Extracellular ATP activates MAPK and ROS signaling during injury response in the fungus trichoderma atroviride

Frontiers in Plant Science

Volumn 5, Issue NOV, 2014, Pages

  Medina Castellanos, Elizabeth ^a   Esquivel Naranjo, Edgardo U ^a,b   Heil, Martin ^a   Herrera Estrella, Alfredo ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^b UNIVERSIDAD AUTÓNOMA DE QUERÉTARO   (Mexico)

Author keywords

Calcium; Conidiation; Extracellular ATP (eATP); Injury response; Mitogen activated protein kinase (MAPK); Reactive oxygen species (ROS)

Indexed keywords

EID: 84979935377     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00659     Document Type: Article

References (71)

1. Abbracchio, M. P., Burnstock, G., Boeynaems, J.-M., Barnard, E. A., Boyer, J. L., Kennedy, C., et al. (2006). International union of pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev. 58, 281-341. doi: 10.1124/pr.58.3.3
2. Aguirre, J., Ríos-Momberg, M., Hewitt, D., and Hansberg, W. (2005). Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 13, 111-118. doi: 10.1016/j.tim.2005.01.007
3. Arimura, G. I., and Maffei, M. E. (2010). Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochem. Biophys. Res. Commun. 400, 455-460. doi: 10.1016/j.bbrc.2010.08.134
4. Bayram, Ö., Bayram, Ö. S., Ahmed, Y. L., Maruyama, J., Valerius, O., Rizzoli, S. O., et al. (2012). The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet. 8:e1002816. doi: 10.1371/journal.pgen.1002816
5. Beneloujaephajri, E., Costa, A., L’haridon, F., Métraux, 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
6. Cano-Domínguez, N., Alvarez-Delfín, K., Hansberg, W., and Aguirre, J. (2008). NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot. Cell 7, 1352-1361. doi: 10.1128/EC.00137-08
7. Carreras-Villasenor, N., Sanchez-Arreguin, J. A., and Herrera-Estrella, A. H. (2012). Trichoderma: sensing the environment for survival and dispersal. Microbiology 158, 3-16. doi: 10.1099/mic.0.052688-0
8. Chen, G. Y., and Nuñez, G. (2010). Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10, 826-37. doi: 10.1038/nri2873
9. Chivasa, S., Murphy, A. M., Hamilton, J. M., Lindsey, K., Carr, J. P., and Slabas, A. R. (2009). Extracellular ATP is a regulator of pathogen defence in plants. Plant J. 60, 436-448. doi: 10.1111/j.1365-313X.2009.03968.x
10. Choi, J., Tanaka, K., Cao, Y., 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
11. Cordeiro, J. V., and Jacinto, A. (2013). The role of transcription-independent damage signals in the initiation of epithelial wound healing. Nat. Rev. Mol. Cell Biol. 14, 249-262. doi: 10.1038/nrm3541
12. Covian-Nares, J. F., Koushik, S. V., Puhl, H. L., and Vogel, S. S. (2010). Membrane wounding triggers ATP release and dysferlin-mediated intercellular calcium signaling. J. Cell Sci. 123, 1884-1893. doi: 10.1242/jcs.066084
13. Delgado-Jarana, J., Sousa, S., González, F., Rey, M., and Llobell, A. (2006). ThHog1 controls the hyperosmotic stress response in Trichoderma harzianum. Microbiology 152, 1687-1700. doi: 10.1099/mic.0.28729-0
14. de Oliveira, S., López-Muñoz, A., Candel, S., Pelegrín, P., Calado, A., and Mulero, V. (2014). ATP modulates acute inflammation in vivo through dual oxidase 1-derived H2O2 production and NF-κB activation. J. Immunol. 192, 5710-5719. doi: 10.4049/jimmunol.1302902
15. Fester, T., and Hause, G. (2005). Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15, 373-379. doi: 10.1007/s00572-005-0363-4
16. Fleissner, A., Leeder, A. C., Roca, M. G., Read, N. D., and Glass, N. L. (2009). Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc. Natl. Acad. Sci. U.S.A. 106, 19387-19392. doi: 10.1073/pnas.0907039106
17. Georgiou, C. D., Patsoukis, N., Papapostolou, I., and Zervoudakis, G. (2006). Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integr. Com. Biol. 46, 691-712. doi: 10.1093/icb/icj034
18. Heil, M. (2012). Damaged-self recognition as a general strategy for injury detection. Plant Signal. Behav. 7, 576-580. doi: 10.4161/psb.19921
19. Heil, M., Ibarra-Laclette, E., Adame-Álvarez, R. M., Martínez, O., Ramirez-Chávez, E., Molina-Torres, J., et al. (2012). How plants sense wounds: damaged-self recognition is based on plant-derived elicitors and induces octadecanoid signaling. PLoS ONE 7:e30537. doi: 10.1371/journal.pone.0030537
20. Heil, M., and Land, W. (2014). Danger signals-damaged-self recognition across the tree of life. Front. Plant Sci. 5:578. doi: 10.3389/fpls.2014.00578
21. Hernández-Oñate, M. A., Esquivel-Naranjo, E. U., Mendoza-Mendoza, A., Stewart, A., and Herrera-Estrella, A. H. (2012). An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc. Natl. Acad. Sci. U.S.A. 109, 14918-14923. doi: 10.1073/pnas.1209396109
22. Herrera-Estrella, A., and Chet, I. (2003). “The biological control agent Trichoderma: from fundamentals to applications,” in Handbook of Fungal Biotechnology, ed. D. Arora (Dekker, New York), 147-156.
23. Hettenhausen, C., Schuman, M. C., and Wu, J. (2014). MAPK signaling - a key element in plant defense response to insects. Insect Sci. doi: 10.1111/1744-7917.12128 [Epub ahead of print].
24. Hou, Z., Xue, C., Peng, Y., Katan, T., Kistler, H. C., and Xu, J.-R. (2002). A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant Microbe Interact. 15, 1119-1127. doi: 10.1094/MPMI.2002.15.11.1119
25. 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
26. Ishikawa, M., Murata, T., Sato, Y., Nishiyama, T., Hiwatashi, Y., Imai, A., et al. (2011). Physcomitrella cyclin-dependent kinase a links cell cycle reactivation to other cellular changes during reprogramming of leaf cells. Plant Cell 23, 2924-2938. doi: 10.1105/tpc.111.088005
27. Jang, H. S., Han, S. J., Kim, J. I., Lee, S., Lipschutz, J. H., and Park, K. M. (2013). Activation of ERK accelerates repair of renal tubular epithelial cells, whereas it inhibits progression of fibrosis following ischemia/reperfusion injury. Biochim. Biophys. Acta Mol. Basis Dis. 1832, 1998-2008. doi: 10.1016/j.bbadis.2013.07.001
28. Jedd, G. (2011). Fungal evo-devo: organelles and multicellular complexity. Trends Cell Biol. 21, 12-19. doi: 10.1016/j.tcb.2010.09.001
29. Kawate, T., Michel, J. C., Birdsong, W. T., and Gouaux, E. (2009). Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 460, 592-598. doi: 10.1038/nature08198
30. Kim, M., and McGinnis, W. (2011). Phosphorylation of Grainy head by ERK is essential for wound-dependent regeneration but not for development of an epidermal barrier. Proc. Natl. Acad. Sci. U.S.A. 108, 650-655. doi: 10.1073/pnas.1016386108
31. Kumar, A., Scher, K., Mukherjee, M., Pardovitz-Kedmi, E., Sible, G. V., Singh, U. S., et al. (2010). Overlapping and distinct functions of two Trichoderma virens MAP kinases in cell-wall integrity, antagonistic properties and repression of conidiation. Biochem. Biophys. Res. Commun. 398, 765-770. doi: 10.1016/j.bbrc.2010.07.020
32. Kurashima, Y., Amiya, T., Nochi, T., Fujisawa, K., Haraguchi, T., Iba, H., et al. (2012). Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat. Commun. 3, 1034. doi: 10.1038/ncomms2023
33. Lara-Ortíz, T., Riveros-Rosas, H., and Aguirre, J. (2003). Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol. Microbiol. 50, 1241-1255. doi: 10.1046/j.1365-2958.2003.03800.x
34. Lara-Rojas, F., Sánchez, O., Kawasaki, L., and Aguirre, J. (2011). Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development and spore functions. Mol. Microbiol. 80, 436-454. doi: 10.1111/j.1365-2958.2011.07581.x
35. Lee, J., and Gardiner, D. M. (2012). Regeneration of limb joints in the Axolotl (Ambystoma mexicanum). PLoS ONE 7:e50615. doi: 10.1371/journal.pone.0050615
36. Lee, K. S., Irie, K., Gotoh, Y., Watanabe, Y., Araki, H., Nishida, E., et al. (1993). A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol. Cell. Biol. 13, 3067-3075. doi: 10.1128/MCB.13.5.3067
37. Lee, K. S., and Levin, D. E. (1992). Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol. Cell. Biol. 12, 172-182. doi: 10.1128/MCB.12.1.172
38. Leonard, B. Y. T. J., and Dick, S. (1968). Chemical induction of haploid fruiting bodies in. Schizophyllum commune. Proc. Natl. Acad. Sci. U.S.A. 59, 745-751. doi: 10.1073/pnas.59.3.745
39. Lichius, A., Lord, K. M., Jeffree, C. E., Oborny, R., Boonyarungsrit, P., and Read, N. D. (2012). Importance of MAP kinases during protoperithecial morphogenesis in Neurospora crassa. PLoS ONE 7:e42565. doi: 10.1371/journal.pone.0042565
40. Liu, Y., and Zhang, S. (2004). Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16, 3386-3399. doi: 10.1105/tpc.104.026609
41. Mendoza-Mendoza, A., Pozo, M. J., Grzegorski, D., Martínez, P., García, J. M., Olmedo-Monfil, V., et al. (2003). Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 100, 15965-15970. doi: 10.1073/pnas.2136716100
42. Mendoza-Mendoza, A., Rosales-Saavedra, T., Cortés, C., Castellanos-Juárez, V., Martínez, P., and Herrera-Estrella, A. (2007). The MAP kinase TVK1 regulates conidiation, hydrophobicity and the expression of genes encoding cell wall proteins in the fungus Trichoderma virens. Microbiology 153, 2137-2147. doi: 10.1099/mic.0.2006/005462-0
43. Moreno-García, M., Recio-Tótoro, B., Claudio-Piedras, F., and Lanz-Mendoza, H. (2014). Injury and immune response: applying the danger theory to mosquitoes. Front. Plant Sci. 5:451. doi: 10.3389/fpls.2014.00451
44. Mu, D., Li, C., Zhang, X., Li, X., Shi, L., Ren, A., et al. (2013). Functions of the nicotinamide adenine dinucleotide phosphate oxidase family in Ganoderma lucidum: an essential role in ganoderic acid biosynthesis regulation, hyphal branching, fruiting body development, and oxidative-stress resistance. Environ. Microbiol. 16, 1709-1728. doi: 10.1111/1462-2920.12326
45. Nacu, E., and Tanaka, E. M. (2011). Limb regeneration: a new development? Annu. Rev. Cell Dev. Biol. 27, 409-440. doi: 10.1146/annurev-cellbio-092910-154115
46. Nadal-Ribelles, M., Conde, N., Flores, O., González-Vallinas, J., Eyras, E., Orozco, M., et al. (2012). Hog1 bypasses stress-mediated down-regulation of transcription by RNA polymerase II redistribution and chromatin remodeling. Genome Biol. 13, R106. doi: 10.1186/gb-2012-13-11-r106
47. Nelson, G., Kozlova-Zwinderman, O., Collis, A. J., Knight, M. R., Fincham, J. R. S., Stanger, C. P., et al. (2004). Calcium measurements in living filamentous fungi expressing codon-optimized aequorin. Mol. Microbiol. 52, 1437-1450. doi: 10.1111/j.1365-2958.2004.04066.x
48. Niethammer, P., Grabher, C., Look, A. T., and Mitchison, T. J. (2009). A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459, 996-999. doi: 10.1038/nature08119
49. Rämet, M., Lanot, R., Zachary, D., and Manfruelli, P. (2002). JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 241, 145-156. doi: 10.1006/dbio.2001.0502
50. Razzell, W., Evans, I. R., Martin, P., and Wood, W. (2013). Calcium flashes orchestrate the wound inflammatory response through duox activation and hydrogen peroxide release. Curr. Biol. 23, 424-429. doi: 10.1016/j.cub.2013.01.058
51. Reithner, B., Schuhmacher, R., Stoppacher, N., Pucher, M., Brunner, K., and Zeilinger, S. (2007). Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism and plant protection. Fungal Genet. Biol. 44, 1123-1133. doi: 10.1016/j.fgb.2007.04.001
52. Roux, S. J., and Steinebrunner, I. (2007). Extracellular ATP: an unexpected role as a signaler in plants. Trends Plant Sci. 12, 522-527. doi: 10.1016/j.tplants.2007.09.003
53. Sambrook, J., and Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory Press.
54. Schmoll, M. (2008). The information highways of a biotechnological workhorse-signal transduction in Hypocrea jecorina. BMC Genomics 9:430. doi: 10.1186/1471-2164-9-430
55. Seo, S., Okamoto, M., 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
56. Shabir, S., and Southgate, J. (2008). Calcium signalling in wound-responsive normal human urothelial cell monolayers. Cell Calcium 44, 453-464. doi: 10.1016/j.ceca.2008.02.008
57. 2+ signaling in human airway epithelial cell wound response. Toxicol. Sci. 121, 191-206. doi: 10.1093/toxsci/kfr044
58. 2+-dependent induction of conidiation in submerged cultures of Trichoderma viride. Can. J. Microbiol. 54, 291-298. doi: 10.1139/W08-001
59. Song, C. J., Steinebrunner, I., Wang, X., Stout, S. C., and Roux, S. J. (2006). Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. Plant Physiol. 140, 1222-1232. doi: 10.1104/pp.105.073072
60. 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
61. Taj, G., Agarwal, P., Grant, M., and Kumar, A. (2010). MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal. Behav. 5, 1370-1378. doi: 10.4161/psb.5.11.13020
62. Tanaka, K., Swanson, S. J., Gilroy, S., and Stacey, G. (2010). Extracellular nucleotides elicit cytosolic free calcium oscillations in Arabidopsis. Plant Physiol. 154, 705-719. doi: 10.1104/pp.110.162503
63. Torres, J., Rivera, A., Clark, G., and Roux, S. J. (2008). Participation of extracellular nucleotides in the wound response of Dasycladus vermicularis and Acetabularia acetabulum (Dasycladales, Chlorophyta). J. Phycol. 44, 1504-1511. doi: 10.1111/j.1529-8817.2008.00602.x
64. Wang, H., Liu, Y., Bruffett, K., Lee, J., Hause, G., Walker, J. C., et al. (2008). Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two MAPKs in Arabidopsis ovule development. Plant Cell 20, 602-613. doi: 10.1105/tpc.108.058032
65. Wei, H., Requena, N., and Fischer, R. (2003). The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol. Microbiol. 47, 1577-1588. doi: 10.1046/j.1365-2958.2003.03405.x
66. Wenemoser, D., Lapan, S. W., Wilkinson, A. W., Bell, G. W., and Reddien, P. W. (2012). A molecular wound response program associated with regeneration initiation in planarians. Genes Dev. 26, 988-1002. doi: 10.1101/gad.187377.112
67. Wu, J., and Baldwin, I. T. (2010). New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44, 1-24. doi: 10.1146/annurev-genet-102209-163500
68. Xu, J. R., Staiger, C. J., and Hamer, J. E. (1998). Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc. Natl. Acad. Sci. U.S.A. 95, 12713-12718. doi: 10.1073/pnas.95.21.12713
69. Yu, J. H., Hamari, Z., Han, K. H., Seo, J. A., Reyes-Domnguez, Y., and Scazzocchio, C. (2004). Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41, 973-981. doi: 10.1016/j.fgb.2004.08.001
70. Zeilinger, S., and Omann, M. (2007). Trichoderma biocontrol: signal transduction pathways involved in host sensing and mycoparasitism. Gene Regul. Syst. Biol. 1, 227-234.
71. Zeiser, R., Penack, O., Holler, E., and Idzko, M. (2011). Danger signals activating innate immunity in graft-versus-host disease. J. Mol. Med. 89, 833-845. doi: 10.1007/s00109-011-0767-x