Abstract
The association between reactive oxygen species (ROS) production and potato resistance to the hemibiotrophic pathogen Phytophthora infestans is poorly understood. In this study, the concentrations of hydrogen peroxide (H2O2), malondialdehyde (MDA), and soluble phenolics, as well as the activities of superoxide dismutase, catalase, and ascorbate peroxidase were measured during the early biotrophic and late necrotrophic stages of P. infestans infection on resistant and susceptible ‘Ovatio’ and ‘Bintje’ potato plants, respectively. Pathogen biomass was examined using semi-quantitative RT-PCR. Late blight (LB) severity was also evaluated. The LB severity in Ovatio was lower than that in Bintje, irrespective of the evaluation time. Moreover, in both cultivars, various biochemical defense responses occurred following pathogen infection. The susceptible cultivar activated defense responses at the later pathogen infection stages, resulting in higher concentrations of H2O2 and greater MDA content, with lower activity of antioxidant enzymes and phenolic content. These responses were accompanied by the necrotrophic phase, leading to extensive necrotic lesions on leaves. In contrast, fast hypersensitive-like lesions, an early peak in H2O2 concentration, low cell membrane integrity during the biotrophic phase, and a more efficient antioxidative system effectively restricted pathogen colonization before the transition to the necrotrophic phase in the resistant cultivar. These results suggest that LB resistance or susceptibility is regulated by a balance between the induction of ROS/antioxidants (intensity and timing) and the trophic phase of P. infestans.
Similar content being viewed by others
References
Anderson D, Prasad K, Stewart R (1995) Changes in isozyme profiles of catalase, peroxidase and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiology 109:1247–1257
Arora A, Sairam RK, Srivastave GC (2002) Oxidative stress and antioxidative systems in plants. Current Science 82:1227–1238
Bao G, Bi Y, Li Y, Kou Z, Hu L, Ge Y, Wang Y (2014) Overproduction of reactive oxygen species involved in the pathogenicity of Fusarium in potato tubers. Physiological and Molecular Plant Pathology 86:35–42
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44:276–286
Bengtsson T, Holefors A, Witzell J, Andreasson E, Liljeroth E (2014) Activation of defence responses to Phytophthora infestans in potato by BABA. Plant Pathology 63:193–202
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:1151–1154
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiology 98:1222–1227
Cui J, Jiang N, Meng J, Yang G, Liu W, Zhou X, Luan Y (2018) Lnc RNA 33732-RESPIRATORY BURST OXIDASE module associated with WRKY 1 in tomato-Phytophthora infestans interactions. The Plant Journal 98:933–946
De Gara L, De Pinto MC, Tommasi F (2003) The antioxidant system Vis-à-Vis reactive oxygen species during plant-pathogen interaction. Plant Physiology and Biochemistry 41:863–870
Debona D, Rodrigues FA, Rios JA, Nascimento KJT (2012) Biochemical changes in the leaves of wheat plants infected by Pyricularia oryzae. Phytopathology 102:1121–1129
Djébali N, Mhadhbi H, Lafitte C, Dumas B, Esquerré-Tugayé MT, Aouani ME, Jacquet C (2011) Hydrogen peroxide scavenging mechanisms are components of Medicago truncatula partial resistance to Aphanomyces euteiches. European Journal of Plant Pathology 131:559–571
Ehsani-Moghaddam B, Charles MT, Carisse O, Khanizadeh S (2006) Superoxide dismutase responses of strawberry cultivars to infection by Mycosphaerella fragariae. Journal of Plant Physiology 163:147–153
Eloy YR, Vasconcelos IM, Barreto AL, Freire-Filho FR, Oliveira JT (2015) H2O2 plays an important role in the lifestyle of Colletotrichum gloeosporioides during interaction with cowpea [Vigna unguiculata (L.) Walp.]. Fungal Biology 119:747–757
Fortunato AA, Debona D, Bernardeli AMA, Rodrigues FA (2015) Changes in the antioxidant system in soybean leaves infected by Corynespora cassiicola. Phytopathology 105:1050–1058
Fry WE, Goodwin SB (1997) Re-emergence of potato and tomato late blight in the United States. Plant Disease 81:1349–1357
Fry W, Patev SP, Meyers K, Bao K, Fei Z (2018) Phytophthora infestans sporangia produced in culture and on tomato leaflet lesions show marked differences in indirect germination rates, aggressiveness, and global transcription profiles. Molecular Plant-Microbe Interactions. https://doi.org/10.1094/MPMI-09-18-0255-TA
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research, 2nd edn. John Wiley, New York
Hajianfar R, Kolics B, Cernák I, Wolf I, Polgár Z, Taller J (2016) Expression of biotic stress response genes to Phytophthora infestans inoculation in white lady, a potato cultivar with race-specific resistance to late blight. Physiological and Molecular Plant Pathology 93:22–28
Hana S, Rachid R, Ibtissem S, Houria B, Mohammed-Rede D (2008) Induction of anti-oxidative enzymes by cadmium stress in tomato (Lycopersicon esculentum). African Journal of Plant Science 2:72–76
Haverkort AJ, Struik PC, Visser RG, Jacobsen E (2009) Applied biotechnology to combat late blight in potato caused by Phytophthora infestans. Potato Research 52:249–264
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125:189–198
Henriquez MA, Adam LR, Daayf F (2012) Alteration of secondary metabolites profiles in potato leaves in response to weakly and highly aggressive isolates of Phytophthora infestans. Plant Physiology and Biochemistry 57:8–14
Kamoun S, van der Lee T, van den Berg G, de Groot KE, Govers F (1998) Loss of production of the elicitor protein INF1 in the clonal lineage US-1 of Phytophthora infestans. Phytopathology 88:1315–1323
Khiutti A, Spooner DM, Jansky SH, Halterman DA (2015) Testing taxonomic predictivity of foliar and tuber resistance to Phytophthora infestans in wild relatives of potato. Phytopathology:1051198–1051205
Kobayashi M, Yoshioka M, Asai S, Nomura H, Kuchimura K, Mori H, Doke N, Yoshioka H (2012) StCDPK5 confers resistance to late blight pathogen but increases susceptibility to early blight pathogen in potato via reactive oxygen species burst. New Phytologist 196:223–237
Kuhl J, Hanneman R, Havey M (2001) Characterization and mapping of Rpi1, a late-blight resistance locus from diploid (1EBN) Mexican Solanum pinnatisectum. Molecular Genetics and Genomics 265:977–985
Lebeda A, Sedlářová M, Petřivalský M, Prokopová J (2008) Diversity of defence mechanisms in plant-oomycete interactions: a case study of Lactuca spp. and Bremia lactucae. European Journal of Plant Pathology 122:71–89
Luan Y, Cui J, Li J, Jiang N, Liu P, Meng J (2018) Effective enhancement of resistance to Phytophthora infestans by overexpression of miR172a and b in Solanum lycopersicum. Planta 247:127–138
Mandal S, Mitra A, Mallick N (2008) Biochemical characterization of oxidative burst during interaction between Solanum lycopersicum and Fusarium oxysporum f. sp. lycopersici. Physiological and Molecular Plant Pathology 72:56–61
Mohaghegh P, Khoshgoftarmanesh AH, Shirvani M, Sharifnabi B, Nili N (2011) Effect of silicon nutrition on oxidative stress induced by Phytophthora melonis infection in cucumber. Plant Diseases 95:455–460
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology 22:867–880
Noorbakhsh Z, Taheri P (2016) Nitric oxide: a signaling molecule which activates cell wall-associated defense of tomato against Rhizoctonia solani. European Journal of Plant Pathology 144:551–568
Orłowska E, Fiil A, Kirk HG, Llorente B, Cvitanich C (2012) Differential gene induction in resistant and susceptible potato cultivars at early stages of infection by Phytophthora infestans. Plant Cell Reports 31:187–203
Polkowska-Kowalczyk L, Wielgat B, Maciejewska U (2004) The elicitor-induced oxidative processes in leaves of Solanum species with differential polygenic resistance to Phytophthora infestans. Journal of Plant Physiology 161:913–920
Polkowska-Kowalczyk L, Wielgat B, Maciejewska U (2007) Changes in the antioxidant status in leaves of Solanum species in response to elicitor from Phytophthora infestans. Journal of Plant Physiology 164:1268–1277
Rastogi A, Pospíšil P (2012) Production of hydrogen peroxide and hydroxyl in potato tuber during the necrotrophic phase of hemibiotrophic pathogen Phytophthora infestans infection. Journal of Photochemistry and Photobiology B: Biology 117:202–206
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor laboratory press. Cold Spring Harbor, New York
SAS Institute Inc., SAS/STATA (2003) Guide for Personal Computers Version 9.1 edition. SAS Institute, Carry NC, USA
Shahbazi H, Aminian H, Sahebani N, Halterman DA (2010) Biochemical evaluation of resistance responses of potato to different isolates of Alternaria solani. Phytopathology 100:454–459
Shetty NP, Kristensen BK, Newmana MA, Moller K, Gregersen PL, Jorgensen HJL (2003) Association of hydrogen peroxide with restriction of Septoria tritici in resistant wheat. Physiological and Molecular Plant Pathology 62:333–346
Shetty NP, Mehrabi R, Lütken H, Haldrup A, Kema GHJ, David B, Collinge DB, Jorgensen HJL (2007) Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytologist 174:637–664
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic phosphotungstic acid reagents. American Journal of Enology and Viticulture 16:144–158
Takahama U (2004) Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: physiological significance of the oxidation reactions. Phytochemical Review 3:207–219
Thomazella DP, Teixeira PJ, Oliveira HC, Saviani EE, Rincones J, Toni IM, Reis O, Garcia O, Meinhardt LW, Salgado I, Pereira GA (2012) The hemibiotrophic cacao pathogen Moniliophthora perniciosa depends on a mitochondrial alternative oxidase for biotrophic development. New Phytologist 194:1025–1034
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain treated bean plants: protective role of exogenous polyamines. Plant Science 151:59–66
Acknowledgments
The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group No. RG-1440-029.
Author information
Authors and Affiliations
Contributions
MHK designed and performed the experiments, collected the data and wrote the manuscript. AAS, YEI, and YYM analyzed the experimental data and helped in writing the manuscript. All authors reviewed the manuscript critically.
Corresponding author
Ethics declarations
Ethical statement
Authors declare that this manuscript have not published elsewhere. All authors read and approved the final version of this manuscript. The authors declare that the present work was developed without any potential conflict of interest, with no human or animal participants.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Leandro J. Dallagnol
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
El_Komy, M.H., Saleh, A.A., Ibrahim, Y.E. et al. Early production of reactive oxygen species coupled with an efficient antioxidant system play a role in potato resistance to late blight. Trop. plant pathol. 45, 44–55 (2020). https://doi.org/10.1007/s40858-019-00318-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40858-019-00318-8