Inhibitory effect of different plant growth regulators on blue mold disease in apple (Malus × domestica Borkh.)
Subject Areas : Genetic
Mansureh
Keshavarzi
1
(Cold and Temperate Fruits Research Center, Horticultural Science Research Institute, Agricultural Research, Education and Extension Organization, Karaj, IranIran)
Saeid
Mirzaei
2
(Department of Biotechnology, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran)
Masoud
Ahmadi-Afzadi
3
(Department of Biotechnology, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran)
Keywords: Resistance, apple, physiology, Plant growth regulator, blue mold,
Abstract :
Apple (Malus × domestica Borkh.) is one of the most economically important crops which is widely used either as fresh fruit or as processed foods. Apple fruit is usually introduced to the markets after a storage period of several months. This makes it important to protect fruits against the post-harvest diseases specially in organic production. Blue mold (Penicillium expansum) is one of these diseases, which due to spreading very fast in storage and producing a carcinogenic compound, called patulin, is of particular importance. In the present study, the impact of methyl jasmonate, abscisic acid, salicylic acid, beta-aminobutyric acid, and carbocyclic acid sprayed was investigated on blue mold. Apple fruits of 10 cultivars were surface sterilized and inoculated with spores of fungus, and then were treated with the plant growth regulators. The fruit firmness, softening rate and lesion decay were evaluated. Data were analyzed in a factorial design with two factors i.e., cultivar and plant growth regulator in a completely randomized design in R software package. The impact of hormones was significant on controlling the blue mold, and three plant growth regulators, methyl jasmonate, salicylic acid, and beta-amino butyric acid had the greatest inhibitory impact on the disease. Carboxylic acid and abscisic acid had contradictory impacts on different cultivars, and did not result in significant impacts in some cultivars. The results of this study can be used in the breeding programs in order to help better understand plant disease mechanisms. They can also be applied as a practical method to control blue mold in apple.
Ahmadi-Afzadi, M. (2015). Genetic variation in resistance to fungal storage diseases in apple. Inoculation-cased screening, transcriptomics and biochemistry. (PhD Thesis), Swedish University of Agricultural Sciencs. ( Vol. 18).
Ahmadi-Afzadi, M., Nybom, H., Ekholm, A., Tahir, I. and Rumpunen, K. (2015). Biochemical contents of apple peel and flesh affect level of partial resistance to blue mold. Postharvest Biology and Technology. 110: 173-182.
Ahmadi-Afzadi, M., Orsel, M., Pelletier, S., Bruneau, M., Proux-Wéra, E., Nybom, H. (2018). Genome-wide expression analysis suggests a role for jasmonates in the resistance to blue mold in apple. Plant Growth Regulation. 85: 375-387.
Ahmadi-Afzadi, M., Tahir, I. and Nybom, H. (2013). Impact of harvesting time and fruit firmness on the tolerance to fungal storage diseases in an apple germplasm collection. Postharvest Biology and Technology. 82: 51-58.
Babalar, M., Asghari, M., Talaei, A. and Khosroshahi, A. (2007). Effect of pre-& postharvest Salicylic acid treatment on ethylene production, fungal decay & overall quality of Selva strawberry fruit. Food Chemistry. 105: 449-453.
Barreira, M. J., Alvito, P. C. and Almeida, C. M. M. (2010). Occurrence of patulin in apple-based-foods in Portugal. Food Chemistry. 121: 653-658.
Beretta, B., Gaiaschi, A., Galli, C. L. and Restani, P. (2000). Patulin in apple-based foods: occurrence and safety evaluation. Food Additives and Contaminants. 17: 399-406.
Brown, S. K. and Maloney, K. (2005). Malus × domestica Apple. In R. E. ILitz (Ed.), Biotechnology of fruit and nut crops (pp. 475-511). Cambrige: CABI Publishing, CAB international, UK.
Conway, W. S., Janisiewicz, W. J., Leverentz, B., Saftner, R. A. and Camp, M. (2007). Control of blue mold of apple by combining controlled atmosphere, an antagonist mixture, and sodium bicarbonate. Postharvest Biology and Technology. 45: 326-332.
Conway, W. S., Sams, C. E., and Hickey, K. D. (2002). Pre- and postharvest calcium treatment of apple fruit and its effect on quality. Proceedings of the International Symposium on Plants as Food and Medicine: The Utilization and Development of Horticultural Plants for Human Health. 594: 413-419.
Costa, F., Peace, C. P., Stella, S., Serra, S., Musacchi, S., Bazzani, M., et al. (2010). QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malus x domestica Borkh.). Journal of Experimental Botany. 61: 3029-3039.
Denancé, N., Sánchez-Vallet, A., Goffner, D. and Molina, A. (2013). Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Frontiers in plant science, 4: 155-161.
Dubery, I. A., Sanabria, N. M. and Huang, J. C. (2012). Nonself perception in plant innate immunity. In Self and nonself (pp. 79-107): Springer, New York, NY.
Ferguson, I., Volz, R. and Woolf, A. (1999). Preharvest factors affecting physiological disorders of fruit. Postharvest Biology and Technology. 15: 255-262.
Hajnajari, H., Tarrahi, S. and Ghahremani, Z. (2010). Correlation of vegetative traits with fire blight resistance in Iranian and imported apple cultivars. XII International Workshop on Fire Blight. 896: 347-352.
Hemmatjo Mahmoudalilo, B. (2016). Effect of postharvest treatment with gamma-aminobutyric acid and salicylic acids on quality and storage life of Shablon plum (Prunus salicina L.). Department of Horticulture, University of Urmia. Pp: 113. In Persian.
Hyson, D. A. (2011). A comprehensive review of apples and apple components and their relationship to human health. Advances in Nutrition. 2: 408-420.
Janick, J., Cummins, J. N., Brown, S. K. and Hemmat, M. (1996). Apples. In J. Janick & J. N. Moore (Eds.), Fruit breeding, tree and tropical fruits.(pp. 1-78): John Wiley & Sons, Inc. UK.
Janisiewicz, W. and Marchi, A. (1992). Control of storage rots on various pear cultivars with saprophytic strain of Pseudomonas syringae. Plant Disease. 76: 555-560.
Jijakli, M. H. and Lepoivre, P. (2004). State of the art and challenges of post-harvest disease management in apples. In K. G. Mukerji (Ed.), Fruit and vegetable diseases. 1: 59-94.
Jones, A. L. and Aldwinckle, H. S. (1990). Compendium of apple and pear diseases: APS Press.pp 1-100.
Jurick, W. M., Janisiewicz, W. J., Saftner, R. A., Vico, I., Gaskins, V. L., Park, E., et al. (2011). Identification of wild apple germplasm (Malus spp.) accessions with resistance to the postharvest decay pathogens Penicillium expansum and Colletotrichum acutatum. Plant Breeding. 130: 481-486.
Kim, D. S. and Hwang, B. K. (2014). An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. Journal of Experimental Botany. 65: 2295-2306.
Leon-Reyes, A., Du, Y., Koornneef, A., Proietti, S., Körbes, A. P. and Memelink, J. (2010). Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Molecular Plant-Microbe Interactions. 23: 187-197.
Martins, C. R., Hoffmann, A., Rombaldi, C. V., Farias, R. D. and Teodoro, A. V. (2013). Apple biological and physiological disorders in the orchard and in postharvest according to production system. Revista Brasileira De Fruticultura. 35: 1-8.
Mo, Y., Gong, D., Liang, G., Han, R., Xie, J. and Li, W. (2008). Enhanced preservation effect of sugar apple fruits by salicylic acid treatment during postharvest storage. Journal of the Science of Food and Agriculture. 88: 2693-2699.
Naeem Abadi, T., Keshavarzi, M., Alaee, H., Hajnagari, H. and Hoseinava, S. (2014). Blue Mold (Penicillium expansum) decay resistance in apple cultivars, and its association with fruit physicochemical traits. Journal of Agricultural Science and Technology. 16: 635-644.
Rahaie, M., Gang-Ping, X. and Schenk, P.M. (2013). The role of transcription factors in wheat under different abiotic stresses. Abiotic Stress - Plant Responses and Applications in Agriculture. 367-387.
Ranjbaran, E. (2010). Effect of salicylic acid on postharvest life and some quality charactristics in table grapes, cvs. Bidaneh Sefid and Bidaneh Ghermez. MSc Thesis, Department of Horticultural Science, Bu-Ali Sina University. Pp: 89. In Persian.
Robert-Seilaniantz, A., Grant, M. and Jones, J. D. (2011). Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology. 49: 317-343.
Sansavini, S., Donati, F., Costa, F. and Tartarini, S. (2004). Advances in apple breeding for enhanced fruit quality and resistance to biotic stresses: new varieties for the European market. Journal of fruit and ornamental plant research. 12: 13-52.
Schovankova, J. and Opatova, H. (2011). Changes in phenols composition and activity of phenylalanine-ammonia lyase in apples after fungal infections. Horticultural Science. 38: 1-10.
Smith, R. B., Loucheede, E. C., Franklin, E. W. and McMillan, I. (1979). The starch-iodine test for determining stage of maturation in apples. Canadian Journal of Plant Science. 59: 725-735.
Solano, R. and Gimenez-Ibanez, S. (2013). Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Frontiers in plant science. 4: 72.
Taherpoor, K. (2016). Effect of methyl jasmonate on cold tolerance of apple (Malus domestica) flowers cv. Golden Delicious. MSc Thesis, Department of Horticultural Sciences, Bu-Ali Sina University. Pp: 89. In Persian.
Tahir, I., Nybom, H., Ahmadi-Afzadi, M., Roen, K., Sehic, J. and Roen, D. (2015). Susceptibility to blue mold caused by Penicillium expansum in apple cultivars adapted to a cool climate. European Journal of Horticultural Sciences. 80: 117-127.
Van der Does, D., Leon-Reyes, A., Koornneef, A., Van Verk, M. C., Rodenburg, N., Pauwels, L., et al. (2013). Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. The Plant Cell. 25: 744-761.
Vidhyasekaran, P. (2015). Plant hormone signaling systems in plant innate immunity: Springer, Dordrecht, Netherlands.
Wang, L., Chen, S., Kong, W., Li, S. and Archbold, D.D. (2006). Salicylic acid pre treatment alleviates chilling injury and affects the anti oxidant system and heat shock proteins of peaches during cold storage. Postharvest Biology and Technology. 41: 244-251.
Weber, R. W. S. (2009). An evaluation of possible effects of climate change on pathogenic fungi in apple production using fruit rots as examples. Erwerbs-Obstbau. 51: 115-120.
Xu, J., Audenaert, K., Hofte, M. and De Vleesschauwer, D. (2013). Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses. Plos One. 8, e67413.
Yang, D.-L., Yang, Y. and He, Z. (2013). Roles of plant hormones and their interplay in rice immunity. Molecular plant. 6: 675-685.
Yao, H. J. and Tian, S. P. (2005). Effects of pre- and post-harvest application of salicylic acid or methyl jasmonate on inducing disease resistance of sweet cherry fruit in storage. Postharvest Biology and Technology. 35: 253-262.
Yoshioka, K., Nakashita, H., Klessig, D. F. and Yamaguchi, I. (2001). Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. The Plant Journal. 25: 149-157.
Zhang, X., Wang, C., Zhang, Y., Sun, Y. and Mou, Z. (2012). The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. The Plant Cell. 24: 4294-4309.
Zhang, Y., Lubberstedt, T. and Xu, M. L. (2013). The genetic and molecular basis of plant resistance to pathogens. Journal of Genetics and Genomics. 40: 23-35.
Zhu, Z., An, F., Feng, Y., Li, P., Xue, L., Mu, A., et al. (2011). Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proceedings of the National Academy of Sciences. 108: 12539-12544.
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Ahmadi-Afzadi, M. (2015). Genetic variation in resistance to fungal storage diseases in apple. Inoculation-cased screening, transcriptomics and biochemistry. (PhD Thesis), Swedish University of Agricultural Sciencs. ( Vol. 18).
Ahmadi-Afzadi, M., Nybom, H., Ekholm, A., Tahir, I. and Rumpunen, K. (2015). Biochemical contents of apple peel and flesh affect level of partial resistance to blue mold. Postharvest Biology and Technology. 110: 173-182.
Ahmadi-Afzadi, M., Orsel, M., Pelletier, S., Bruneau, M., Proux-Wéra, E., Nybom, H. (2018). Genome-wide expression analysis suggests a role for jasmonates in the resistance to blue mold in apple. Plant Growth Regulation. 85: 375-387.
Ahmadi-Afzadi, M., Tahir, I. and Nybom, H. (2013). Impact of harvesting time and fruit firmness on the tolerance to fungal storage diseases in an apple germplasm collection. Postharvest Biology and Technology. 82: 51-58.
Babalar, M., Asghari, M., Talaei, A. and Khosroshahi, A. (2007). Effect of pre-& postharvest Salicylic acid treatment on ethylene production, fungal decay & overall quality of Selva strawberry fruit. Food Chemistry. 105: 449-453.
Barreira, M. J., Alvito, P. C. and Almeida, C. M. M. (2010). Occurrence of patulin in apple-based-foods in Portugal. Food Chemistry. 121: 653-658.
Beretta, B., Gaiaschi, A., Galli, C. L. and Restani, P. (2000). Patulin in apple-based foods: occurrence and safety evaluation. Food Additives and Contaminants. 17: 399-406.
Brown, S. K. and Maloney, K. (2005). Malus × domestica Apple. In R. E. ILitz (Ed.), Biotechnology of fruit and nut crops (pp. 475-511). Cambrige: CABI Publishing, CAB international, UK.
Conway, W. S., Janisiewicz, W. J., Leverentz, B., Saftner, R. A. and Camp, M. (2007). Control of blue mold of apple by combining controlled atmosphere, an antagonist mixture, and sodium bicarbonate. Postharvest Biology and Technology. 45: 326-332.
Conway, W. S., Sams, C. E., and Hickey, K. D. (2002). Pre- and postharvest calcium treatment of apple fruit and its effect on quality. Proceedings of the International Symposium on Plants as Food and Medicine: The Utilization and Development of Horticultural Plants for Human Health. 594: 413-419.
Costa, F., Peace, C. P., Stella, S., Serra, S., Musacchi, S., Bazzani, M., et al. (2010). QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malus x domestica Borkh.). Journal of Experimental Botany. 61: 3029-3039.
Denancé, N., Sánchez-Vallet, A., Goffner, D. and Molina, A. (2013). Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Frontiers in plant science, 4: 155-161.
Dubery, I. A., Sanabria, N. M. and Huang, J. C. (2012). Nonself perception in plant innate immunity. In Self and nonself (pp. 79-107): Springer, New York, NY.
Ferguson, I., Volz, R. and Woolf, A. (1999). Preharvest factors affecting physiological disorders of fruit. Postharvest Biology and Technology. 15: 255-262.
Hajnajari, H., Tarrahi, S. and Ghahremani, Z. (2010). Correlation of vegetative traits with fire blight resistance in Iranian and imported apple cultivars. XII International Workshop on Fire Blight. 896: 347-352.
Hemmatjo Mahmoudalilo, B. (2016). Effect of postharvest treatment with gamma-aminobutyric acid and salicylic acids on quality and storage life of Shablon plum (Prunus salicina L.). Department of Horticulture, University of Urmia. Pp: 113. In Persian.
Hyson, D. A. (2011). A comprehensive review of apples and apple components and their relationship to human health. Advances in Nutrition. 2: 408-420.
Janick, J., Cummins, J. N., Brown, S. K. and Hemmat, M. (1996). Apples. In J. Janick & J. N. Moore (Eds.), Fruit breeding, tree and tropical fruits.(pp. 1-78): John Wiley & Sons, Inc. UK.
Janisiewicz, W. and Marchi, A. (1992). Control of storage rots on various pear cultivars with saprophytic strain of Pseudomonas syringae. Plant Disease. 76: 555-560.
Jijakli, M. H. and Lepoivre, P. (2004). State of the art and challenges of post-harvest disease management in apples. In K. G. Mukerji (Ed.), Fruit and vegetable diseases. 1: 59-94.
Jones, A. L. and Aldwinckle, H. S. (1990). Compendium of apple and pear diseases: APS Press.pp 1-100.
Jurick, W. M., Janisiewicz, W. J., Saftner, R. A., Vico, I., Gaskins, V. L., Park, E., et al. (2011). Identification of wild apple germplasm (Malus spp.) accessions with resistance to the postharvest decay pathogens Penicillium expansum and Colletotrichum acutatum. Plant Breeding. 130: 481-486.
Kim, D. S. and Hwang, B. K. (2014). An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. Journal of Experimental Botany. 65: 2295-2306.
Leon-Reyes, A., Du, Y., Koornneef, A., Proietti, S., Körbes, A. P. and Memelink, J. (2010). Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Molecular Plant-Microbe Interactions. 23: 187-197.
Martins, C. R., Hoffmann, A., Rombaldi, C. V., Farias, R. D. and Teodoro, A. V. (2013). Apple biological and physiological disorders in the orchard and in postharvest according to production system. Revista Brasileira De Fruticultura. 35: 1-8.
Mo, Y., Gong, D., Liang, G., Han, R., Xie, J. and Li, W. (2008). Enhanced preservation effect of sugar apple fruits by salicylic acid treatment during postharvest storage. Journal of the Science of Food and Agriculture. 88: 2693-2699.
Naeem Abadi, T., Keshavarzi, M., Alaee, H., Hajnagari, H. and Hoseinava, S. (2014). Blue Mold (Penicillium expansum) decay resistance in apple cultivars, and its association with fruit physicochemical traits. Journal of Agricultural Science and Technology. 16: 635-644.
Rahaie, M., Gang-Ping, X. and Schenk, P.M. (2013). The role of transcription factors in wheat under different abiotic stresses. Abiotic Stress - Plant Responses and Applications in Agriculture. 367-387.
Ranjbaran, E. (2010). Effect of salicylic acid on postharvest life and some quality charactristics in table grapes, cvs. Bidaneh Sefid and Bidaneh Ghermez. MSc Thesis, Department of Horticultural Science, Bu-Ali Sina University. Pp: 89. In Persian.
Robert-Seilaniantz, A., Grant, M. and Jones, J. D. (2011). Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology. 49: 317-343.
Sansavini, S., Donati, F., Costa, F. and Tartarini, S. (2004). Advances in apple breeding for enhanced fruit quality and resistance to biotic stresses: new varieties for the European market. Journal of fruit and ornamental plant research. 12: 13-52.
Schovankova, J. and Opatova, H. (2011). Changes in phenols composition and activity of phenylalanine-ammonia lyase in apples after fungal infections. Horticultural Science. 38: 1-10.
Smith, R. B., Loucheede, E. C., Franklin, E. W. and McMillan, I. (1979). The starch-iodine test for determining stage of maturation in apples. Canadian Journal of Plant Science. 59: 725-735.
Solano, R. and Gimenez-Ibanez, S. (2013). Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Frontiers in plant science. 4: 72.
Taherpoor, K. (2016). Effect of methyl jasmonate on cold tolerance of apple (Malus domestica) flowers cv. Golden Delicious. MSc Thesis, Department of Horticultural Sciences, Bu-Ali Sina University. Pp: 89. In Persian.
Tahir, I., Nybom, H., Ahmadi-Afzadi, M., Roen, K., Sehic, J. and Roen, D. (2015). Susceptibility to blue mold caused by Penicillium expansum in apple cultivars adapted to a cool climate. European Journal of Horticultural Sciences. 80: 117-127.
Van der Does, D., Leon-Reyes, A., Koornneef, A., Van Verk, M. C., Rodenburg, N., Pauwels, L., et al. (2013). Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. The Plant Cell. 25: 744-761.
Vidhyasekaran, P. (2015). Plant hormone signaling systems in plant innate immunity: Springer, Dordrecht, Netherlands.
Wang, L., Chen, S., Kong, W., Li, S. and Archbold, D.D. (2006). Salicylic acid pre treatment alleviates chilling injury and affects the anti oxidant system and heat shock proteins of peaches during cold storage. Postharvest Biology and Technology. 41: 244-251.
Weber, R. W. S. (2009). An evaluation of possible effects of climate change on pathogenic fungi in apple production using fruit rots as examples. Erwerbs-Obstbau. 51: 115-120.
Xu, J., Audenaert, K., Hofte, M. and De Vleesschauwer, D. (2013). Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses. Plos One. 8, e67413.
Yang, D.-L., Yang, Y. and He, Z. (2013). Roles of plant hormones and their interplay in rice immunity. Molecular plant. 6: 675-685.
Yao, H. J. and Tian, S. P. (2005). Effects of pre- and post-harvest application of salicylic acid or methyl jasmonate on inducing disease resistance of sweet cherry fruit in storage. Postharvest Biology and Technology. 35: 253-262.
Yoshioka, K., Nakashita, H., Klessig, D. F. and Yamaguchi, I. (2001). Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. The Plant Journal. 25: 149-157.
Zhang, X., Wang, C., Zhang, Y., Sun, Y. and Mou, Z. (2012). The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. The Plant Cell. 24: 4294-4309.
Zhang, Y., Lubberstedt, T. and Xu, M. L. (2013). The genetic and molecular basis of plant resistance to pathogens. Journal of Genetics and Genomics. 40: 23-35.
Zhu, Z., An, F., Feng, Y., Li, P., Xue, L., Mu, A., et al. (2011). Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proceedings of the National Academy of Sciences. 108: 12539-12544.