The morphological and physiological traits of Cucumis sativus- Phelipanche aegyptiaca association affected by arbuscular mycorrhizal fungi symbiosis

Volume 10, Issue 4
December 2021
Pages 669-684

Document Type : Original Research

Authors

1 Department of Agrotechnology, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran.

2 Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan University of Technology, Isfahan, Iran.

Abstract
The plant symbiotic fungi, Arbuscular mycorrhizae (AM), increases host competency and causes partial control of Egyptian broomrape Phelipanche aegyptiaca (Orobanchaceae). In this study, a greenhouse experiment was designed to investigate the AM efficacy on the morphological and physiological traits in the association of cucumber and P. aegyptiaca. Findings showed that the broomrape contamination increased the activity of ascorbate, peroxidase, and catalase in cucumber. In contrast, AM decreased ascorbate, peroxidase activity and increased total phenolic compounds. However, AM in P. aegyptiaca-infected genotypes had no significant effect on malondialdehyde and hydrogen peroxide content. In AM inoculated treatments, the height and number of cucumber leaves were unaffected by P. aegyptiaca infestation. Also, AM decreased the harmful effects of the P. aegyptiaca by reducing the total dry weight and number of attachments, increasing the leaf area, the shoot, and the dry root weight of cucumber genotypes. Despite the positive effect of AM, about 35 and 50% reduction in shoot and dry root weight of cucumber indicated high susceptibility of the host. Overall, It seems that the AM cannot be effective as a primary broomrape control strategy in cucumber.

Keywords

Subjects
Aebi, H. 1983. Catalase in vitro. Methods in Enzymology, 105:121-126.
Albrecht, C., Burgess, T., Dell, B. and Lapeyrie, F. 1994. Chitinase and peroxidase activities are induced in eucalyptus roots according to aggressiveness of Australian ectomycorrhizal strains of Pisolithus sp. New Phytologist, 127:217–222.
Al-karaki, G. N. 2006. Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Scientia Horticulture, 109: 1-7.
Antonova, T.S. and Ter Borg, S.J. 1996. The role of peroxidase in the resistance of sunflower against Orobanche cumana in Russia. Weed Research, 36: 113–121.
Angeles Castillejo, M., Amiour, N., Dumas-Gaudot, E., Rubiales, D. and Jorrın, V. 2004. A proteomic approach to studying plant response to crenate broomrape (Orobanche crenata) in pea (Pisum sativum). Phytochemistry, 65(12): 1817–1828.
Baum, C., El-Tohamy, W. and Gruda, B. 2015. Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: A review. Scientia Horticulturae, 187 : 131–141
Bocova, B., Huttova, J., Liptakova, L., Mistrık, I., Olle, M. and Tamas, L. 2012. Impact of short term cadmium treatment on catalase and ascorbate peroxidase activities in barley root tips. Plant Biology, 56(4): 724-728.
Boyer, F., Saint germain, A. Pouvreau, J. and Clave, G. 2013. New Strigolactone Analogs as Plant Hormones with Low Activities in the Rhizosphere. Molecular plant. 8:1-17.
Brewer, P. B., Koltai, H. and Beveridge, C.A. 2013. Diverse roles of strigolactones in plant development. Molecular plant. 6: 18–28.
Cagras, S., Sari, N. and Ortas, I. 2000. The effects of vesicular-arbuscular mycorrhizae on the plant growth and nutrient uptake of cucumber. Turkish Journal of Agriculture and Forestry, 24:571-578.
Chance, B. and Maehly, A.C. 1955. Assay of Catalase and Peroxidase. Methods in Enzymology, 2: 764-775.
Charron, G., Furlan, V., Bernier, M. and Doyon, G. 2001. Response of onion plants to arbuscular mycorrhizae. 2. Effects of inoculum method and phosphorus fertilization on biomass and bulp firmness. Mycorrhiza, 11:187-197.
Criquet, S., Joner, E., Leglize, P. and Leyval, C. 2000. Anthracene and mycorrhiza affect the activity of oxidoreductase in the roots and rhizosphere of lucerne (Medicago sativa L.). Biotechnology Letters, 22:1733–1737.
Demirbas, S. and Okan, A. 2017. Physiological and biochemical defence reactions of Arabidopsis thalana to Phelipanche ramosa infection and salt stress. Fresenius Environmentah Bulletine, 26(3): 2275-2268.
El-Halmouch, Y., Benharrat, H. and Thalouarn, P. 2006. Effect of root exudates from different tomato genotypes onbroomrape (O. aegyptiaca) seed germination and tubercle development. Crop Protection, 25: 501–507.
Goldwasser, Y. H., Eizenberg, H., Golan, S. and Kleinfeld Y. 2003. Control of Orobanche crenata and Orobanche aegyptiaca in parsley. Crop Protection, 22: 295–305.
Goldwasser, Y., Kleifeld, Y. 2002. Tolerance of parsley varieties to Orobanche. Crop Protection, 21: 1101-1107 https://doi.org/10.1016/S0261-2194(02)00066-2
Goldwasser, Y., Plakhine, D., Kleifeld, Y., Zamski, E. and Rubin, B. 2000. The differential susceptibility of vetch (Vicia spp.) to Orobanche aegyptiaca: anatomical studies. Annals of Botany, 85: 257–262.
Gonzalez-Verdejo, C. I., Barandiaran, X., Moreno, M. T., Cubero, J. I. and Di Pietro A. 2006. A peroxidase gene expressed during early developmental stages of the parasitic plant Orobanche ramosa. Journal of Experiment Botany, 57: 185–192.
Hammond-Kosack, K.E. and Jones, J.D.G. 1996. Resistance gene dependent plant defense responses. The Plant Cell, 8: 1773–1791.
Hosseini Faradonbeh, N., Izadi Darbandi, E., Karimmojeni, H. and Nezami, A. 2020. Physiological and growth responses of cucumber (Cucumis sativus L.) genotypes to Egyptian broomrape (Phelipanche aegyptiaca (Pers.) Pomel) parasitism. Acta Physiologiae Plantarum, 42(140) https://doi.org/10.1007/s11738-020-03127-8
Hsieh, T.H., Lee, J.T., Charng, Y.Y. and Chan, M.T. 2002. How to define resistance to water deficit stress? Plant Physiology, 130: 618-626.
Herzog, V. and Fahimi, H. 1973. Determination of activity of peroxidase. Annals of Biochemistry 55: 554-562.
Joel, D.M., Lytton, J.G. and Musselman, J. 2013. Parasitic Orobanchaceae, Parasitic Mechanisms and Control Strategies. Springer. p:325.
Kofalvi, S.A. and Nassuth, A. 1995. Influence of wheat streak mosaic virus infection on phenylpropanoid metabolism and the accumulation of phenolics and lignin in wheat. hysiological and Molecular Plant Pathology, 47(6): 365-377.
Kohlen, W., Charnikhova, T., Lammers, M., Pollina, T., Toth, P., Haider, I., Pozo, M.J., de Maagd, R.A., Ruyter-Spira, C., Bouwmeester, H. J. and Lopez-Raez J. A. 2012. The tomato Carotenoid Cleavage Dioxygenase8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytologist journal, 196: 535–547.
Labrousse, P., Arnaud, M.C., Seryes, H., Berville, A., and Thalouarn, P. 2001. Several mechanisms are involved in resistance of Helianthus to Orobanche cumana Wallr. Annals of Botany, 88: 859–868.
Labrousse, P., Arnaud, M. C., Griveau, Y., Fer, A., and Thalouarn, P. 2004. Analysis of resistance criteria of sunflower recombined in bred lines against Orobanche cumana Wallr. Crop Protection, 23: 407–413
Lendzemo, V. and Kuyper, T. 2001. Effects of arbuscular mycorrhizal fungi on damage by Striga hermonthica on two contrasting cultivars of sorghum, Sorghum bicolor. Agriculture, Ecosystem and Environment journal, 87: 29– 35.
Lendzemo, V., Kuyper, T., Matusova, R., Bouwmeester, H. J., and Van Ast, A. 2007. Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachement and emergence of Striga hermonthica. Plant Signaling and Behavior journal, 2: 58–62.
López-Ráeza, J.A., Charnikhovab, T., Fernándeza, I., Bouwmeester, H., and Pozoa, M.J. 2011. Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. Journal of Plant Physiology, 168: 294–297.
Mabrouk, Y., Simier, P., Delavault, P., Delgrange, S., Sifi, B., Zourgui, L. and Belhad, O. 2007. Molecular and biochemical mechanisms of defense induced in pea by Rhizobium leguminosarum against Orobanche crenata. Weed Research, 47:452–460.
Mor, A., Mayer, A.M., and Levine, A. 2008. Possible peroxidase functions in the interaction between the parasitic plant, Orobanche aegyptiaca, and its host, Arabidopsis thaliana. Weed Biology Management, 8: 1–10.
Munzenberger, B., Otter, T., Wustrich, D. and Polle, A. 1997. Peroxidase and laccase activities in mycorrhizal and non-mycorrhizal fine roots of Norway spruce (Picea abies) and larch (Larix decidua). Canadian Journal of Botany, 75:932–938.
Nakano, Y. and Asada, K. 1981. Hydrogen peroxide is scavenged by ascorbate specific peroxides in spinach chloroplasts. Plant Cell Physiology, 22: 867-880.
Ortas, I., Kaya, Z. and Çakmak, I. 2001. Influence of Vamycorrhiza inoculation on growth of maize and green pepper plants in phosphorus and zinc deficient soils. In: Plant nutrition- Food security and sustainability of agroecosystems (Horst W.J. et al., eds). Kluwer Acad Publ, Dordrecht. pp. 632-633.
Ortas, I. 2003. Effect of selected mycorrhizal inoculation on phosphorus sustainability in sterile and no-sterile soilsin the Harran Plain in south Anatolia. Journal of Plant Nutrition, 26(1):1-17.
Ortas, I. 2010. Effect of mycorrhiza application on plant growth and nutrient uptake in cucumber production under field conditions.Spanish Journal of Agricalture Research, 8(S1): S116-S122.
Pérez-de-Luque A, Jorrín J., Cubero J.I. and Rubiales D. 2005a. Resistance and avoidance against Orobanche crenata in pea (Pisum spp.) operate at different developmental stages of the parasite. Weed Research, 45: 379–387.
Pérez-de-Luque, A., Lozano, M.D., Madrid E. and Rubiales D. 2005b. Histochemistry of the resistance to Orobanche crenata in Medicago truncatula and Pisum sativum. In: Ellis N, ed. Grain legumes annual meeting. Norwich, UK: John Innes Centre, 9.
Pérez-de-Luque, A., Gonzalez-Verdejo, C. I., Lozano, M. D., Dita, M. A., Cubero, J. I., González-Melendi, P., Risueno, M. C. and Rubiales, D. 2006. Protein cross-linking, peroxidase and b-1,3-endoglucanase involved in resistance of pea against Orobanche crenata. Journal of Experimental Botany, 57: 1461–1469
Samejima, H. and Sugimoto, Y. 2018. Recent research progress in combatting root parasitic weeds. Biotechnology and Biotechnology Equipment, 32(2): 221-240
Serghini, K., Perez-De-Luque, A., Castejon-Munoz, M., Garcıa-Torres, L. and Jorrın, J.V. 2001. Sunflower (Helianthus annuus L.) response to broomrape (Orobanche cernua Loefl.) parasitism: induced synthesis and excretion of 7-hydroxylated simple coumarins. Journal of Experimental Botany, 52: 2227–2234.
Shahid, M., Pourrut, B., Dumat, C., Nadeem, M., Aslam, M. and Pinelli, E. 2014. Heavy-metal induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Reviews of Environmental Contamination and Toxicology, 232: 1-44.
Sharma, I. 2013. Arsenic induced oxidative stress and antioxidant defense system of Pisum sativum and Pennisetum typhoides: A comparative study. Research Journal of Biotechnology, 8: 48-56.
Steinkellner, S., Lendzemo, V., Langer, I., Schweiger, P., Khaosaad, T., Toussaint, J. P. andVierheilig, H. 2007. Flavonoids and Strigolactones in Root Exudates as Signals in Symbiotic and Pathogenic Plant-Fungus Interactions. Molecules, 12: 1290-1306.
Sun Z., Has J. and Walter, M.H. 2008. Cloning and characterization of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions. Planta journal, 228: 789–801
Tarvainen, O., Markkola, A.M., Ahonen-Jonnarth, U., Jumpponen, A. and Strommer, R. 2004. Changes in ectomycorrhizal colonization and root peroxidase activity in Pinus sylvestris nursery seedlings planted in forest humus. Scandinavian Journal of Forest Research, 19:400–408
Torres, A.M., Avila, C.M., Gutierrez, N., Palomino, C., Moreno, M.T. and Cubero, J.I. 2010. Marker-assisted selection in faba bean (Vicia faba L.). Field Crops Research, 115:243–252.
Umehara, M., A. Hanada, S. Yoshida, K. Akiyama, T. Arite, N. Takeda-Kamiya, H. Magome, Y. and Kamiya, K. Shirasu. 2008. Inhibition of Shoot Branching by New Terpenoid Plant Hormones. Nature, 455 (7210): 195-200.
Velikova, V., Yordanov, I. and Edreva, A. 2000. Oxidative Stress and Some Antioxidant Systems in Acid RainTreated Bean Plants: Protective Role of Exogenous Polyamines. Plant Science, 151, 59-66.
Verma, S. and Dubay, R.S. 2003. Lead toxicity induces lipid peroxidation and alters the activities of ntioxidant enzymes in growing rice plants. Plant Science, 164:645-655.
Vieira Dos Santos, C., Delavault, P., Letousey, P. and Thalouarn, P. 2003. Identification by suppression subtractive hybridization and expression analysis of Arabidopsis thaliana putative defence genes during Orobanche ramosa infestation. Physiological and Molecular Plant Pathology, 62: 297–303.
Youssef, M.M. and Azooz, M.M. 2013. Biochemical studies on the effects of zinc and lead on oxidative stress, antioxidant enzymes and lipid peroxidation in Okra (Hibiscus esculentus cv. Hassawi). Science International, 1: 12-16.
Zhou, W. J. and Leul, M. 1998. Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regulation, 26: 41–47.
ZhongQun, H., HaoRu, T., HuanXiu, L., ChaoXing, H., ZhiBin, Z. and HuaiSong, W. 2010. Arbuscular mycorrhizal alleviated ion toxicity, oxidative damage and enhanced osmotic adjustment in tomato subjected to NaCl stress. Am. Eurasian Journal of Agricalture and Environmental Science, 7: 676–683.