Induced Resistance to Ustilago maydis in Zea mays Inoculated in Non-Sterile Conditions

Authors

  • Domingo Martínez-Soto Departamento de Ingeniería Genética, Unidad Irapuato, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional
  • José Ruiz-Herrera Departamento de Ingeniería Genética, Unidad Irapuato, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional

DOI:

https://doi.org/10.6000/1927-3037.2016.05.02.4

Keywords:

Ustilago maydis, Zea mays, Biotic and abiotic stresses, induced resistance, Priming effect

Abstract

Plants are able to acquire induced resistance to pathogens (priming) by its previous exposure to biotic or abiotic stresses. To analyze whether this process is involved in the maize infection by Ustilago maydis, we have compared the infection occurring in plants inoculated under axenic conditions or in sterile soil to plants grown in non-sterile soil. Our results showed that plants grown under axenic conditions were more susceptible to infection than those inoculated in non-sterile soil. Accordingly, disease symptoms: chlorosis development, anthocyanin production, tumor development, and necrosis, were more and severe in axenic plants. In addition, cell death and reactive oxygen species production, as well as ethylene, were higher in axenic plants. These observations indicate for the first time, that different physical stressors and contact with microorganisms of the environment are responsible for the induction of resistance (priming) in this pathosystem.

References


[1]Ferreira RB, Monteiro S, Freitas R, Santos CS, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR. Fungal pathogens: the battle for plant infection. Crit Rev Plant Sci 2006; 25: 505-24. http://dx.doi.org/10.1080/07352680601054610
[2]Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR. The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 2007; 8: 677-700. http://dx.doi.org/10.1111/j.1364-3703.2007.00419.x
[3]Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, Kämper J. Reprograming a maize plant: transcriptional and metabolic changes induced by fungal biotroph Ustilago maydis. Plant J 2008; 56: 181-95.http://dx.doi.org/10.1111/j.1365-313X.2008.03590.x
[4]Zipfel C. Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 2008; 20: 10-6. http://dx.doi.org/10.1016/j.coi.2007.11.003
[5]Chester KS. The problem of acquired physiological immunity in plants. Q Rev Biol 1933; 8: 275-324.http://dx.doi.org/10.1086/394440
[6]Conrath U. Priming of induced plant defense responses. In: Jean-Pierre J, Pierre G, Eds.Advances in botanical research. Amsterdam: Elsevier 2009; pp. 361-95.
[7]Heil M, Karban R. Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 2010; 25: 137-44. http://dx.doi.org/10.1016/j.tree.2009.09.010
[8]Song Y, Chen D, Lu K, Sun Z, Zeng R. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 2015; 6: 786.http://dx.doi.org/10.3389/fpls.2015.00786
[9]Conrath U. Molecular aspects of defense priming. Trends Plant Sci 2011; 16: 524-31. http://dx.doi.org/10.1016/j.tplants.2011.06.004
[10]Planchamp C, Glauser G, Mauch-Mani B. Root inoculation with Pseudomonas putida KT2440 induces transcriptional and metabolic changes and systematic resistance in maize plants. Front Plant Sci 2015; 5: 719.http://dx.doi.org/10.3389/fpls.2014.00719
[11]Saville BJ, Donaldson ME, Doyle CE. Investigating Host Induced Meiosis in a Fungal Plant Pathogen. In: Swan A, editor. Meiosis-Molecular Mechanisms and Cytogenetic Diversity. Rijeka: Intech 2012; pp. 411-50.
[12]León-Ramírez CG, Sánchez-Arreguín JA, Ruiz-Herrera J. Ustilago maydis, a delicacy of the aztec cuisine and a model for research. Natural Resources 2014; 5: 256-67. http://dx.doi.org/10.4236/nr.2014.56024
[13]Bölker M. Ustilago maydis-a valuble model system for the study of fungal dimorphism and virulence. Microbiology 2001; 147: 1395-401. http://dx.doi.org/10.1099/00221287-147-6-1395
[14]Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R. Ustilago maydis as a patogen. Annu Rev Phytopathol 2009; 47: 423-45. http://dx.doi.org/10.1146/annurev-phyto-080508-081923
[15]León-Ramírez CG, Cabrera-Ponce JL, Martínez-Espinoza AD, Herrera-Estrella L, Méndez L, Reynaga-Peña CG, Ruiz-Herrera J. Infection of alternative host plant species by Ustilago maydis. New Phytol 2004; 164: 337-46. http://dx.doi.org/10.1111/j.1469-8137.2004.01171.x
[16]Méndez-Morán L, Reynaga-Peña CG, Springer PS, Ruiz-Herrera J. Ustilago maydis infection of the non-natural host Arabidopsis thaliana. Phytopathology 2005; 95: 480-88. http://dx.doi.org/10.1094/PHYTO-95-0480
[17]Martínez-Soto D, Briones-Robledo AM, Estrada-Luna AA, Ruiz-Herrera J. Transcriptomic analysis of Ustilago maydis infecting Arabidopsis reveals important aspects of the fungus pathogenic mechanisms. Plant Signal Behav2013; 8:e25059. http://dx.doi.org/10.4161/psb.25059
[18]Mazaheri-Naeini M, Sabbagh SK, Martinez Y, Séjalon-Delmas N, Roux C. Assessment of Ustilago maydis as a fungal model for root infection studies. Fugal Biol 2015; 119: 145-153. http://dx.doi.org/10.1016/j.funbio.2014.12.002
[19]Martínez-Soto D, Pérez-García FE, Ruiz-Herrera J. Arabidopsis infection by haploid or diploid strains of Ustilago maydis reveals its capacity as a necrotrophic or biotrophic phytopathogen. Fungal Genom Biol 2016; 6: 1. http://dx.doi.org/10.4172/2165-8056.1000133
[20]Banuett F, Herskowitz I. Different a alleles of Ustilago maydisare necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA 1989; 86: 5878-82.http://dx.doi.org/10.1073/pnas.86.15.5878
[21]Martínez-Espinoza AD, León-Ramírez CG, Elizarraraz G, Ruiz-Herrera J. Monomorphic nonpathogenic mutants of Ustilago maydis. Phytopathology 1997; 87: 259-65.http://dx.doi.org/10.1094/PHYTO.1997.87.3.259
[22]Ruiz-Herrera J, Martínez-Espinoza AD, Alvarez PE, Xoconostle-Cazares B. Carboxin-resistant mutant of Ustilago maydis is impaired in its pathogenicity for Zea mays. Curr Microbiol 1999; 39: 291-4.http://dx.doi.org/10.1007/s002849900461
[23]Holliday R. Ustilago maydis. In: King RC, editor. The Handbook of Genetics. New York: Plenum Press 1974; p. 575-95.http://dx.doi.org/10.1007/978-1-4899-1710-2_31
[24]Murashige T, Skoog F. A revised medium for growth and bioassays with tobacco tissue cultures. Physiol Plant 1962; 15: 473-97. http://dx.doi.org/10.1111/j.1399-3054.1962.tb08052.x
[25]Sato T, Oku H, Tsuruma K, Katsumura K, Shimazawa M, Hara H, Sugiyama T, Ikeda T. Effect of hypoxia on susceptibility of RGC-5 cells to nitric oxide. Invest Ophthalmol Vis Sci 2010; 51: 2575-86. http://dx.doi.org/10.1167/iovs.09-4303
[26]Martinez-Pacheco M, Ruiz-Herrera J. Diferential comparmentation of ornithine decarboxylase in cell of Mucor rouxii. J Gen Microbiol 1993; 139: 1387-94. http://dx.doi.org/10.1099/00221287-139-6-1387
[27]Altman SA, Randers L, Rau G. Comparison of trypan blue dye exclusion and fluorometric assay for mammalian cell viability determination. Biotechnol Prog 1993; 9: 671-74.http://dx.doi.org/10.1021/bp00024a017
[28]Malamy J, Hennig J, Klessig DF. Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 1992; 4: 359-66. http://dx.doi.org/10.1105/tpc.4.3.359
[29]Conrath U, Pieterse CM, Mauch-Mani B. Priming in plant-pathogen interactions. Trends Plant Sci 2002; 7: 210-16. http://dx.doi.org/10.1016/S1360-1385(02)02244-6
[30]Aranega-Bou P, de la O Leyva M, Finiti I, García-Agustín P, González-Bosch C. Priming of plant resistance by natural compounds. Hexanoic acid as a model. Front Plant Sci 2014. http://dx.doi.org/10.3389/fpls.2014.00488
[31]Morrison EN, Emery RJ, Saville BJ. Phytohormone involvement in the Ustilago maydis-Zea mays pathosystem: Relationships between abscisic acid and cytokin levels andstrain virulence in infected cob tissue. PLoS One 2015; 10: e0130945.http://dx.doi.org/10.1371/journal.pone.0130945
[32]Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Macek B, Mann M, Kahmann R. Metabolic priming by a secreted fungal effector. Nature 2011; 478: 395-98.http://dx.doi.org/10.1038/nature10454
[33]Doehlemann G, Requena N, Schaefer P, Brunner F, O ?Connell R, Parker JE. Reprogramming of plant cells by filamentous plant-colonizing microbes. New Phytol 2014; 204: 803-14. http://dx.doi.org/10.1111/nph.12938
[34]Okmen B, Doehlemann G. Inside plant: biotrophic strategies to modulate host immunity and metabolism. Curr Opin Plant Biol 2014; 20: 19-25. http://dx.doi.org/10.1016/j.pbi.2014.03.011
[35]Rabe F, Ajami-Rashidi Z, Doehlemann G, Kahmann R, Djamei A. Degradation of the plant defense hormone salicylic acid by the biotrophic fungus Ustilago maydis. Mol Microbiol 2013; 89: 179-88. http://dx.doi.org/10.1111/mmi.12269
[36]Martínez-Soto D, González-Prieto JM, Ruiz-Herrera J. Transcriptomic analysis of the GCN5 gene reveals mechanisms of the epigenetic regulation of virulence and morphogenesis in Ustilago maydis. FEMS Yeast Res 2015. http://dx.doi.org/10.1093/femsyr/fov055
[37]Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 2005; 43: 205-27. http://dx.doi.org/10.1146/annurev.phyto.43.040204.135923

Downloads

Published

2016-08-12

Issue

Section

Articles