Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions

Frontiers in Plant Science

Volumn 5, Issue MAY, 2014, Pages

  Bellincampi, Daniela ^a   Cervone, Felice ^a   Lionetti, Vincenzo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Cell wall; Cell wall integrity; Host cell wall metabolism reprogramming; Plant defense; Susceptibility factors

Indexed keywords

EID: 84902294433     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00228     Document Type: Review

References (100)

1. Aguero, C. B., Uratsu, S. L., Greve, C., Powell, A. L. T., Labavitch, J. M., Meredith, C. P., et al. (2005). Evaluation of tolerance to pierce's disease and botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Mol. Plant Pathol. 6, 43-51. doi: 10.1111/j.1364-3703.2004.00262.x
2. Ahmad, S., Veyrat, N., Gordon-Weeks, R., Zhang, Y. H., Martin, J., Smart, L., et al. (2011). Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol. 157, 317-327. doi: 10.1104/pp.111.180224
3. Aist, J. R. (1976). Papillae and related wound plugs of plant cells. Annu. Rev. Phytopathol. 14, 145-163. doi: 10.1146/annurev.py.14.090176.001045
4. Arancibia, R. A., and Motsenbocker, C. E. (2006). Pectin methylesterase activity in vivo differs from activity in vitro and enhances polygalacturonase-mediated pectin degradation in tabasco pepper. J. Plant Physiol. 163, 488-496. doi: 10.1016/j.jplph.2005.06.022
5. Bar, M., Sharfman, M., Ron, M., and Avni, A. (2010). BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. 63, 791-800. doi: 10.1111/j.1365-313X.2010.04282.x
6. Barcala, M., Garcia, A., Cabrera, J., Casson, S., Lindsey, K., Favery, B., et al. (2010). Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J. 61, 698-712. doi: 10.1111/j.1365-313X.2009.04098.x
7. Bechinger, C., Giebel, K. F., Schnell, M., Leiderer, P., Deising, H. B., and Bastmeyer, M. (1999). Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285, 1896-1899. doi: 10.1126/science.285.5435.1896
8. Bednarek, P., Pislewska-Bednarek, M., Svatos, A., Schneider, B., Doubsky, J., Mansurova, M., et al. (2009). A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323, 101-106. doi: 10.1126/science.1163732
9. Bellincampi, D., Camardella, L., Delcour, J. A., Desseaux, V., D'Ovidio, R., Durand, A., et al. (2004). Potential physiological role of plant glycosidase inhibitors. Biochim. Biophys. Acta 1696, 265-274. doi: 10.1016/j.bbapap.2003.10.011
10. Bethke, G., Grundman, R. E., Sreekanta, S., Truman, W., Katagiri, F., and Glazebrook, J. (2013). Arabidopsis pectin methylesterases contribute to immunity against pseudomonas syringae. Plant Physiol. 164, 1093-1107. doi: 10.1104/pp.113.227637
11. Bily, A. C., Reid, L. M., Taylor, J. H., Johnston, D., Malouin, C., Burt, A. J., et al. (2003). Dehydrodimers of ferulic acid in maize grain pericarp and aleurone: resistance factors to Fusarium graminearum. Phytopathology 93, 712-719. doi: 10.1094/PHYTO.2003.93.6.712
12. Bohlmann, H., and Sobczak, M. (2014). The plant cell wall in the feeding sites of cyst nematodes. Front. Plant Sci.5:89. doi: 10.3389/fpls.2014.00089
13. Boller, T., and He, S. Y. (2009). Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324, 742-744. doi: 10.1126/science.1171647
14. Brutus, A., Sicilia, F., Macone, A., Cervone, F., and De Lorenzo, G. (2010). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Sci. U.S.A. 107, 9452-9457. doi: 10.1073/pnas.1000675107
15. Buttner, D., and He, S. Y. (2009). Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150, 1656-1664. doi: 10.1104/pp.109.139089
16. Cano-Delgado, A., Penfield, S., Smith, C., Catley, M., and Bevan, M. (2003). Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J. 34, 351-362. doi: 10.1046/j.1365-313X.2003.01729.x
17. Cantu, D., Blanco-Ulate, B., Yang, L., Labavitch, J. M., Bennett, A. B., and Powell, A. L. T. (2009). Ripening-regulated susceptibility of tomato fruit to botrytis cinerea requires nor but not rin or ethylene. Plant Physiol. 150, 1434-1449. doi: 10.1104/pp.109.138701
18. Cantu, D., Vicente, A. R., Greve, L. C., Dewey, F. M., Bennett, A. B., Labavitch, J. M., et al. (2008a). The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proc. Natl. Acad. Sci. U.S.A.105, 859-864. doi: 10.1073/pnas.0709813105
19. Cantu, D., Vicente, A. R., Labavitch, J. M., Bennett, A. B., and Powell, A. L. (2008b). Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends Plant Sci. 13, 610-617. doi: 10.1016/j.tplants.2008.09.002
20. Caprari, C., Bergmann, C., Migheli, Q., Salvi, G., Albersheim, P., Darvill, A., et al. (1993). Fusarium moniliformesecretes four endopolygalacturonases derived from a single gene product. Physiol. Mol. Plant Pathol. 43, 453-462. doi: 10.1006/pmpp.1993.1073
21. Celio, G. J., Mims, C. W., and Richardson, E. A. (2004). Ultra-structure and immuno cytochemistry of the host-pathogen interface in poinsettia leaves infected with powdery mildew. Can. J. Bot. 82, 421-429. doi: 10.1139/b04-019
22. Chassot, C., and Metraux, J. P. (2005). The cuticle as source of signals for plant defense. Plant Biosyst. 139, 28-31. doi: 10.1080/11263500500056344
23. Chassot, C., Nawrath, C., and Metraux, J. P. (2007). Cuticular defects lead to full immunity to a major plant pathogen. Plant J. 49, 972-980. doi: 10.1111/j.1365-313X.2006.03017.x
24. Chen, M. H., Sheng, J., Hind, G., Handa, A. K., and Citovsky, V. (2000). Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J.19, 913-920. doi: 10.1093/emboj/19.5.913
25. D'Ovidio, R., Mattei, B., Roberti, S., and Bellincampi, D. (2004). Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Biochim. Biophys. Acta 1696, 237-244. doi: 10.1016/j.bbapap.2003.08.012
26. Dangl, J. L., Horvath, D. M., and Staskawicz, B. J. (2013). Pivoting the plant immune system from dissection to deployment. Science 341, 746-751. doi: 10.1126/science.1236011
27. Daudi, A., Cheng, Z. Y., O'Brien, J. A., Mammarella, N., Khan, S., Ausubel, F. M., et al. (2012). The apoplastic oxidative burst peroxidase in arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24, 275-287. doi: 10.1105/tpc.111.093039
28. Davis, E. L., Hussey, R. S., and Baum, T. J. (2004). Getting to the roots of parasitism by nematodes. Trends Parasitol. 20, 134-141. doi: 10.1016/j.pt.2004.01.005
29. Davis, E. L., Hussey, R. S., Mitchum, M. G., and Baum, T. J. (2008). Parasitism proteins in nematode-plant interactions. Curr. Opin. Plant Biol. 11, 360-366. doi: 10.1016/j.pbi.2008.04.003
30. Deepak, S., Shailasree, S., Kini, R. K., Muck, A., Mithofer, A., and Shetty, S. H. (2010). Hydroxyproline-rich glycoproteins and plant defense. J. Phytopathol. 158, 585-593. doi: 10.1111/j.1439-0434.2010.01669.x
31. De Lorenzo, G., Brutus, A., Savatin, D. V., Sicilia, F., and Cervone, F. (2011). Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett. 585, 1521-1528. doi: 10.1016/j.febslet.2011.04.043
32. Di Matteo, A., Giovane, A., Raiola, A., Camardella, L., Bonivento, D., De Lorenzo, G., et al. (2005). Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17, 849-858. doi: 10.1105/tpc.104.028886
33. Dorokhov, Y. L., Komarova, T. V., Petrunia, I. V., Frolova, O. Y., Pozdyshev, D. V., and Gleba, Y. Y. (2012). Airborne signals from a wounded leaf facilitate viral spreading and induce antibacterial resistance in neighboring plants. PLoS Pathog. 8:e1002640. doi: 10.1371/journal.ppat.1002640
34. Ellinger, D., Naumann, M., Falter, C., Zwikowics, C., Jamrow, T., Manisseri, C., et al. (2013). Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol. 161, 1433-1444. doi: 10.1104/pp.112.211011
35. 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. doi: 10.1105/tpc.002022
36. Ellis, C., and Turner, J. G. (2001). The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13, 1025-1033. doi: 10.1105/tpc.13.5.1025
37. Eynck, C., Seguin-Swartz, G., Clarke, W. E., and Parkin, I. A. P. (2012). Monolignol biosynthesis is associated with resistance to Sclerotinia sclerotiorum in Camelina sativa. Mol. Plant Pathol. 13, 887-899. doi: 10.1111/j.1364-3703.2012.00798.x
38. Feng, J., Wang, F., Hughes, G. R., Kaminskyj, S., and Wei, Y. D. (2011). An important role for secreted esterase in disease establishment of the wheat powdery mildew fungus Blumeria graminis f. sp tritici. Can. J. Microbiol. 57, 211-216. doi: 10.1139/W10-120
39. Ferrari, S., Galletti, R., Pontiggia, D., Manfredini, C., Lionetti, V., Bellincampi, D., et al. (2008). Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol. 146, 669-681. doi: 10.1104/pp.107.109686
40. Ferrari, S., Savatin, D. V., Sicilia, F., Gramegna, G., Cervone, F., and De Lorenzo, G. (2013). Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 4:49. doi: 10.3389/fpls.2013.00049
41. Ferrari, S., Sella, L., Janni, M., Favaron, F., and D'Ovidio, R. (2012). Transgenic expression of polygalacturonase-inhibiting proteins in Arabidopsis and wheat increases resistance to the flower pathogen Fusarium graminearum. Plant Biol. (Stuttg.) 14, 31-38. doi: 10.1111/j.1438-8677.2011.00449.x
42. Flors, V., Leyva, M. D., Vicedo, B., Finiti, I., Real, M. D., Garcia-Agustin, P., et al. (2007). Absence of the endo-beta-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. Plant J. 52, 1027-1040. doi: 10.1111/j.1365-313X.2007.03299.x
43. Flors, V., Ton, J., van Doorn, R., Jakab, G., Garcia-Agustin, P., and Mauch-Mani, B. (2008). Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J. 54, 81-92. doi: 10.1111/j.1365-313X.2007.03397.x
44. Gallego-Giraldo, L., Jikumaru, Y., Kamiya, Y., Tang, Y. H., and Dixon, R. A. (2011). Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytol. 190, 627-639. doi: 10.1111/j.1469-8137.2010.03621.x
45. Galletti, R., Denoux, C., Gambetta, S., Dewdney, J., Ausubel, F. M., De Lorenzo, G., et al. (2008). The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol. 148, 1695-1706. doi: 10.1104/pp.108.127845
46. Gille, S., and Pauly, M. (2012). O-acetylation of plant cell wall polysaccharides. Front. Plant Sci. 3:12. doi: 10.3389/fpls.2012.00012
47. Giraldo, M. C., and Valent, B. (2013). Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11, 800-814. doi: 10.1038/nrmicro3119
48. Hamann, T. (2012). Plant cell wall integrity maintenance as an essential component of biotic stress response mechanisms. Front. Plant Sci. 3:77. doi: 10.3389/fpls.2012.00077
49. Hauck, P., Thilmony, R., and He, S. Y. (2003). A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. U.S.A. 100, 8577-8582. doi: 10.1073/pnas.1431173100
50. Hematy, K., Sado, P. E., Van Tuinen, A., Rochange, S., Desnos, T., Balzergue, S., et al. (2007). A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17, 922-931. doi: 10.1016/j.cub.2007.05.018
51. Herbert, C., O'Connell, R., Gaulin, E., Salesses, V., Esquerre-Tugaye, M. T., and Dumas, B. (2004). Production of a cell wall-associated endopolygalacturonase by Colletotrichum lindemuthianum and pectin degradation during bean infection. Fungal Genet. Biol. 41, 140-147. doi: 10.1016/j.fgb.2003.09.008
52. Hernandez-Blanco, C., Feng, D. X., Hu, J., Sanchez-Vallet, A., Deslandes, L., Llorente, F., et al. (2007). Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19, 890-903. doi: 10.1105/tpc.106.048058
53. Hewezi, T., Howe, P., Maier, T. R., Hussey, R. S., Mitchum, M. G., Davis, E. L., et al. (2008). Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20, 3080-3093. doi: 10.1105/tpc.108.063065
54. Hok, S., Attard, A., and Keller, H. (2010). Getting the most from the host: how pathogens force plants to cooperate in disease. Mol. Plant Microbe Interact. 23, 1253-1259. doi: 10.1094/MPMI-04-10-0103
55. Jacobs, A. K., Lipka, V., Burton, R. A., Panstruga, R., Strizhov, N., Schulze-Lefert, P., et al. (2003). An Arabidopsiscallose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15, 2503-2513. doi: 10.1105/tpc.016097
56. Juge, N. (2006). Plant protein inhibitors of cell wall degrading enzymes. Trends Plant Sci. 11, 359-367. doi: 10.1016/j.tplants.2006.05.006
57. King, B. C., Waxman, K. D., Nenni, N. V., Walker, L. P., Bergstrom, G. C., and Gibson, D. M. (2011). Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnol. Biofuels 4:4. doi: 10.1186/1754-6834-4-4
58. Komarova, T. V., Sheshukova, E. V., and Dorokhov, Y. L. (2014). Cell wall methanol as a signal in plant immunity. Front. Plant Sci. 5:101. doi: 10.3389/fpls.2014.00101
59. Laluk, K., and Mengiste, T. (2010). Necrotroph attacks on plants: wanton destruction or covert extortion?Arabidopsis Book 8:e0136. doi: 10.1199/tab.0136
60. Lionetti, V., Cervone, F., and Bellincampi, D. (2012). Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. J. Plant Physiol. 169, 1623-1630. doi: 10.1016/j.jplph.2012.05.006
61. Lionetti, V., Raiola, A., Camardella, L., Giovane, A., Obel, N., Pauly, M., et al. (2007). Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol. 143, 1871-1880. doi: 10.1104/pp.106.090803
62. Lionetti, V., Raiola, A., Cervone, F., and Bellincampi, D. (2013). Transgenic expression of pectin methylesterase inhibitors limits tobamovirus spread in tobacco and Arabidopsis. Mol. Plant Pathol. 15, 265-274. doi: 10.1111/mpp.12090
63. 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 fungusPlectosphaerella cucumerina. Plant J. 43, 165-180. doi: 10.1111/j.1365-313X.2005.02440.x
64. Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B., and Ton, J. (2011). Callose deposition: a multifaceted plant defense response. Mol. Plant Microbe Interact. 24, 183-193. doi: 10.1094/MPMI-07-10-0149
65. Manabe, Y., Nafisi, M., Verhertbruggen, Y., Orfila, C., Gille, S., Rautengarten, C., et al. (2011). Loss-of-function mutation of reduced wall acetylation2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol. 155, 1068-1078. doi: 10.1104/pp.110.168989
66. Mattei, B., Raiola, A., Caprari, C., Federici, L., Bellincampi, D., De Lorenzo, G., et al. (2002) "Studies on plant inhibitors of pectin modifying enzymes: polygalacturonase-inhibiting protein (PGIP) and pectin methylesterase inhibitor (PMEI), " in Carbohydrate Bioengineering Interdisciplinary approaches, eds T. T. Teeri, B. Svensson, H. J. Gilbert, and T. Feizi (CambridgeRoyal Society of Chemistry), 160-167.
67. Moscetti, I., Tundo, S., Janni, M., Sella, L., Gazzetti, K., Tauzin, A., et al. (2013). Constitutive expression of the xylanase inhibitor TAXI-III delays fusarium head blight symptoms in durum wheat transgenic plants. Mol. Plant Microbe Interact. 26, 1464-1472. doi: 10.1094/MPMI-04-13-0121-R
68. Noda, J., Brito, N., and González, C. (2010). The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol. 10, 1-15 doi: 10.1186/1471-2229-10-38
69. O'Brien, J. A., Daudi, A., Butt, V. S., and Bolwell, G. P. (2012). Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236, 765-779. doi: 10.1007/s00425-012-1696-9
70. Passardi, F., Penel, C., and Dunand, C. (2004). Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci. 9, 534-540. doi: 10.1016/j.tplants.2004.09.002
71. Pogorelko, G., Lionetti, V., Bellincampi, D., and Zabotina, O. (2013a). Cell wall integrity: Targeted post-synthetic modifications to reveal its role in plant growth and defense against pathogens. Plant Signal. Behav. 8, 1-8. doi: 10.4161/psb.25435
72. Pogorelko, G., Lionetti, V., Fursova, O., Sundaram, R. M., Qi, M. S., Whitham, S. A., et al. (2013b). Arabidopsis andBrachypodium distachyon transgenic plants expressing Aspergillus nidulans acetylesterases have decreased degree of polysaccharide acetylation and increased resistance to pathogens. Plant Physiol. 162, 9-23. doi: 10.1104/pp.113.214460
73. Prins, T. W., Tudzynski, P., Von Tiedemann, A., Tudzynski, B., ten Have, A., Hansen, M. E., et al. (2000). "Infection strategies of Botrytis cinerea and related necrotrophic pathogens, " in Fungal Pathology, ed. J. Kronstad (Dordrecht: Kluwer Academic Publishers), 33-64. doi: 10.1007/978-94-015-9546-9_2
74. Raiola, A., Camardella, L., Giovane, A., Mattei, B., De Lorenzo, G., Cervone, F., et al. (2004). Two Arabidopsis thaliana genes encode functional pectin methylesterase inhibitors. FEBS Lett. 557, 199-203. doi: 10.1016/S0014-5793(03)01491-1
75. Raiola, A., Lionetti, V., Elmaghraby, I., Immerzeel, P., Mellerowicz, E. J., Salvi, G., et al. (2011). Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol. Plant Microbe Interact. 24, 432-440. doi: 10.1094/MPMI-07-10-0157
76. Ramirez, V., Agorio, A., Coego, A., Garcia-Andrade, J., Hernandez, M. J., Balaguer, B., et al. (2011). MYB46 modulates disease susceptibility to Botrytis cinerea in Arabidopsis. Plant Physiol. 155, 1920-1935. doi: 10.1104/pp.110.171843
77. Reca, I. B., Lionetti, V., Camardella, L., D'Avino, R., Giardina, T., Cervone, F., et al. (2012). A functional pectin methylesterase inhibitor protein (SolyPMEI) is expressed during tomato fruit ripening and interacts with PME-1. Plant Mol. Biol. 79, 429-442. doi: 10.1007/s11103-012-9921-2
78. Rocchi, V., Janni, M., Bellincampi, D., Giardina, T., and D'Ovidio, R. (2011). Intron retention regulates the expression of pectin methylesterase inhibitor (Pmei) genes during wheat growth and development. Plant Biol. 14, 365-373. doi: 10.1111/j.1438-8677.2011.00508.x
79. Ron, M., and Avni, A. (2004). The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16, 1604-1615. doi: 10.1105/tpc.022475
80. Sanchez-Rodriguez, C., Estevez, J. M., Llorente, F., Hernandez-Blanco, C., Jorda, L., Pagan, I., et al. (2009). The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in Arabidopsis thaliana. Mol. Plant Microbe Interact. 22, 953-963. doi: 10.1094/MPMI-22-8-0953
81. Sattler, S. E., and Funnell-Harris, D. L. (2013). Modifying lignin to improve bioenergy feedstocks: strengthening the barrier against pathogens? Front. Plant Sci. 4:70. doi: 10.3389/fpls.2013.00070
82. Sella, L., Gazzetti, K., Faoro, F., Odorizzi, S., D'Ovidio, R., Schafer, W., et al. (2013). A Fusarium graminearumxylanase expressed during wheat infection is a necrotizing factor but is not essential for virulence. Plant Physiol. Biochem. 64, 1-10. doi: 10.1016/j.plaphy.2012.12.008
83. Spadoni, S., Zabotina, O., Di Matteo, A., Mikkelsen, J. D., Cervone, F., DL, G., et al. (2006). Polygalacturonase-inhibiting protein (PGIP) interacts with pectin through a binding site formed by four clustered residues of arginine and lysine. Plant Physiol. 141, 557-564. doi: 10.1104/pp.106.076950
84. Taurino, M., Abelenda, J. A., Rio-Alvarez, I., Navarro, C., Vicedo, B., Farmaki, T., et al. (2014). Jasmonate-dependent modifications of the pectin matrix during potato development function as a defense mechanism targeted by Dickeya dadantii virulence factors. Plant J. 77, 418-429. doi: 10.1111/tpj.12393
85. Ton, J., and Mauch-Mani, B. (2004). Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 38, 119-130. doi: 10.1111/j.1365-313X.2004.02028.x
86. Udatha, D. B. R. K., Mapelli, V., Panagiotou, G., and Olsson, L. (2012). Common and distant structural characteristics of feruloyl esterase families from Aspergillus oryzae. PLoS ONE 7:e39473. doi: 10.1371/journal.pone.0039473
87. Underwood, W. (2012). The plant cell wall: a dynamic barrier against pathogen invasion. Front. Plant Sci. 3:85. doi: 10.3389/fpls.2012.00085
88. Vanholme, B., De Meutter, J., Tytgat, T., Van Montagu, M., Coomans, A., and Gheysen, G. (2004). Secretions of plant-parasitic nematodes: a molecular update. Gene 332, 13-27. doi: 10.1016/j.gene.2004.02.024
89. 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. doi: 10.1105/tpc.003509
90. 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. doi: 10.1111/j.1365-313X.2004.02264.x
91. Voigt, C. A. (2014). Callose-mediated resistance to pathogenic intruders in plant defense-related papillae. Front. Plant Sci. 5:168. doi: 10.3389/fpls.2014.00168
92. Volpi, C., Janni, M., Lionetti, V., Bellincampi, D., Favaron, F., and D'Ovidio, R. (2011). The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol. Plant Microbe Interact. 24, 1012-1019. doi: 10.1094/MPMI-01-11-0021
93. Wieczorek, K., Golecki, B., Gerdes, L., Heinen, P., Szakasits, D., Durachko, D. M., et al. (2006). Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J. 48, 98-112. doi: 10.1111/j.1365-313X.2006.02856.x
94. Wieczorek, K., Hofmann, J., Blochl, A., Szakasits, D., Bohlmann, H., and Grundler, F. M. W. (2008). Arabidopsisendo-1,4-beta-glucanases are involved in the formation of root syncytia induced by Heterodera schachtii. Plant J.53, 336-351. doi: 10.1111/j.1365-313X.2007.03340.x
95. Williamson, V. M., and Kumar, A. (2006). Nematode resistance in plants: the battle underground. Trends Genet. 22, 396-403. doi: 10.1016/j.tig.2006.05.003
96. Wilson, R. A., and Talbot, N. J. (2009). Under pressure: investigating the biology of plant infection byMagnaporthe oryzae. Nat. Rev. Microbiol. 7, 185-195. doi: 10.1038/nrmicro2032
97. Xu, L., Zhu, L. F., Tu, L. L., Liu, L. L., Yuan, D. J., Jin, L., et al. (2011). Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J. Exp. Bot. 62, 5607-5621. doi: 10.1093/jxb/err245
98. Zhang, L., Kars, I., Essenstam, B., Liebrand, T. W., Wagemakers, L., Elberse, J., et al. (2014). Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein responsiveness to Botrytis polygalacturonases1. Plant Physiol. 164, 352-364. doi: 10.1104/pp.113.230698
99. Zhao, Z. T., Liu, H. Q., Wang, C. F., and Xu, J. R. (2013). Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14:274. doi: 10.1186/1471-2164-14-274
100. Zhong, R., Richardson, E. A., and Ye, Z. H. (2007). The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19, 2776-2792. doi: 10.1105/tpc.107.053678