder, M.N., Metraux, J.P., and Mauch-Mani, B. (2005). Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17: 987-999.
66. Ton, J., and Mauch-Mani, B. (2004). Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant J. 38: 119-130.
67. Turner, S., and Hall, M. (2000). The gapped xylem mutant identifies a common regulatory step in secondary cell wall deposition. Plant J. 24: 477-488.
68. Vogel, J., and Somerville, S. (2000). Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc. Natl. Acad. Sci. USA 97: 1897-1902.
69. Vogel, J.P., Raab, T.K., Schiff, C., and Somerville, S.C. (2002). PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14: 2095-2106.
70. Vogel, J.P., Raab, T.K., Somerville, C.R., and Somerville, S.C. (2004). Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J. 40: 968-978.
71. Weyman, P.D., Pan, Z., Feng, Q., Gilchrist, D.G., and Bostock, R.M. (2005). A circadian rhythm-regulated tomato gene is induced by arachidonic acid and Phytophthora infestans infection. Plant Physiol. 140: 235-248.
72. Wildermuth, M.C., Dewdney, J., Wu, G., and Ausubel, F.M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565.
73. Williamson, J.D., Stoop, J.M., Massel, M.O., Conkling, M.A., and Pharr, D.M. (1995). Sequence analysis of a mannitol dehydrogenase cDNA from plants reveals a function for the pathogenesis-related protein ELI3. Proc. Natl. Acad. Sci. USA 92: 7148-7152.
74. Xiong, L., Ishitani, M., Lee, H., and Zhu, J.K. (2001). The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13: 2063-2083.
75. Zhu, Y., et al. (2003). Identification of Arabidopsis rat mutants. Plant Physiol. 132: 494-505.