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Effects of Salicylic Acid and Indole Acetic Acid Exogenous Applications on Induction of Faba Bean Resistance against Orobanche crenata

  • Briache, Fatima Zahra (Biotechnology Unit, CRRA-Rabat, National Institute of Agricultural Research (INRA)) ;
  • Ennami, Mounia (Biotechnology Unit, CRRA-Rabat, National Institute of Agricultural Research (INRA)) ;
  • Mbasani-Mansi, Joseph (Biotechnology Unit, CRRA-Rabat, National Institute of Agricultural Research (INRA)) ;
  • Lozzi, Assia (Department of Crop Production, Protection and Biotechnology, Institute of Agronomy and Veterinary Medicine Hassan) ;
  • Abousalim, Abdelhadi (Department of Crop Production, Protection and Biotechnology, Institute of Agronomy and Veterinary Medicine Hassan) ;
  • El Rodeny, Walid (Sakha Agricultural Research Station, Agricultural Research Center (ARC)) ;
  • Amri, Moez (Agro-sciences (AgBS), University Mohammed VI Polytechnic (UM6P)) ;
  • Triqui, Zine El Abidine (Department of Biotechnology and Plant Physiology, Faculty of Sciences, Mohammed V University) ;
  • Mentag, Rachid (Biotechnology Unit, CRRA-Rabat, National Institute of Agricultural Research (INRA))
  • Received : 2020.03.18
  • Accepted : 2020.08.06
  • Published : 2020.10.01

Abstract

The parasitic weed, Orobanche crenata, is one of the most devastating constraint for faba bean production in Mediterranean regions. Plant host defense induction was reported as one of the most appropriate control methods in many crops. The aim of this study was to elucidate the effect of salicylic acid (SA) and indole acetic acid (IAA) on the induction of faba bean resistance to O. crenata under the field and controlled experimental conditions. Both hormones were tested on two contrasting faba bean genotypes: Giza 843 (partially resistant to O. crenata) and Lobab (susceptible) at three different application methods (seed soaking, foliar spray, and the combination of both seed soaking and foliar spray). Soaking seeds in SA or IAA provided the highest protection levels reaching ~75% compared to the untreated control plants. Both elicitors limited the chlorophyll content decrease caused by O. crenata infestation and increased phenolic compound production in host plants. Phenylalanine ammonia lyase, peroxidase, and polyphenol oxidase activities were stimulated in the host plant roots especially in the susceptible genotype Lobab. The magnitude of induction was more obvious in infested than in non-infested plants. Histological study revealed that both SA and IAA decreased the number of attached O. crenata spikes which could be related to specific defense responses in the host plant roots.

Keywords

References

  1. Abbes, Z., Kharrat, M., Delavault, P., Chaibi, W. and Simier, P. 2009. Nitrogen and carbon relationships between the parasitic weed Orobanche foetida and susceptible and tolerant faba bean lines. Plant Physiol. Biochem. 47:153-159. https://doi.org/10.1016/j.plaphy.2008.10.004
  2. Abbes, Z., Kharrat, M., Delavault, P., Simier, P. and Chaibi, W. 2007. Field evaluation of the resistance of some faba bean (Vicia faba L.) genotypes to the parasitic weed Orobanche foetida Poiret. Crop Prot. 26:1777-1784. https://doi.org/10.1016/j.cropro.2007.03.012
  3. Abbes, Z., Mkadmi, M., Trabelsi, I., Amri, M. and Kharrat, M. 2014. Orobanche foetida control in faba bean by foliar application of benzothiadiazole (BTH) and salicylic acid. Bulg. J. Agric. Sci. 20:1439-1443.
  4. Abd El-Aty, M. S. M., El-Galaly, O. A. M. and Soliman, A. A. M. 2016. Heterosis and combining ability for yield, yield components and inheritance of tolerance to Orobanche in Faba bean. Egypt. J. Plant Breed. 20:397-412. https://doi.org/10.12816/0031711
  5. Abu-Irmaileh, B. E. and Labrada, R. 2014. The problem of Orobanche spp. in Africa and Near East Online: Food and Agriculture Organization of the United Nations (FAO) (2014). URL: http://www.fao.org/agriculture/crops/thematic-sitemap/theme/biodiversity/weeds/issues/oro/en/ [1 June 2014].
  6. Achuo, E. A., Audenaert, K., Meziane, H. and Hofte, M. 2004. The salicylic acid-dependent defence pathway is effective against different pathogens in tomato and tobacco. Plant Pathol. 53:65-72. https://doi.org/10.1111/j.1365-3059.2004.00947.x
  7. Al-Wakeel, S. A. M., Moubasher, H., Gabr, M. M. A. and Madany, M. M. Y. 2012. Induction of systemic resistance in tomato plants against Orobanche ramosa L. using hormonal inducers. Egypt. J. Bot. 52:403-416.
  8. Al-Wakeel, S. A. M., Moubasher, H., Gabr, M. M. and Madany, M. M. Y. 2013. Induced systemic resistance: an innovative control method to manage branched broomrape (Orobanche ramosa L.) in tomato. IUFS J. Biol. 72:9-21.
  9. Amri, M., Abbes, Z., Trabelsi, I. and Kharrat, M. 2019. Release of a new faba bean variety "Chourouk" resistant to the parasitic plants Orobanche foetida and O. crenata in Tunisia. Int. J. Agric. Biol. 23:499-505.
  10. Banerjee, A., Das, A. B. and Mittra, B. 2016. Aluminium pretreatment induces activation of defense responses against Fusarium infection in Triticum aestivum. Russ. J. Plant Physiol. 63:483-489. https://doi.org/10.1134/S1021443716040038
  11. Bar-Nun, N., Sachs, T. and Mayer, A. M. 2007. A role for IAA in the infection of Arabidopsis thaliana by Orobanche aegyptiaca. Ann. Bot. 101:261-265. https://doi.org/10.1093/aob/mcm032
  12. Benhamou, N., Gagn, S., Le Quer, D. and Dehbi, L. 2000. Bacterial-mediated induced resistance in cucumber: beneficial effect of the endophytic bacterium Serratia plymuthica on the protection against infection by Pythium ultimum. Phytopathology 90:45-56. https://doi.org/10.1094/PHYTO.2000.90.1.45
  13. Bigirimana, J. and Hofte, M. 2002. Induction of systemic resistance to Colletotrichum lindemuthianum in bean by a benzothiadiazole derivative and rhizobacteria. Phytoparasitica 30:159-168. https://doi.org/10.1007/BF02979698
  14. Briache, F. Z., Ennami, M., Mbasani-Mansi, J., Gaboun, F., Abdelwahd, R., Fatemi, Z. E. A., El-Rodeny, W., Amri, M., Triqui, Z. E. A. and Mentag, R. 2019. Field and controlled conditions screenings of some faba bean (Vicia faba L.) genotypes for resistance to the parasitic plant Orobanche crenata Forsk. and investigation of involved resistance mechanisms. J. Plant Dis. Prot. 126:211-224. https://doi.org/10.1007/s41348-019-00207-x
  15. Burdziej, A., Da Costa, G., Gougeon, L., Le Mao, I., Bellee, A., Corio-Costet, M.-F., Merillon, J.-M., Richard, T., Szakiel, A. and Cluzet, S. 2019. Impact of different elicitors on grapevine leaf metabolism monitored by 1H NMR spectroscopy. Metabolomics 15:67. https://doi.org/10.1007/s11306-019-1530-5
  16. Buschmann, H., Fan, Z.-W. and Sauerborn, J. 2005. Effect of resistance-inducing agents on sunflower (Helianthus annuus L.) and its infestation with the parasitic weed Orobanche cumana Wallr. J. Plant Dis. Prot. 112:386-397.
  17. Chrzanowski, G., Ciepiela, A. P., Sprawka, I., Sempruch, C., Sytykiewicz, H. and Czerniewicz, P. 2003. Activity of polyphenoloxidase in the ears of spring wheat and triticale infested by grain aphid (Sitobion avenae [F.]). Electron. J. Pol. Agric. Univ. 6:1-5.
  18. Clarke, J. D., Volko, S. M., Ledford, H., Ausubel, F. M. and Dong, X. 2000. Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12:2175-2190. https://doi.org/10.1105/tpc.12.11.2175
  19. Durrant, W. E. and Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185-209. https://doi.org/10.1146/annurev.phyto.42.040803.140421
  20. Echevarria-Zomeno, S., Perez-de-Luque, A., Jorrin, J. and Maldonado, A. M. 2006. Pre-haustorial resistance to broomrape (Orobanche cumana) in sunflower (Helianthus annuus): cytochemical studies. J. Exp. Bot. 57:4189-4200. https://doi.org/10.1093/jxb/erl195
  21. Ennami, M., Briache, F. Z., Mansi, J. M., Gaboun, F., Ghaouti, L., Belqadi, L. and Mentag, R. 2017. Genetic diversity of Moroccan Orobanche crenata populations revealed by sequencerelated amplified polymorphism markers. J. Agric. Sci. 9:164-175.
  22. Ennami, M., Mbasani-mansi, J., Briache, F. Z., Oussible, N., Gaboun, F., Ghaouti, L., Belqadi, L., Ghanem, M. E., Aberkani, K., Westwood, J. and Mentag, R. 2020. Growth-defense tradeoffs and source-sink relationship during both faba bean and lentil interactions with Orobanche crenata Forsk. Crop Prot. 127:104924. https://doi.org/10.1016/j.cropro.2019.104924
  23. Fadeel, A. A. 1962. Location and properties of chloroplasts and pigment determination in roots. Physiol. Plant. 15:130-146. https://doi.org/10.1111/j.1399-3054.1962.tb07994.x
  24. Fernandez-Aparicio, M., Reboud, X. and Gibot-Leclerc, S. 2016. Broomrape weeds. Underground mechanisms of parasitism and associated strategies for their control: a review. Front. Plant Sci. 7:135.
  25. Fernandez-Aparicio, M., Kisugi, T., Xie, X., Rubiales, D. and Yoneyama, K. 2014. Low strigolactone root exudation: a novel mechanism of broomrape (Orobanche and Phelipanche spp.) resistance available for faba bean breeding. J. Agric. Food Chem. 62:7063-7071. https://doi.org/10.1021/jf5027235
  26. Fernandez-Aparicio, M., Sillero, J. C., Perez-de-Luque, A. and Rubiales, D. 2008. Identification of sources of resistance to crenate broomrape (Orobanche crenata) in Spanish lentil (Lens culinaris) germplasm. Weed Res. 48:85-94. https://doi.org/10.1111/j.1365-3180.2008.00604.x
  27. Goldwasser, Y., Plakhine, D., Kleifeld, Y., Zamski, E. and Rubin, B. 2000. The differential susceptibility of vetch (Vicia spp.) to Orobanche aegyptiaca: anatomical studies. Ann. Bot. 85:257-262. https://doi.org/10.1006/anbo.1999.1029
  28. Gonsior, G., Buschmann, H., Szinicz, G., Spring, O. and Sauerborn, J. 2004. Induced resistance: an innovative approach to manage branched broomrape (Orobanche ramosa) in hemp and tobacco. Weed Sci. 52:1050-1053. https://doi.org/10.1614/WS-04-088R1
  29. Gravel, V., Antoun, H. and Tweddell, R. J. 2007. Effect of indoleacetic acid (IAA) on the development of symptoms caused by Pythium ultimum on tomato plants. Eur. J. Plant Pathol. 119:457-462. https://doi.org/10.1007/s10658-007-9170-4
  30. Habimana, S., Nduwumuremyi, A. and Chinama, R. J. D. 2014. Management of orobanche in field crops: a review. J. Soil Sci. Plant Nutr. 14:43-62.
  31. Katoch, R., Mann, A. P. S. and Sohal, B. S. 2005. Enhanced enzyme activities and induction of acquired resistance in pea with elicitors. J. Veg. Sci. 11:67-83. https://doi.org/10.1300/J484v11n01_07
  32. Kosesakal, T. and Unal, M. 2009. Role of zinc deficiency in photosynthetic pigments and peroxidase activity of tomato seedlings. IUFS J. Biol. 68:113-120.
  33. Kusumoto, D., Goldwasser, Y., Xie, X., Yoneyama, K., Takeuchi, Y. and Yoneyama, K. 2007. Resistance of red clover (Trifolium pratense) to the root parasitic plant Orobanche minor is activated by salicylate but not by jasmonate. Ann. Bot. 100:537-544. https://doi.org/10.1093/aob/mcm148
  34. Labrousse, P., Arnaud, M. C., Griveau, Y., Fer, A. and Thalouarn, P. 2004. Analysis of resistance criteria of sunflower recombined inbred lines against Orobanche cumana Wallr. Crop Prot. 23:407-413. https://doi.org/10.1016/j.cropro.2003.09.013
  35. Lopez, A. M. Q. and Lucas, J. A. 2002. Effects of plant defence activators on anthracnose disease of cashew. Eur. J. Plant Pathol. 108:409-420. https://doi.org/10.1023/A:1016010710703
  36. Mandal, S. and Mitra, A. 2007. Reinforcement of cell wall in roots of Lycopersicon esculentum through induction of phenolic compounds and lignin by elicitors. Physiol. Mol. Plant Pathol. 71:201-209. https://doi.org/10.1016/j.pmpp.2008.02.003
  37. Monci, F., Garcia-Andres, S., Sanchez-Campos, S., Fernandez-Munoz, R., Diaz-Pendon, J. A. and Moriones, E. 2019. Use of systemic acquired resistance and whitefly optical barriers to reduce tomato yellow leaf curl disease damage to tomato crops. Plant Dis. 103:1181-1188. https://doi.org/10.1094/PDIS-06-18-1069-RE
  38. Nascimento, K. J. T., Debona, D., Franca, S. K. S., Goncalves, M. G. M., DaMatta, F. M. and Rodrigues, F. 2014. Soybean resistance to Cercospora sojina infection is reduced by silicon. Phytopathology 104:1183-1191. https://doi.org/10.1094/PHYTO-02-14-0047-R
  39. Ojha, S. and Chatterjee, N. C. 2012. Induction of resistance in tomato plants against Fusarium oxysporum f. sp. lycopersici mediated through salicylic acid and Trichoderma harzianum. J. Plant Prot. Res. 52:220-225.
  40. Passardi, F., Penel, C. and Dunand, C. 2004. Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci. 9:534-540. https://doi.org/10.1016/j.tplants.2004.09.002
  41. Perez-de-Luque, A., Eizenberg, H., Grenz, J. H., Sillero, J. C., Avila, C., Sauerborn, J. and Rubiales, D. 2010. Broomrape management in faba bean. Field Crops Res. 115:319-328. https://doi.org/10.1016/j.fcr.2009.02.013
  42. Perez-de-Luque, A., Gonzalez-Verdejo, C. I., Lozano, M. D., Dita, M. A., Cubero, J. I., Gonzalez-Melendi, P., Risueno, M. C. and Rubiales, D. 2006. Protein cross-linking, peroxidase and ${\beta}$-1,3-endoglucanase involved in resistance of pea against Orobanche crenata. J. Exp. Bot. 57:1461-1469. https://doi.org/10.1093/jxb/erj127
  43. Perez-de-Luque, A., Jorrin, J. V. and Rubiales, D. 2004. Crenate broomrape control in pea by foliar application of benzothiadiazole (BTH). Phytoparasitica 32:21. https://doi.org/10.1007/BF02980855
  44. Perez-de-Luque, A., Rubiales, D., Cubero, J. I., Press, M. C., Scholes, J., Yoneyama, K., Takeuchi, Y., Plakhine, D. and Joel, D. M. 2005. Interaction between Orobanche crenata and its host legumes: unsuccessful haustorial penetration and necrosis of the developing parasite. Ann. Bot. 95:935-942. https://doi.org/10.1093/aob/mci105
  45. Perez, L., Rodriguez, M. E., Rodriguez, F. and Roson, C. 2003. Efficacy of acibenzolar-S-methyl, an inducer of systemic acquired resistance against tobacco blue mould caused by Peronospora hyoscyami f. sp. tabacina. Crop Prot. 22:405-413. https://doi.org/10.1016/S0261-2194(02)00198-9
  46. Polle, A., Otter, T. and Seifert, F. 1994. Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol. 106:53-60. https://doi.org/10.1104/pp.106.1.53
  47. Pradeep, T. and Jambhale, N. D. 2012. Relationship between phenolics, polyphenol oxidase and peroxidases and resistance to powdery mildew in Zizhyphus. Indian Phytopathol. 55:195-196.
  48. Raasch-Fernandes, L. D., Bonaldo, S. M., de Jesus Rodrigues, D., Vieira-Junior, G. M., Schwan-Estrada, K. R. F., da Silva, C. R., Vercosa, A. G. A., de Oliveira, D. L. and Debiasi, B. W. 2019. Induction of phytoalexins and proteins related to pathogenesis in plants treated with extracts of cutaneous secretions of southern Amazonian Bufonidae amphibians. PLoS ONE 14:e0211020. https://doi.org/10.1371/journal.pone.0211020
  49. Ragab, M. M. M., Saber, M. M., El-Morsy, S. A. and El-Aziz, A. R. M. A. 2009. Induction of systemic resistance against root rot of basil using some chemical inducers. Egypt. J. Phytopathol. 37:59-70.
  50. Ramakrishna, R., Sarkar, D. and Shetty, K. 2019. Metabolic stimulation of phenolic biosynthesis and antioxidant enzyme response in dark germinated barley (Hordeum vulgare L.) sprouts using bioprocessed elicitors. Food Sci. Biotechnol. 28:1093-1106. https://doi.org/10.1007/s10068-018-0535-6
  51. Reddy, A. R., Chaitanya, K. V., Jutur, P. P. and Sumithra, K. 2004. Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environ. Exp. Bot. 52:33-42. https://doi.org/10.1016/j.envexpbot.2004.01.002
  52. Rispail, N., Dita, M.-A., Gonzalez-Verdejo, C., Perez-de-Luque, A., Castillejo, M.-A., Prats, E., Roman, B., Jorrin, J. and Rubiales, D. 2007. Plant resistance to parasitic plants: molecular approaches to an old foe. New Phytol. 173:703-712. https://doi.org/10.1111/j.1469-8137.2007.01980.x
  53. Rubiales, D. 2018. Can we breed for durable resistance to broomrapes? Phytopathol. Mediterr. 57:170-185.
  54. Rubiales, D. and Fernandez-Aparicio, M. 2012. Innovations in parasitic weeds management in legume crops: a review. Agron. Sustain. Dev. 32:433-449. https://doi.org/10.1007/s13593-011-0045-x
  55. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H.-Y. and Hunt, M. D. 1996. Systemic acquired resistance. Plant Cell 8:1809-1819. https://doi.org/10.2307/3870231
  56. Sauerborn, J., Buschmann, H., Ghiasi, K. G. and Kogel, K.-H. 2002. Benzothiadiazole activates resistance in sunflower (Helianthus annuus) to the root-parasitic weed Orobanche cuman. Phytopathology 92:59-64. https://doi.org/10.1094/PHYTO.2002.92.1.59
  57. Sestak, Z. 1971. Determination of chlorophyll a and b. In: Plant photosynthetic production: manual of methods, eds. by Z. Sestak, J. Catsk and P. G. Jarvis, pp. 672-697. Junk N.V., The Hague, Netherlands.
  58. Sillero, J. C., Rojas-Molina, M. M., Avila, C. M. and Rubiales, D. 2012. Induction of systemic acquired resistance against rust, ascochyta blight and broomrape in faba bean by exogenous application of salicylic acid and benzothiadiazole. Crop Prot. 34:65-69. https://doi.org/10.1016/j.cropro.2011.12.001
  59. Sindelarova, M., Sindelar, L. and Burketova, L. 2002. Glucose-6-phosphate dehydrogenase, ribonucleases and esterases upon tobacco mosaic virus infection and benzothiodiazole treatment in tobacco. Biol. Plant. 45:423-432. https://doi.org/10.1023/A:1016277919634
  60. Singleton, V. L., Orthofer, R. and Lamuela-Raventos, R. M. 1999. [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol. 299:152-178. https://doi.org/10.1016/S0076-6879(99)99017-1
  61. Smirnoff, N. 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 125:27-58. https://doi.org/10.1111/j.1469-8137.1993.tb03863.x
  62. Solecka, D. and Kacperska, A. 2003. Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiol. Plant. 119:253-262. https://doi.org/10.1034/j.1399-3054.2003.00181.x
  63. Stalikas, C. D. 2007. Extraction, separation, and detection methods for phenolic acids and flavonoids. J. Sep. Sci. 30:3268-3295. https://doi.org/10.1002/jssc.200700261
  64. Thakur, M. and Sohal, B. S. 2013. Role of elicitors in inducing resistance in plants against pathogen infection: a review. ISRN Biochem. 2013:762412. https://doi.org/10.1155/2013/762412
  65. Trabelsi, I., Yoneyama, K., Abbes, Z., Amri, M., Xie, X., Kisugi, T., Kim, H. I. and Kharrat, M. 2017. Characterization of strigolactones produced by Orobanche foetida and Orobanche crenata resistant faba bean (Vicia faba L.) genotypes and effects of phosphorous, nitrogen, and potassium deficiencies on strigolactone production. S. Afr. J. Bot. 108:15-22. https://doi.org/10.1016/j.sajb.2016.09.009
  66. Triki, E., Trabelsi, I., Amri, M., Nefzi, F., Kharrat, M. and Abbes, Z. 2018. Effect of benzothiadiazole and salicylic acid resistance inducers on Orobanche foetida infestation in Vicia faba. Tunis. J. Plant Prot. 13:113-125.
  67. Ueno, M., Kumura, Y., Ueda, K., Kihara, J. and Arase, S. 2011. Indole derivatives enhance resistance against the rice blast fungus Magnaporthe oryzae. J. Gen. Plant Pathol. 77:209-213. https://doi.org/10.1007/s10327-011-0300-7
  68. Veronesi, C., Delavault, P. and Simier, P. 2009. Acibenzolar-Smethyl induces resistance in oilseed rape (Brassica napus L.) against branched broomrape (Orobanche ramosa L.). Crop Prot. 28:104-108. https://doi.org/10.1016/j.cropro.2008.08.014
  69. Walters, D. R. and Fountaine, J. M. 2009. Practical application of induced resistance to plant diseases: an appraisal of effectiveness under field conditions. J. Agric. Sci. 147:523-535. https://doi.org/10.1017/S0021859609008806
  70. Walters, D. R., Ratsep, J. and Havis, N. D. 2013. Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64:1263-1280. https://doi.org/10.1093/jxb/ert026
  71. Wang, Y. and Zhang, Y. 2010. Salicylic acid induces the accumulation of defense-related enzymes in Whangkeumbae pear and protects from pear black spot. Front. Agric. China 4:215-219. https://doi.org/10.1007/s11703-010-0002-5
  72. Xu, B. J. and Chang, S. K. C. 2007. A comparative study on phenolic profiles and antioxidant activities of legumes as affected by extraction solvents. J. Food Sci. 72:S159-S166. https://doi.org/10.1111/j.1750-3841.2006.00260.x
  73. Yamunarani, K., Jaganathan, R., Bhaskaran, R., Govindaraju, P. and Velazhahan, R. 2004. Induction of early blight resistance in tomato by Quercus infectoria gall extract in association with accumulation of phenolics and defense-related enzymes. Acta Physiol. Plant. 26:281-290. https://doi.org/10.1007/s11738-004-0018-7