Wounding in the plant tissue: The defense of a dangerous passage

Frontiers in Plant Science

Volumn 5, Issue SEP, 2014, Pages

  Savatin, Daniel V ^a   Gramegna, Giovanna ^a   Modesti, Vanessa ^a   Cervone, Felice ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Jasmonate; Oligogalacturonides; Systemin; Wound response; Wounding

Indexed keywords

EID: 84908191790     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00470     Document Type: Article

References (179)

1. Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783-801. doi: 10.1016/j.cell.2006.02.015
2. Andreou, A., and Feussner, I. (2009). Lipoxygenases - structure and reaction mechanism. Phytochemistry 70, 1504-1510. doi: 10.1016/j.phytochem.2009.05.008
3. Arimura, G., Kost, C., and Boland, W. (2005). Herbivore-induced, indirect plant defenses. Biochim. Biophys. Acta1734, 91-111. doi: 10.1016/j.bbalip.2005.03.001
4. Asahina, M., Azuma, K., Pitaksaringkarn, W., Yamazaki, T., Mitsuda, N., Ohme-Takagi, M.,et al. (2011). Spatially selective hormonal control of RAP2.6L and ANAC071 transcription factors involved in tissue reunion inArabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 16128-16132. doi: 10.1073/pnas.1110443108
5. Asahina, M., Iwai, H., Kikuchi, A., Yamaguchi, S., Kamiya, Y., Kamada, H.,et al. (2002). Gibberellin produced in the cotyledon is required for cell division during tissue reunion in the cortex of cut cucumber and tomato hypocotyls. Plant Physiol. 129, 201-210. doi: 10.1104/pp.010886
6. Bartels, S., Lori, M., Mbengue, M., van Verk, M., Klauser, D., Hander, T.,et al. (2013). The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J. Exp. Bot. 64, 5309-5321. doi: 10.1093/jxb/ert330
7. Baydoun, E. A. H., and Fry, S. C. (1985). The immobility of pectic substances in injured tomato leaves and its bearing on the identity of the wound hormone. Planta 165, 269-276. doi: 10.1007/BF00395050
8. Bellincampi, D., Cardarelli, M., Zaghi, D., Serino, G., Salvi, G., Gatz, C.,et al. (1996). Oligogalacturonides prevent rhizogenesis in rol B transformed tobacco explants by inhibiting auxin-induced expression of the rol B gene. Plant Cell 8, 477-487. doi: 10.1105/tpc.8.3.477
9. Bellincampi, D., Cervone, F., and Lionetti, V. (2014). Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Front. Plant Sci. 5:228. doi: 10.3389/fpls.2014.00228
10. Bellincampi, D., Dipierro, N., Salvi, G., Cervone, F., and De Lorenzo, G. (2000). Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol. 122, 1379-1385. doi: 10.1104/pp.122.4.1379
11. Beneloujaephajri, E., Costa, A., L'Haridon, F., Metraux, J. P., and Binda, M. (2013). Production of reactive oxygen species and wound-induced resistance in Arabidopsis thaliana against Botrytis cinerea are preceded and depend on a burst of calcium. BMC Plant Biol. 13:160. doi: 10.1186/1471-2229-13-160
12. Benikhlef, L., L'Haridon, F., Abou-Mansour, E., Serrano, M., Binda, M., Costa, A.,et al. (2013). Perception of soft mechanical stress in Arabidopsis leaves activates disease resistance. BMC Plant Biol. 13:133. doi: 10.1186/1471-2229-13-133
13. Benitez-Alfonso, Y., Jackson, D., and Maule, A. (2011). Redox regulation of intercellular transport. Protoplasma248, 131-140. doi: 10.1007/s00709-010-0243-4
14. Bergey, D. R., Howe, G. A., and Ryan, C. A. (1996). Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc. Natl. Acad. Sci. U.S.A. 93, 12053-12058. doi: 10.1073/pnas.93.22.12053
15. Bergey, D. R., Orozco-Cardenas, M., De Moura, D. S., and Ryan, C. A. (1999). A wound- and systemin-inducible polygalacturonase in tomato leaves. Proc. Natl. Acad. Sci. U.S.A. 96, 1756-1760. doi: 10.1073/pnas.96.4.1756
16. Bessire, M., Chassot, C., Jacquat, A. C., Humphry, M., Borel, S., Petetot, J. M.,et al. (2007). A permeable cuticle inArabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J. 26, 2158-2168. doi: 10.1038/sj.emboj.7601658
17. Bhattacharya, R., Koramutla, M. K., Negi, M., Pearce, G., and Ryan, C. A. (2013). Hydroxyproline-rich glycopeptide signals in potato elicit signaling associated with defense against insects and pathogens. Plant Sci. 207, 88-97. doi: 10.1016/j.plantsci.2013.03.002
18. Boller, T., and Felix, G. (2009). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379-406. doi: 10.1146/annurev.arplant.57.032905.105346
19. Bonaventure, G., and Baldwin, I. T. (2010). Transduction of wound and herbivory signals in plastids. Commun. Integr. Biol. 3, 313-317. doi: 10.4161/cib.3.4.11834
20. Bostock, R. M., and Stermer, B. A. (1989). Perspectives on wound healing in resistance to pathogens. Annu. Rev. Phytopathol. 27, 343-371. doi: 10.1146/annurev.py.27.090189.002015
21. 2+ sensor protein kinases. Nature 464, 418-422. doi: 10.1038/nature08794
22. Bouquin, T., Lasserre, E., Pradier, J., Pech, J. C., and Balague, C. (1997). Wound and ethylene induction of the ACC oxidase melon gene CM-ACO1 occurs via two direct and independent transduction pathways. Plant Mol. Biol. 35, 1029-1035. doi: 10.1023/A:1005902226054
23. Branca, C., De Lorenzo, G., and Cervone, F. (1988). Competitive inhibition of the auxin-induced elongation by α-D-oligogalacturonides in pea stem segments. Physiol. Plant. 72, 499-504. doi: 10.1111/j.1399-3054.1988.tb09157.x
24. Browse, J. (2009). The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry70, 1539-1546. doi: 10.1016/j.phytochem.2009.08.004
25. 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
26. Cabrera, J. C., Boland, A., Messiaen, J., Cambier, P., and Van Cutsem, P. (2008). Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18, 473-482. doi: 10.1093/glycob/cwn027
27. 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
28. Chauvin, A., Caldelari, D., Wolfender, J. L., and Farmer, E. E. (2013). Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol. 197, 566-575. doi: 10.1111/nph.12029
29. Chen, X. Y., and Kim, J. Y. (2009). Callose synthesis in higher plants. Plant Signal. Behav. 4, 489-492. doi: 10.4161/psb.4.6.8359
30. Chen, Y. C., Siems, W. F., Pearce, G., and Ryan, C. A. (2008). Six peptide wound signals derived from a single precursor protein in Ipomoea batatas leaves activate the expression of the defense gene sporamin. J. Biol. Chem.283, 11469-11476. doi: 10.1074/jbc.M709002200
31. Cheong, Y. H., Chang, H. S., Gupta, R., Wang, X., Zhu, T., and Luan, S. (2002). Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129, 661-677. doi: 10.1104/pp.002857
32. Choi, J., Tanaka, K., Cao, Y. R., Qi, Y., Qiu, J., Liang, Y.,et al. (2014). Identification of a plant receptor for extracellular ATP. Science 343, 290-294. doi: 10.1126/science.343.6168.290
33. Cona, A., Tisi, A., Ghuge, S. A., Franchi, S., De Lorenzo, G., and Angelini, R. (2014). Wound healing response and xylem differentiation in tobacco plants over-expressing a fungal endopolygalacturonase is mediated by copper amine oxidase activity. Plant Physiol. Biochem. 82, 54-65. doi: 10.1016/j.plaphy.2014.05.004
34. Craigon, D. J., James, N., Okyere, J., Higgins, J., Jotham, J., and May, S. (2004). NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res. 32, D575-D577. doi: 10.1093/nar/gkh133
35. Creelman, R. A., and Mullet, J. E. (1997). Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 355-381. doi: 10.1146/annurev.arplant.48.1.355
36. Cui, F., Brosche, M., Sipari, N., Tang, S., and Overmyer, K. (2013). Regulation of ABA dependent wound induced spreading cell death by MYB108. New Phytol. 200, 634-640. doi: 10.1111/nph.12456
37. 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
38. 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
39. Decreux, A., and Messiaen, J. (2005). Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol. 46, 268-278. doi: 10.1093/pcp/pci026
40. Delessert, C., Wilson, I. W., Van Der, S. D., Dennis, E. S., and Dolferus, R. (2004). Spatial and temporal analysis of the local response to wounding in Arabidopsis leaves. Plant Mol. Biol. 55, 165-181. doi: 10.1007/s11103-004-0112-7
41. Dengler, N., and Kang, J. (2001). Vascular patterning and leaf shape. Curr. Opin. Plant Biol. 4, 50-56. doi: 10.1016/S1369-5266(00)00135-7
42. Denness, L., McKenna, J. F., Segonzac, C., Wormit, A., Madhou, P., Bennett, M.,et al. (2011). Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process inArabidopsis. Plant Physiol. 156, 1364-1374. doi: 10.1104/pp.111.175737
43. Denoux, C., Galletti, R., Mammarella, N., Gopalan, S., Werck, D., De Lorenzo, G.,et al. (2008). Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1, 423-445. doi: 10.1093/mp/ssn019
44. Diaz, J., ten Have, A., and van Kan, J. A. (2002). The role of ethylene and wound signaling in resistance of tomato toBotrytis cinerea. Plant Physiol. 129, 1341-1351. doi: 10.1104/pp.001453
45. Drerup, M. M., Schlucking, K., Hashimoto, K., Manishankar, P., Steinhorst, L., Kuchitsu, K.,et al. (2013). The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol. Plant 6, 559-569. doi: 10.1093/mp/sst009
46. Dubiella, U., Seybold, H., Durian, G., Komander, E., Lassig, R., Witte, C. P.,et al. (2013). Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. U.S.A. 110, 8744-8749. doi: 10.1073/pnas.1221294110
47. 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
48. Farmer, E. E., and Ryan, C. A. (1992). Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4, 129-134. doi: 10.1105/tpc.4.2.129
49. Ferrari, S., Galletti, R., Denoux, C., De Lorenzo, G., Ausubel, F. M., and Dewdney, J. (2007). Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol. 144, 367-379. doi: 10.1104/pp.107.095596
50. 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
51. 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
52. Finkelstein, R. (2013). Abscisic acid synthesis and response. Arabidopsis Book 11:e0166. doi: 10.1199/tab.0166
53. Fonseca, S., Chico, J. M., and Solano, R. (2009). The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr. Opin. Plant Biol. 12, 539-547. doi: 10.1016/j.pbi.2009.07.013
54. 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
55. 2+-dependent protein kinases. PLoS Pathog. 9:e1003127. doi: 10.1371/journal.ppat.1003127
56. Glauser, G., Dubugnon, L., Mousavi, S. A., Rudaz, S., Wolfender, J. L., and Farmer, E. E. (2009). Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J. Biol. Chem. 284, 34506-34513. doi: 10.1074/jbc.M109.061432
57. Gomi, K., Ogawa, D., Katou, S., Kamada, H., Nakajima, N., Saji, H.,et al. (2005). A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol. 46, 1902-1914. doi: 10.1093/pcp/pci211
58. Guo, H. Q., Li, L., Ye, H. X., Yu, X. F., Algreen, A., and Yin, Y. H. (2009). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 106, 7648-7653. doi: 10.1073/pnas.0812346106
59. Hadiarto, T., Nanmori, T., Matsuoka, D., Iwasaki, T., Sato, K., Fukami, Y.,et al. (2006). Activation of ArabidopsisMAPK kinase kinase (AtMEKK1) and induction of AtMEKK1-AtMEK1 pathway by wounding. Planta 223, 708-713. doi: 10.1007/s00425-005-0126-7
60. Harper, J. F., and Harmon, A. (2005). Plants, symbiosis and parasites: A calcium signalling connection. Nat. Rev. Mol. Cell Biol. 6, 555-566. doi: 10.1038/nrm1679
61. Haswell, E. S., Peyronnet, R., Barbier-Brygoo, H., Meyerowitz, E. M., and Frachisse, J. M. (2008). Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr. Biol. 18, 730-734. doi: 10.1016/j.cub.2008.04.039
62. Hause, B., Hause, G., Kutter, C., Miersch, O., and Wasternack, C. (2003). Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol. 44, 643-648. doi: 10.1093/pcp/pcg072
63. He, G. Z., Tarui, Y., and Iino, M. (2005). A novel receptor kinase involved in jasmonate-mediated wound and phytochrome signaling in maize coleoptiles. Plant Cell Physiol. 46, 870-883. doi: 10.1093/pcp/pci092
64. Heiling, S., Schuman, M. C., Schoettner, M., Mukerjee, P., Berger, B., Schneider, B.,et al. (2010). Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata. Plant Cell 22, 273-292. doi: 10.1105/tpc.109.071449
65. 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
66. Herde, O., Atzorn, R., Fisahn, J., Wasternack, C., Willmitzer, L., and Peña-Cortés, H. (1996). Localized wounding by heat initiates the accumulation of proteinase inhibitor II in abscisic acid-deficient plants by triggering jasmonic acid biosynthesis. Plant Physiol. 112, 853-860.
67. Hind, S. R., Malinowski, R., Yalamanchili, R., and Stratmann, J. W. (2010). Tissue-type specific systemin perception and the elusive systemin receptor. Plant Signal. Behav. 5, 42-44. doi: 10.4161/psb.5.1.10119
68. Huffaker, A., Dafoe, N. J., and Schmelz, E. A. (2011). ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol. 155, 1325-1338. doi: 10.1104/pp.110.166710
69. Huffaker, A., Pearce, G., and Ryan, C. A. (2006). An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. U.S.A. 103, 10098-10103. doi: 10.1073/pnas.0603727103
70. Huffaker, A., Pearce, G., Veyrat, N., Erb, M., Turlings, T. C. J., Sartor, R.,et al. (2013). Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proc. Natl. Acad. Sci. U.S.A. 110, 5707-5712. doi: 10.1073/pnas.1214668110
71. Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T., and Shinozaki, K. (2000). Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24, 655-665. doi: 10.1046/j.1365-313x.2000.00913.x
72. Ito, N., Takabatake, R., Seo, S., Hiraga, S., Mitsuhara, I., and Ohashi, Y. (2002). Induced expression of a temperature-sensitive leucine-rich repeat receptor-like protein kinase gene by hypersensitive cell death and wounding in tobacco plant carrying the N resistance gene. Plant Cell Physiol. 43, 266-274. doi: 10.1093/pcp/pcf031
73. Jacinto, T., McGurl, B., Franceschi, V., Delano-Freier, J., and Ryan, C. A. (1997). Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the β-glucuronidase gene in transgenic tomato plants. Planta 203, 406-412. doi: 10.1007/s004250050207
74. 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
75. Kadota, Y., Sklenar, J., Derbyshire, P., Stransfeld, L., Asai, S., Ntoukakis, V.,et al. (2014). Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54, 43-55. doi: 10.1016/j.molcel.2014.02.021
76. Kamiyoshihara, Y., Iwata, M., Fukaya, T., Tatsuki, M., and Mori, H. (2010). Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J. 64, 140-150. doi: 10.1111/j.1365-313X.2010.04316.x
77. Kanchiswamy, C. N., Takahashi, H., Quadro, S., Maffei, M. E., Bossi, S., Bertea, C.,et al. (2010). Regulation ofArabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol.10:97. doi: 10.1186/1471-2229-10-97
78. Kanzaki, M., Nagasawa, M., Kojima, I., Sato, C., Naruse, K., Sokabe, M.,et al. (1999). Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. Science 285, 882-886. doi: 10.1126/science.285.5429.882
79. Ketela, T., Green, R., and Bussey, H. (1999). Saccharomyces cerevisiae Mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway. J. Bacteriol. 181, 3330-3340.
80. 2+ and reactive oxygen species. Biochim. Biophys. Acta 1823, 398-405. doi: 10.1016/j.bbamcr.2011.09.011
81. Ko, J. H., Kim, J. H., Jayanty, S. S., Howe, G. A., and Han, K. H. (2006). Loss of function of COBRA, a determinant of oriented cell expansion, invokes cellular defense responses in Arabidopsis thaliana. J. Exp. Bot. 57, 2923-2936. doi: 10.1093/jxb/erl052
82. Kobayashi, M., Ohura, I., Kawakita, K., Yokota, N., Fujiwara, M., Shimamoto, K.,et al. (2007). Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065-1080. doi: 10.1105/tpc.106.048884
83. Kobayashi, M., Yoshioka, M., Asai, S., Nomura, H., Kuchimura, K., Mori, H.,et al. (2012). StCDPK5 confers resistance to late blight pathogen but increases susceptibility to early blight pathogen in potato via reactive oxygen species burst. New Phytol. 196, 223-237. doi: 10.1111/j.1469-8137.2012.04226.x
84. Kohorn, B. D., Johansen, S., Shishido, A., Todorova, T., Martinez, R., Defeo, E.,et al. (2009). Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J. 60, 974-982. doi: 10.1111/j.1365-313X.2009.04016.x
85. Kohorn, B. D., and Kohorn, S. L. (2012). The cell wall-associated kinases, WAKs, as pectin receptors. Front. Plant Sci. 3:88. doi: 10.3389/fpls.2012.00088
86. Kohorn, B. D., Kohorn, S. L., Todorova, T., Baptiste, G., Stansky, K., and McCullough, M. (2012). A dominant allele of Arabidopsis pectin-binding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Mol. Plant 5, 841-851. doi: 10.1093/mp/ssr096
87. 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
88. Krautz, R., Arefin, B., and Theopold, U. (2014). Damage signals in the insect immune response. Front. Plant Sci.5:342. doi: 10.3389/fpls.2014.00342
89. Krol, E., Mentzel, T., Chinchilla, D., Boller, T., Felix, G., Kemmerling, B.,et al. (2010). Perception of the Arabidopsisdanger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J. Biol. Chem. 285, 13471-13479. doi: 10.1074/jbc.M109.097394
90. Krupkova, E., Immerzeel, P., Pauly, M., and Schmulling, T. (2007). The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. Plant J. 50, 735-750. doi: 10.1111/j.1365-313X.2007.03123.x
91. Kudla, J., Batistic, O., and Hashimoto, K. (2010). Calcium signals: the lead currency of plant information processing. Plant Cell 22, 541-563. doi: 10.1105/tpc.109.072686
92. Kurusu, T., Hamada, J., Nokajima, H., Kitagawa, Y., Kiyoduka, M., Takahashi, A.,et al. (2010). Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol. 153, 678-692. doi: 10.1104/pp.109.151852
93. Kwaaitaal, M., Huisman, R., Maintz, J., Reinstadler, A., and Panstruga, R. (2011). Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem. J. 440, 355-365. doi: 10.1042/BJ20111112
94. L’Haridon, F., Besson-Bard, A., Binda, M., Serrano, M., Abou-Mansour, E., Balet, F.,et al. (2011). A permeable cuticle is associated with the release of reactive oxygen species and induction of innate immunity. PLoS Pathog.7:e1002148. doi: 10.1371/journal.ppat.1002148
95. Laluk, K., Luo, H. L., Chai, M. F., Dhawan, R., Lai, Z. B., and Mengiste, T. (2011). Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell 23, 2831-2849. doi: 10.1105/tpc.111.087122
96. Lecourieux, D., Ranjeva, R., and Pugin, A. (2006). Calcium in plant defense-signaling pathways. New Phytol. 171, 249-269. doi: 10.1111/j.1469-8137.2006.01777.x
97. Leon, J., Rojo, E., and Sanchez-Serrano, J. J. (2001). Wound signaling in plants. J. Exp. Bot. 52, 1-9. doi: 10.1093/jexbot/52.354.1
98. Li, H., Zhou, S. Y., Zhao, W. S., Su, S. C., and Peng, Y. L. (2008). A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol. Biol. 69, 337-346. doi: 10.1007/s11103-008-9430-5
99. 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
100. Lionetti, V., Francocci, F., Ferrari, S., Volpi, C., Bellincampi, D., Galletti, R.,et al. (2010). Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc. Natl. Acad. Sci. U.S.A. 107, 616-621. doi: 10.1073/pnas.0907549107
101. 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
102. Liu, J. H., Lee-Tamon, S. H., and Reid, D. M. (1997). Differential and wound-inducible expression of 1-aminocylopropane-1-carboxylate oxidase genes in sunflower seedlings. Plant Mol. Biol. 34, 923-933. doi: 10.1023/A:1005801420172
103. Luan, S. (2009). The CBL-CIPK network in plant calcium signaling. Trends Plant Sci. 14, 37-42. doi: 10.1016/j.tplants.2008.10.005
104. Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S., and Gruissem, W. (2002). Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14, S389-S400. doi: 10.1105/tpc.001115
105. Ludwig, A. A., Saitoh, H., Felix, G., Freymark, G., Miersch, O., Wasternack, C.,et al. (2005). Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc. Natl. Acad. Sci. U.S.A. 102, 10736-10741. doi: 10.1073/pnas.0502954102
106. Maffei, M. E., Mithofer, A., and Boland, W. (2007). Before gene expression: early events in plant-insect interaction. Trends Plant Sci. 12, 310-316. doi: 10.1016/j.tplants.2007.06.001
107. 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. doi: 10.1105/tpc.014167
108. Minibayeva, F., Beckett, R. P., and Kranner, I. (2014). Roles of apoplastic peroxidases in plant response to wounding. Phytochemistry doi: 10.1016/j.phytochem.2014.06.008 [Epub ahead of print].
109. Mithofer, A., Ebel, J., and Felle, H. H. (2005). Cation fluxes cause plasma membrane depolarization involved in beta-glucan elicitor-signaling in soybean roots. Mol. Plant Microbe Interact. 18, 983-990. doi: 10.1094/MPMI-18-0983
110. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K.,et al. (2011). ROS signaling: the new wave? Trends Plant Sci. 16, 300-309. doi: 10.1016/j.tplants.2011.03.007
111. Monshausen, G. B., Bibikova, T. N., Messerli, M. A., Shi, C., and Gilroy, S. (2007). Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl. Acad. Sci. U.S.A. 104, 20996-21001. doi: 10.1073/pnas.0708586104
112. Mouille, G., Ralet, M. C., Cavelier, C., Eland, C., Effroy, D., Hematy, K.,et al. (2007). Homogalacturonan synthesis inArabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J. 50, 605-614. doi: 10.1111/j.1365-313X.2007.03086.x
113. Mousavi, S. A. R., Chauvin, A., Pascaud, F., Kellenberger, S., and Farmer, E. E. (2013). GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500, 422-426. doi: 10.1038/nature12478
114. Nakagami, H., Pitzschke, A., and Hirt, H. (2005). Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10, 339-346. doi: 10.1016/j.tplants.2005.05.009
115. 2+ influx and touch sensing in roots. Proc. Natl. Acad. Sci. U.S.A. 104, 3639-3644. doi: 10.1073/pnas.0607703104
116. Narvaez-Vasquez, J., Pearce, G., and Ryan, C. A. (2005). The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc. Natl. Acad. Sci. U.S.A. 102, 12974-12977. doi: 10.1073/pnas.0505248102
117. Narvaez-Vasquez, J., and Ryan, C. A. (2004). The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta 218, 360-369. doi: 10.1007/s00425-003-1115-3
118. Nawrath, C. (2006). Unraveling the complex network of cuticular structure and function. Curr. Opin. Plant Biol. 9, 281-287. doi: 10.1016/j.pbi.2006.03.001
119. Nemoto, K., Seto, T., Takahashi, H., Nozawa, A., Seki, M., Shinozaki, K.,et al. (2011). Autophosphorylation profiling of Arabidopsis protein kinases using the cell-free system. Phytochemistry 72, 1136-1144. doi: 10.1016/j.phytochem.2011.02.029
120. Nuhse, T. S. (2012). Cell wall integrity signaling and innate immunity in plants. Front. Plant Sci. 3:280. doi: 10.3389/fpls.2012.00280
121. Nurnberger, T., Brunner, F., Kemmerling, B., and Piater, L. (2004). Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198, 249-266. doi: 10.1111/j.0105-2896.2004.0119.x
122. 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
123. O’Donnell, P. J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H. M. O., and Bowles, D. J. (1996). Ethylene as a signal mediating the wound response of tomato plants. Science 274, 1914-1917. doi: 10.1126/science.274.5294.1914
124. Oda, T., Hashimoto, H., Kuwabara, N., Akashi, S., Hayashi, K., Kojima, C.,et al. (2010). Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. J. Biol. Chem. 285, 1435-1445. doi: 10.1074/jbc.M109.058909
125. Onkokesung, N., Baldwin, I. T., and Galis, I. (2010). The role of jasmonic acid and ethylene crosstalk in direct defense of Nicotiana attenuata plants against chewing herbivores. Plant Signal. Behav. 5, 1305-1307. doi: 10.4161/psb.5.10.13124
126. Orozco-Cardenas, M., McGurl, B., and Ryan, C. A. (1993). Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc. Natl. Acad. Sci. U.S.A. 90, 8273-8276. doi: 10.1073/pnas.90.17.8273
127. Orozco-Cardenas, M., and Ryan, C. A. (1999). Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 6553-6655. doi: 10.1073/pnas.96.11.6553
128. Oyarce, P., and Gurovich, L. (2011). Evidence for the transmission of information through electric potentials in injured avocado trees. J. Plant Physiol. 168, 103-108. doi: 10.1016/j.jplph.2010.06.003
129. Pearce, G., Bhattacharya, R., Chen, Y. C., Barona, G., Yamaguchi, Y., and Ryan, C. A. (2009). Isolation and characterization of hydroxyproline-rich glycopeptide signals in black nightshade leaves. Plant Physiol. 150, 1422-1433. doi: 10.1104/pp.109.138669
130. Pearce, G., Moura, D. S., Stratmann, J., and Ryan, C. A. (2001). Production of multiple plant hormones from a single polyprotein precursor. Nature 411, 817-820. doi: 10.1038/35081107
131. Pearce, G., and Ryan, C. A. (2003). Systemic signaling in tomato plants for defense against herbivores. Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J. Biol. Chem. 278, 30044-30050. doi: 10.1074/jbc.M304159200
132. Pearce, G., Siems, W. F., Bhattacharya, R., Chen, Y. C., and Ryan, C. A. (2007). Three hydroxyproline-rich glycopeptides derived from a single petunia polyprotein precursor activate defensin I, a pathogen defense response gene. J. Biol. Chem. 282, 17777-17784. doi: 10.1074/jbc.M701543200
133. Peña-Cortés, H., Fisahn, J., and Willmitzer, L. (1995). Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl. Acad. Sci. U.S.A. 92, 4106-4113. doi: 10.1073/pnas.92.10.4106
134. Proels, R. K., Oberhollenzer, K., Pathuri, I. P., Hensel, G., Kumlehn, J., and Huckelhoven, R. (2010). RBOHF2 of barley is required for normal development of penetration resistance to the parasitic fungus Blumeria graminis f. sp. hordei. Mol. Plant Microbe Interact. 23, 1143-1150. doi: 10.1094/MPMI-23-9-1143
135. 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
136. Rasul, S., Dubreuil-Maurizi, C., Lamotte, O., Koen, E., Poinssot, B., Alcaraz, G.,et al. (2012). Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ. 35, 1483-1499. doi: 10.1111/j.1365-3040.2012.02505.x
137. Reddy, A. S., Ali, G. S., Celesnik, H., and Day, I. S. (2011). Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23, 2010-2032. doi: 10.1105/tpc.111.084988
138. Rehrig, E. M., Appel, H., Jones, A. D., and Schultz, C. J. (2014). Roles for jasmonate- and ethylene-induced transcription factors in the ability of Arabidopsis to respond differentially to damage caused by two insect herbivores. Front. Plant Sci. 5:407. doi: 10.3389/fpls.2014.00407
139. Reymond, P., Weber, H., Damond, M., and Farmer, E. E. (2000). Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12, 707-720. doi: 10.1105/tpc.12.5.707
140. Riederer, M., and Schreiber, L. (2001). Protecting against water loss: analysis of the barrier properties of plant cuticles. J. Exp. Bot. 52, 2023-2032. doi: 10.1093/jexbot/52.363.2023
141. Roberts, K. (1992). Potential awareness of plants. Nature 360, 14-15. doi: 10.1038/360014a0
142. Rodriguez, M. C., Petersen, M., and Mundy, J. (2010). Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621-649. doi: 10.1146/annurev-arplant-042809-112252
143. Ryan, C. A., and Jagendorf, A. (1995). Self defense by plants. Proc. Natl. Acad. Sci. U.S.A. 92:4075. doi: 10.1073/pnas.92.10.4075
144. Sanders, D., Pelloux, J., Brownlee, C., and Harper, J. F. (2002). Calcium at the crossroads of signaling. Plant Cell 14, S401-S417. doi: 10.1105/tpc.002899
145. Savatin, D. V., Ferrari, S., Sicilia, F., and De Lorenzo, G. (2011). Oligogalacturonide-auxin antagonism does not require posttranscriptional gene silencing or stabilization of auxin response repressors in Arabidopsis. Plant Physiol. 157, 1163-1174. doi: 10.1104/pp.111.184663
146. Savatin, D. V., Gigli, B. N., Marti, L., Fabbri, C., Cervone, F., and De Lorenzo, G. (2014). The Arabidopsis NPK1-related protein kinases ANPs are required for elicitor-induced oxidative burst and immunity. Plant Physiol. 165, 1188-1202. doi: 10.1104/pp.114.236901
147. Schaller, A., and Stintzi, A. (2009). Enzymes in jasmonate biosynthesis - structure, function, regulation. Phytochemistry 70, 1532-1538. doi: 10.1016/j.phytochem.2009.07.032
148. Scheer, J. M., and Ryan, C. A. (1999). A 160-kD systemin receptor on the surface of Lycopersicon peruvianumsuspension-cultured cells. Plant Cell 11, 1525-1535. doi: 10.1105/tpc.11.8.1525
149. Schilmiller, A. L., and Howe, G. A. (2005). Systemic signaling in the wound response. Curr. Opin. Plant Biol. 8, 369-377. doi: 10.1016/j.pbi.2005.05.008
150. Schweighofer, A., Kazanaviciute, V., Scheikl, E., Teige, M., Doczi, R., Hirt, H.,et al. (2007). The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell 19, 2213-2224. doi: 10.1105/tpc.106.049585
151. Schweizer, P., Felix, G., Buchala, A., Müller, C., and Métraux, J. P. (1996a). Perception of free cutin monomers by plant cells. Plant J. 10, 331-341. doi: 10.1046/j.1365-313X.1996.10020331.x
152. Schweizer, P., Jeanguenat, A., Whitacre, D., Metraux, J. P., and Mosinge, E. (1996b). Induction of resistance in barley against Erysiphe graminis f.sp. hordei by free cutin monomers. Physiol. Mol. Plant Pathol. 49, 103-120. doi: 10.1006/pmpp.1996.0043
153. Schweizer, P., Jeanguenat, A., Mosinger, E., and Metraux, J. P. (1994). Plant protection by free cutin monomers in two cereal pathosystems. Adv. Mol. Gen. Plant Microbe Interact. 21, 371-374. doi: 10.1007/978-94-011-0177-6_55
154. Seo, S., Katou, S., Seto, H., Gomi, K., and Ohashi, Y. (2007). The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J. 49, 899-909. doi: 10.1111/j.1365-313X.2006.03003.x
155. Seo, S., Okamoto, N., Seto, H., Ishizuka, K., Sano, H., and Ohashi, Y. (1995). Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270, 1988-1992. doi: 10.1126/science.270.5244.1988
156. Sieber, P., Schorderet, M., Ryser, U., Buchala, A., Kolattukudy, P., Metraux, J. P.,et al. (2000). TransgenicArabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12, 721-737. doi: 10.1105/tpc.12.5.721
157. Staswick, P. E., and Tiryaki, I. (2004). The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16, 2117-2127. doi: 10.1105/tpc.104.023549
158. Stenzel, I., Hause, B., Maucher, H., Pitzschke, A., Miersch, O., Ziegler, J.,et al. (2003). Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato - amplification in wound signalling. Plant J. 33, 577-589. doi: 10.1046/j.1365-313X.2003.01647.x
159. Suzuki, N., and Mittler, R. (2012). Reactive oxygen species-dependent wound responses in animals and plants. Free Radic. Biol. Med. 53, 2269-2276. doi: 10.1016/j.freeradbiomed.2012.10.538
160. Szczegielniak, J., Borkiewicz, L., Szurmak, B., Lewandowska-Gnatowska, E., Statkiewicz, M., Klimecka, M.,et al. (2012). Maize calcium-dependent protein kinase (ZmCPK11): local and systemic response to wounding, regulation by touch and components of jasmonate signaling. Physiol. Plant. 146, 1-14. doi: 10.1111/j.1399-3054.2012.01587.x
161. Takabatake, R., Seo, S., Ito, N., Gotoh, Y., Mitsuhara, I., and Ohashi, Y. (2006). Involvement of wound-induced receptor-like protein kinase in wound signal transduction in tobacco plants. Plant J. 47, 249-257. doi: 10.1111/j.1365-313X.2006.02781.x
162. Takeda, S., Gapper, C., Kaya, H., Bell, E., Kuchitsu, K., and Dolan, L. (2008). Local positive feedback regulation determines cell shape in root hair cells. Science 319, 1241-1244. doi: 10.1126/science.1152505
163. 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
164. Tisi, A., Angelini, R., and Cona, A. (2008). Wound healing in plants: cooperation of copper amine oxidase and flavin-containing polyamine oxidase. Plant Signal. Behav. 3, 204-206. doi: 10.4161/psb.3.3.5372
165. Toufighi, K., Brady, S. M., Austin, R., Ly, E., and Provart, N. J. (2005). The Botany array resource: e-northerns, expression angling, and promoter analyses. Plant J. 43, 153-163. doi: 10.1111/j.1365-313X.2005.02437.x
166. Verica, J. A., Chae, L., Tong, H. Y., Ingmire, P., and He, Z. H. (2003). Tissue-specific and developmentally regulated expression of a cluster of tandemly arrayed cell wall-associated kinase-like kinase genes in Arabidopsis. Plant Physiol. 133, 1732-1746. doi: 10.1104/pp.103.028530
167. Wagner, T. A., and Kohorn, B. D. (2001). Wall-Associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13, 303-318. doi: 10.1105/tpc.13.2.303
168. Wang, L., Tsuda, K., Sato, M., Cohen, J. D., Katagiri, F., Glazebrook, J.,et al. (2009). Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against. PLoS Pathog. 5:e1000301. doi: 10.1371/journal.ppat.1000301
169. Wildon, D. C., Thain, J. F., Minchin, P. E. H., Gubb, I. R., Reilly, A. J., Skipper, Y. D.,et al. (1992). Electrical signaling and systemic proteinase inhibitor induction in the wounded plant. Nature 360, 62-65. doi: 10.1038/360062a0
170. Wolf, S., Hematy, K., and Hofte, H. (2012). Growth control and cell wall signaling in plants. Annu. Rev. Plant Biol.63, 381-407. doi: 10.1146/annurev-arplant-042811-105449
171. Yamaguchi, Y., Huffaker, A., Bryan, A. C., Tax, F. E., and Ryan, C. A. (2010). PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22, 508-522. doi: 10.1105/tpc.109.068874
172. Yamaguchi, Y., Pearce, G., and Ryan, C. A. (2006). The cell surface leucine-rich repeat receptor for AtPEP1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc. Natl. Acad. Sci. U.S.A.103, 10104-10109. doi: 10.1073/pnas.0603729103
173. 2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol. 152, 1284-1296. doi: 10.1104/pp.109.147371
174. Yang, D. H., Hettenhausen, C., Baldwin, I. T., and Wu, J. (2012). Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations. Plant Physiol. 159, 1591-1607. doi: 10.1104/pp.112.199018
175. Zhang, S. Q., and Klessig, D. F. (1998a). The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl. Acad. Sci. U.S.A. 95, 7225-7230. doi: 10.1073/pnas.95.12.7225
176. Zhang, S. Q., and Klessig, D. F. (1998b). Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc. Natl. Acad. Sci. U.S.A. 95, 7433-7438. doi: 10.1073/pnas.95.13.7433
177. Zimmermann, M. R., Maischak, H., Mithofer, A., Boland, W., and Felle, H. H. (2009). System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol. 149, 1593-1600. doi: 10.1104/pp.108.133884
178. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D. G., Boller, T.,et al. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749-760. doi: 10.1016/j.cell.2006.03.037
179. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D., Felix, G.,et al. (2004). Bacterial disease resistance inArabidopsis through flagellin perception. Nature 428, 764-767. doi: 10.1038/nature02485