Plant pathogens affecting the establishment of plant-symbiont interaction

Frontiers in Plant Science

Volumn 7, Issue JAN2016, 2016, Pages

  de Souza, Eduardo M ^a   Granada, Camille E ^a   Sperotto, Raul A ^a  

^a CENTRO UNIVERSITÁRIO UNIVATES   (Brazil)

Author keywords

Mycorrhiza; Pathogen; Plant interaction; Rhizobium; Signal transduction; Symbiont

Indexed keywords

EID: 85000774183     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00015     Document Type: Article

References (53)

1. Antunes, P. M., Miller, J., Carvalho, L. M., Klironomos, J. N., and Newman, J. A. (2008). Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct. Ecol. 22, 912-918. doi: 10.1111/j.1365-2435.2008.01432.x
2. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu. Rev. Plant Biol. 55, 373-379. doi: 10.1146/annurev.arplant.55.031903.141701
3. Ballhorn, D. J., Younginger, B. S., and Kautz, S. (2014). An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseolus vulgaris. BMCPlant Biol. 14:321. doi: 10.1186/s12870-014-0321-4
4. Benizri, E., Piutti, S., Verger, S., Pages, L., Vercambre, G., Poessel, J. L., et al. (2005). Replant diseases: bacterial community structure and diversity in peach rhizosphere as determined by metabolic and genetic fingerprinting. Soil Biol. Biochem. 37, 1738-1746. doi: 10.1016/j.soilbio.2005.02.009
5. Blilou, I., Ocampo, J. A., and Garcia-Garrido, J. M. (1999). Resistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid. J. Exp. Bot. 50, 1663-1668. doi: 10.1093/jxb/50.340.1663
6. Blilou, I., Ocampo, J. A., and Garcia-Garrido, J. M. (2000). Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J. Exp. Bot. 51, 1969-1977. doi: 10.1093/jexbot/51.353.1969
7. Cardenas, L., Martinez, A., Sanchez, F., and Quinto, C. (2008). Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant J. 56, 802-813. doi: 10.1111/j.1365-313X.2008.03644.x
8. Chihaoui, S. A., Mhadhbi, H., and Mhamdi, R. (2012). The antibiosis of nodule-endophytic agrobacteria and its potential effect on nodule functioning of Phaseolus vulgaris. Arch. Microbiol. 194, 1013-1021. doi: 10.1007/s00203-012-0837-7
9. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., et al. (1994). A central role of salicylic Acid in plant disease resistance. Science 266, 1247-1250. doi: 10.1126/science.266.5188.1247
10. de Roman, M., Fernandez, I., Wyatt, T., Sahrawy, M., Heil, M., and Pozo, M. J. (2011). Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. J. Ecol. 99, 7-15. doi: 10.1111/j.1365-2745.2010.01752.x
11. de Vleeschauwer, D., and Hofte, M. (2009). "Rhizobacteria-induced systemic resistance," in Plant Innate Immunity, ed L. C. van Loon (London: Elsevier), 224-283.
12. Dodds, P. N., and Rathjen, J. P. (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548. doi: 10.1038/nrg2812
13. Duffy, B., Schouten, A., and Raaijmakers, J. M. (2003). Pathogen self-defense: mechanisms to counteract microbial antagonism. Annu. Rev. Phytopathol. 41, 501-538. doi: 10.1146/annurev.phyto.41.052002.095606
14. Faessel, L., Nassr, N., Lebeau, T., and Walter, B. (2010). Chemically-induced resistance on soybean inhibits nodulation and mycorrhization. Plant Soil 329, 259-268. doi: 10.1007/s11104-009-0150-7
15. Gechev, T. S., Van Breusegem, F., Stone, J. M., Denev, I., and Laloi, C. (2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28, 1091-1101. doi: 10.1002/bies.20493
16. Gianinazzi-Pearson, V., Gianinazzi, S., Guillemin, J. P., Trouvelot, A., and Duc, G. (1991). "Genetic and cellular analysis of resistance to vesicular arbuscular (VA) mycorrhizal fungi in pea mutants," in Advances in Molecular Genetics of Plant-Microbe Interactions, eds H. Hennecke and D. P. S. Verma (Dordrecht: Springer), 336-342.
17. Gutjahr, C., and Paszkowski, U. (2009). Weights in the balance: Jasmonic Acid and Salicylic Acid signaling in root-biotroph interactions. Mol. Plant Microbe Interact. 22, 763-772. doi: 10.1094/MPMI-22-7-0763
18. Heil, M. (2007). "Trade-offs associated with induced resistance," in Induced Resistance for Plant Defence: A Sustainable Approach to Crop Protection, eds D. Walters, C. A. Newton, and G. D. Lyon (Oxford: Blackwell), 157-177.
19. Herrera Medina, M. J., Gagnon, H., Piche, Y., Ocampo, J. A., Garcia Garrido, J. M., and Vierheilig, H. (2003). Root colonization byarbuscularmycorrhizal fungiis affected by the salicylic acid content of the plant. Plant Sci. 164, 993-998. doi: 10.1016/S0168-9452(03)00083-9
20. Holtsmark, I., Eijsink, V. G., and Brurberg, M. B. (2008). Bacteriocins from plant pathogenic bacteria. FEMS Microbiol. Lett. 280, 7. doi: 10.1111/j.1574-6968.2007.01010.x
21. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
22. Kumar, H., Dubey, R. C., and Maheshwari, D. K. (2011). Effect of plant growth promoting rhizobia on seed germination, growth promotion and suppression of Fusarium wilt of fenugreek (Trigonella foenum-graecum L.). Crop Prot. 30, 1396-1403. doi: 10.1016/j.cropro.2011.05.001
23. Lahlali, R., and Hijri, M. (2010). Screening, identification and evaluation of potential biocontrol fungal endophytes against Rhizoctonia solani AG3 on potato plants. FEMS Microbiol. Lett. 311, 152-159. doi: 10.1111/j.1574-6968.2010.02084.x
24. Liang, Y., Cao, Y., Tanaka, K., Thibivilliers, S., Wan, J., Choi, J., et al. (2013). Non legumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341, 1384-1387. doi: 10.1126/science.1242736
25. Liu, J., Wang, E. T., Ren, D. W., and Chen, W. X. (2010). Mixture of endophytic Agrobacterium and Sinorhizobium meliloti strains could induce nonspecific nodulation on some woody legumes. Arch. Microbiol. 192, 229-234. doi: 10.1007/s00203-010-0543-2
26. Lohar, D. P., Haridas, S., Gantt, J. S., and VandenBosch, A. (2007). A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New Phytol. 173, 39-49. doi: 10.1111/j.1469-8137.2006.01901.x
27. Marsh, J. F., and Schultze, M. (2001). Analysis of arbuscular mycorrhiza using symbiosis-defective plant mutants. New Phytol. 150, 525-532. doi: 10.1046/j.1469-8137.2001.00140.x
28. Martinez-Abarca, F., Herrera-Cervera, J. A., Bueno, P., Sanjuan, J., Bisseling, T., and Olivares, J. (1998). Involvement of salicylic acid in the establishment of the Rhizobium meliloti - Alfalfa symbiosis. Molec. Plant-Microbe Interac. 11, 153-155. doi: 10.1094/MPMI.1998.11.2.153
29. Mithofer, A., Bhagwat, A. A., Feger, M., and Ebel, J. (1996). Suppression of fungal |3-glucan-induced plant defense in soybean (Glycine max) by cyclic 1,3-1,6-|3-glucans from the symbiont Bradyrhizobium japonicum. Planta 199, 270-275. doi: 10.1007/BF00196568
30. Montiel, J., Nava, N., Cardenas, L., Sanchez-Lopez, R., Arthikala, M. K., Santana, O., et al. (2012). A Phaseolus vulgaris NADPH oxidase gene is required for root infection by Rhizobia. Plant Cell Physiol. 53, 1751-1767. doi: 10.1093/pcp/pcs120
31. Mrabet, M., Mnasri, B., Romdhane, S. B., Laguerre, G., Aouani, M. E., and Mhamdi, R. (2006). Agrobacterium strains isolated from root nodules of common bean specifically reduce nodulation by Rhizobium gallicum. FEMS Microbiol. Ecol. 56, 304-309. doi: 10.1111/j.1574-6941.2006. 00069.x
32. Mucha, J., Dahm, H., Strzelczyk, E., and Werner, A. (2006). Synthesis of enzymes connected withmycoparasitismbyectomycorrhizalfungi. Arch. Microbiol. 185, 69-77. doi: 10.1007/s00203-005-0068-2
33. Mucha, J., Zadworny, M., and Werner, A. (2009). Cytoskeleton and mitochondrial morphology of saprotrophs and the pathogen Heterobasidion annosum in the presence of Suillus bovinus metabolites. Mycol. Res. 113, 981-990. doi:10.1016/j.mycres.2009.06.002
34. Munoz, N., Robert, G., Melchiorre, M., Racca, R., and Lascano, R. (2012). Saline and osmotic stress differentially affects apoplastic and intracellular reactive oxygen species production, curling and death of root hair during Glycine max L.-Bradyrhizobium japonicum interaction. Environm. Experim. Botany 78, 76-83. doi: 10.1016/j.envexpbot.2011.12.008
35. Muthomi, J. W., Otieno, P. E., Cheminingwa, G. N., Nderitu, J. H., and Wagacha, J. M. (2007). Effect of legume root rot pathogens and fungicide seed treatment on nodulation and biomass accumulation. J. Biol. Sci. 7, 1163-1170. doi:10.3923/jbs.2007.1163.1170
36. Nanda, A. K., Andrio, E., Marino, D., Pauly, N., and Dunand, C. (2010). Reactive oxygen species during plant-microorganism earlyinteractions. J. Integrat. Plant Biol. 52, 195-204. doi: 10.1111/j.1744-7909.2010.00933.x
37. Netzker, T., Fischer, J., Weber, J., Mattern, D. J., Konig, C. C., Valiante, V., et al. (2015). Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front. Microbiol. 6:299. doi: 10.3389/fmicb.2015.00299
38. Pauly, N., Pucciariello, C., Mandon, K., Innocenti, G., Jamet, A., Baudouin, E., et al. (2006). Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. J. Exp. Bot. 57, 1769-1776. doi: 10.1093/jxb/erj184
39. Pieterse, C. M. J., van Pelt, J. A., van Wees, S. C. M., Ton, J., Leon-Kloosterziel, K., Keurentjes, J. J. B., et al. (2001). Rhizobacteria-mediated induced systemic resistance: triggering, signalling and expression. Eur. J. Plant Pathol. 107, 51-61. doi: 10.1023/A1008747926678
40. Pozo, M. J., and Azcon-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393-398. doi: 10.1016/j.pbi.2007.05.004
41. Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C., and Moenne-Loccoz, Y. (2009). The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321, 341-361. doi: 10.1007/s11104-008-9568-6
42. Rey, T., Chatterjee, A., Buttay, M., Toulotte, J., and Schornack, S. (2015). Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. NewPhytol. 206, 497-500. doi: 10.1111/nph.13233
43. Schouten, A., van den Berg, G., Edel-Hermann, V., Steinberg, C., Gautheron, N., Alabouvette, C., et al. (2004). Defense responses of Fusarium oxysporum to 2, 4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by Pseudomonas fluorescens. Mol. Plant-Microbe Interact. 17, 1201-1211. doi:10.1094/MPMI.2004.17.11.1201
44. Siciliano, V., Genre, A., Balestrini, R., Cappellazzo, G., de Wit, P. J. G. M., and Bonfante, P. (2007). Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol. 144, 1455-1466. doi: 10.1104/pp 107.097980
45. Sillo, F., Zampieri, E., Giordano, L., Lione, G., Colpaert, J. V., Balestrini, R., et al. (2015). Identification of genes differentially expressed during the interaction between the plant symbiont Suillus luteus and two plant pathogenic allopatric Heterobasidion species. Mycol. Progress 14, 13. doi: 10.1007/s11557-015-1130-3
46. Spaepen, S., Vanderleyden, J., and Okon, Y. (2009). "Plant growth-promoting actions ofrhizobacteria," in Plant Innate Immunity, ed L. C. VanLoon(London: Elsevier), 284-321.
47. Stacey, G., McAlvin, C. B., Kim, S. Y., Olivares, J., and Soto, M. J. (2006). Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiol. 141, 1473-1481. doi: 10.1104/pp 106.080986
48. Torres, M. A., Jones, J. D. G., and Dangl, J. L. (2006). Reactive Oxygen Species signaling in response to pathogens. Plant Physiol. 141, 373-378. doi: 10.1104/pp 106.079467
49. Toth, K., and Stacey, G. (2015). Does plant immunity play a critical role during initiation of the legume-rhizobium symbiosis? Front. Plant Sci. 6:401. doi: 10.3389/fpls.2015.00401
50. van Dam, N. M., and Heil, M. (2011). Multitrophic interactions below and above ground: en route to the next level. J. Ecol. 99, 77-88. doi: 10.1111/j.1365-2745.2010.01761.x
51. van Spronsen, P. C., Tak, T., Rood, A. M., van Brussel, A. A., Kijne, J. W., and Boot, K. J. (2003). Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation. Mol. Plant Microbe Interact. 16, 83-91. doi: 10.1094/MPMI.2003.16.1.83
52. Wang, E., Schornack, S., Marsh, J. F., Gobbato, E., Schwessinger, B., Eastmond, P., et al. (2012). A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22, 2242-2246. doi:10.1016/j.cub.2012.09.043
53. Zou, C. S., Mo, M. H., Gu, Y. Q., Zhou, J. P., and Zhang, K. Q. (2007). Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol. Biochem. 39, 2371-2379. doi: 10.1016/j.soilbio.2007.04.009