The combination of Trichoderma harzianum and chemical fertilization leads to the deregulation of phytohormone networking, preventing the adaptive responses of tomato plants to salt stress

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Rubio, M B ^a   Hermosa, Rosa ^a   Vicente, Rubén ^b   Gómez Acosta, Fabio A ^a   Morcuende, Rosa ^b   Monte, Enrique ^a   Bettiol, Wagner ^a,c  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^c EMBRAPA CERRADOS   (Brazil)

Author keywords

Abiotic stress; Growth promotion; Nitrogen fertilizer; Phytohormone regulation; Saline

Indexed keywords

EID: 85014896465     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.00294     Document Type: Article

References (55)

1. Alfano, G., Ivey, M. L. L., Cakir, C., Bos, J. I. B., Miller, S. A., Madden, L. V., et al. (2007). Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97, 429–437. doi: 10.1094/PHYTO-97-4-0429
2. Allakhverdiev, S. I., Sakamoto, A., Nishiyama, Y., Inaba, M., and Murata, N. (2000). Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol. 123, 1047–1056. doi: 10.1104/pp.123.3.1047
3. Alonso, J. M., Stepanova, A. N., Solano, R., Wisman, E., Ferrari, S., Ausubel, F., et al. (2003). Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100, 2992–2997. doi: 10.1073/pnas.0438070100
4. Aquastat (2016). Available at: www.fao.org/nr/water/aquastat/main/index.stm
5. Bianco, C., and Defez, R. (2009). Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid overproducing Sinorhizobium meliloti strain. J. Exp. Bot. 60, 3097–3107. doi: 10.1093/jxb/erp140
6. 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. doi: 10.1105/tpc.6.11.1583
7. + -induced SOS1 mRNA stability in Arabidopsis. Plant J. 53, 554–565. doi: 10.1111/j.1365-313X.2007.03364.x
8. Courty, P. E., Smith, P., Koegel, S., Redecker, D., and Wipf, D. (2015). Inorganic nitrogen uptake and transport in beneficial plant root-microbe interactions. Crit. Rev. Plant Sci. 34, 4–16. doi: 10.1080/07352689.2014.897897
9. Craufurd, P. Q., Flower, D. J., and Peacock, J. M. (2008). Effect of heat and drought stress on sorghum (Sorghum bicolor). I. panicle development and leaf appearance. Exp Agric. 29, 61–76. doi: 10.1017/S001447970002041X
10. Dimkpa, C., Weinand, T., and Asch, F. (2009). Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 32, 1682–1694. doi: 10. 1111/j.1365-3040.2009.02028.x
11. Dodd, I. C., and Pérez-Alfocea, F. (2012). Microbial amelioration of crop salinity stress. J. Exp. Bot. 63, 3415–3428. doi: 10.1093/jxb/ers033
12. Domínguez, S., Rubio, M. R., Cardoza, R. E., Gutiérrez, S., Nicolás, C., Bettiol, W., et al. (2016). Nitrogen metabolism and growth enhancement in tomato plants challenged with Trichoderma harzianum expressing the Aspergillus nidulans acetamidase amdS gene. Front. Microbiol. 7:1182. doi: 10.3389/fmicb.2016.01182
13. Dong, H., Zhen, Z., Peng, J., Chang, L., Gong, Q., and Wang, N. N. (2011). Loss of ACS7 confers abiotic stress tolerance by modulating ABA sensitivity and accumulation in Arabidopsis. J. Exp. Bot. 62, 4875–4887. doi: 10.1093/jxb/err143
14. Druzhinina, I. S., Seidl-Seiboth, V., Herrera-Estrella, A., Horwitz, B. A., Kenerley, C. M., Monte, E., et al. (2011). Trichoderma: the genomics of opportunistic success. Nat. Rev. Microbiol. 9, 749–759. doi: 10.1038/nrmicro2637
15. Evelin, H., Kapoor, R., and Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann. Bot. 104, 1263–1280. doi: 10.1093/aob/mcp25
16. Gao, F., Hao, J., Yao, Y., Wang, X., and Hasi, A. (2013). Cloning and characterization of ethylene-insensitive 2 (EIN2) gene from Cucumis melo. Rus. J. Plant Physiol. 60, 713–719. doi: 10.1134/S102144371305004X
17. Gazzarrini, S., and McCourt, P. (2001). Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr. Opin. Plant Biol. 4, 387–391. doi: 10.1016/S1369-5266(00)00190-4
18. Harman, G. E. (2000). Myths and dogmas of biocontrol: changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis. 84, 377–393. doi: 10.1094/PDIS.2000.84.4.377
19. Harman, G. E., Obregon, M. A., Samuels, G. J., and Lorito, M. (2010). Changing models for commercialization and implementation of biocontrol in the developed and developing world. Plant Dis. 94, 928–939. doi: 10.1094/PDIS-94-8-0928
20. Hermosa, R., Viterbo, A., Chet, I., and Monte, E. (2012). Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158, 17–25. doi: 10.1099/mic.0. 052274-0
21. Jayakannan, M., Bose, J., Babourina, O., Shabala, S., Massart, A., and Poschenrieder, C. (2015). The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J. Exp. Bot. 66, 1865–1875. doi: 10.1093/jxb/eru528
22. Jesus, J., Castro, F., Niemelä, A., Borges, M. T., and Danko, A. S. (2015). Evaluation of the impact of different soil salinization processes on organic and mineral soils. Water Air Soil Pollut. 226, 102. doi: 10.1007/s11270-015-2373-y
23. Kraiser, T., Gras, D. E., Gutiérrez, A. G., González, B., and Gutiérrez, R. A. (2011). A holistic view of nitrogen acquisition in plants. J. Exp. Bot. 62, 1455–1466. doi: 10.1093/jxb/erq425
24. Lei, G., Shen, M., Li, Z. G., Zhang, B., Duan, K. X., Wang, N., et al. (2011). EIN2 regulates salt stress response and interacts with a MA3 domain-containing protein ECIP1 in Arabidopsis. Plant Cell Environ. 34, 1678–1692. doi: 10.1111/j.1365-3040.2011.02363.x
25. Liu, D., Ford, K. L., Roessner, U., Natera, S., Cassin, A. M., Patterson, J. H., et al. (2013). Rice suspension cultured cells are evaluated as a model system to study salt responsive networks in plants using a combined proteomic and metabolomics profiling approach. Proteomics 13, 2046–2062. doi: 10.1002/pmic.201200425
26. Lorito, M., Woo, S. L., Harman, G. E., and Monte, E. (2010). Translational research on Trichoderma: from ‘omics to the field. Annu. Rev. Phytopathol. 48, 395–417. doi: 10.1146/annurev-phyto-073009-114314
27. Lucena, M. A., Romero-Aranda, R., Mercado, J. A., Cuartero, J., Valpuesta, V., and Quesada, M. A. (2003). Structural and physiological changes in the roots of tomato plants over-expressing a basic peroxidase. Physiol. Plant 118, 422–429. doi: 10.1034/j.1399-3054.2003.00115.x
28. Mastouri, F., Björkman, T., and Harman, G. E. (2010). Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100, 1213–1221. doi: 10.1094/PHYTO-03-10-0091
29. Meng, S., Su, L., Li, Y., Wang, Y., Zhang, C., and Zhao, Z. (2016). Nitrate and ammonium contribute to the distinct nitrogen metabolism of Populus simonii during moderate salt stress. PLoS ONE 11:e0150354. doi: 10.1371/journal.pone. 0150354
30. Mittler, R., and Blumwald, E. (2010). Genetic engineering for modern agriculture: challenges and perspectives. Annu. Rev. Plant Biol. 61, 443–462. doi: 10.1146/annurev-arplant-042809-112116
31. Mittler, R., and Blumwald, E. (2015). The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27, 64–70. doi: 10.1105/tpc.114.133090
32. Morán-Diez, E., Rubio, M. B., Domínguez, S., Hermosa, R., Monte, E., and Nicolás, C. (2012). Transcriptomic response of Arabidopsis thaliana after root colonization by Trichoderma harzianum. J. Plant Physiol. 169, 614–620. doi: 10.1016/j.jplph.2011.12.016
33. Mulvaney, R. L., Khan, S. A., and Ellsworth, T. R. (2009). Synthetic nitrogen fertilizers deplete soil nitrogen: a global dilemma for sustainable cereal production. J. Environ. Qual. 38, 2295–2314. doi: 10.2134/jeq2008. 0527
34. Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239–250. doi: 10.1046/j.0016-8025.2001.00808.x
35. Parida, A. K., and Das, A. B. (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicol. Environ. Saf. 60, 324–349. doi: 10.1016/j.ecoenv.2004.06.010
36. Park, H. J., Kim, W. Y., and Yun, D. J. (2016). A new insight of salt stress signaling in plant. Mol. Cells 39, 447–459. doi: 10.14348/molcells.2016. 0083
37. Peleg, Z., and Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 14, 290–295. doi: 10.1016/j.pbi.2011.02.001
38. Philippot, L., Raaijmakers, J. M., Lemanceau, P., and van der Puttern, W. H. (2013). Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799. doi: 10.1038/nrmicro3109
39. Rawat, L., Singh, Y., Shukla, N., and Kumar, J. (2011). Alleviation of the adverse effects of salinity stress in wheat (Triticum aestivum L.) by seed biopriming with salinity tolerant isolates of Trichoderma harzianum. Plant Soil 347:387. doi: 10.1007/s11104-011-0858-z
40. Rockström, J., Steffen, W., Noone, K., Persson, A., Chapin, F. S., Lambin, E. F., et al. (2009). A safe operating space for humanity. Nature 461, 472–475. doi: 10.1038/461472a
41. Rubio, M. B., Domínguez, S., Monte, E., and Hermosa, R. (2012). Comparative study of Trichoderma gene expression in interactions with tomato plants using high-density oligonucleotide microarrays. Microbiology 158, 119–128. doi: 10. 1099/mic.0.052118-0
42. Rubio, M. B., Quijada, N. M., Pérez, E., Domínguez, S., Monte, E., and Hermosa, R. (2014). Identifying beneficial qualities of Trichoderma parareesei for plants. Appl. Environ. Microbiol. 80, 1864–1873. doi: 10.1128/AEM.03375-13
43. Sánchez-Bel, P., Troncho, P., Gamir, J., Pozo, M. J., Camañes, G., Cerezo, M., et al. (2016). The nitrogen availability interferes with mycorrhiza-induced resistance against Botrytis cinerea in tomato. Front. Microbiol. 7:1598. doi: 10.3389/fmicb. 2016.01598
44. Saxena, I., Srikanth, S., and Chen, Z. (2016). Cross talk between H2O2 and interacting signal molecules under plant stress response. Front. Plant Biol. 7:570. doi: 10.3389/fpls.2016.00570
45. Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–1108. doi: 10.1038/nprot.2008.73
46. + antiporter. Proc. Natl. Acad. Sci. U.S.A. 97, 6896–6901. doi: 10.1073/pnas.120170197
47. + antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat. Biotechnol. 21, 81–85. doi: 10.1038/nbt766
48. Shoresh, M., Harman, G. E., and Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 48, 21–43. doi: 10.1146/annurev-phyto-073009-114450
49. Spoel, S. H., Mou, Z., Tada, Y., Spivey, N. W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137, 860–872. doi: 10.1016/j.cell. 2009.03.038
50. Suzuki, N., Miller, G., Salazar, C., Mondal, H. A., Shulaev, E., Cortes, D. F., et al. (2013). Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25, 3553–3569. doi: 10.1105/tpc.113.114595
51. Wang, C., El-Shetehy, M., Shine, M. B., Yu, K., Navarre, D., and Wendehenne, D. (2014). Free radicals mediate systemic acquired resistance. Cell Rep. 7, 348–355. doi: 10.1016/j.celrep.2014.03.032
52. Yuan, Z., Druzhinina, I., Labbé, J., Redman, R., Qin, Y., Rodriguez, R., et al. (2016). Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. Sci. Rep. 6:32467. doi: 10.1038/srep32467
53. Zandalinas, S. I., Balfagón, D., Arbona, V., Gómez-Cadenas, A., Inupakutika, M. A., and Mittler, R. (2016a). ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J. Exp. Bot. 67, 5381–5390. doi: 10.1093/jxb/erw299
54. Zandalinas, S. I., Rivero, R. M., Martínez, V., Gómez-Cadenas, A., and Arbona, V. (2016b). Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biol. 16:105. doi: 10.1186/s12870-016-0791-7
55. Zhu, J. K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247–273. doi: 10.1146/annurev.arplant.53.091401.143329