COLONIZATION OF TOMATO ROOTS WITH ARBUSCULAR MYCORRHIZAL FUNGI CHANGES OF ANTIOXIDATIVE ACTIVITY AND IMPROVES TOLERANCE TO Verticillium dahliae

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YOUSSEF AIT RAHOU
HANANE BOUTAJ
ABDERRAHIM BOUTASKNIT
ALLAL DOUIRA
RACHID BENKIRANE
CHERKAOUI EL MODAFAR
ABDELILAH MEDDICH

Abstract

The present study aims to assess the effect of autochthonous mycorrhizal fungi “Rhizolive consortium” on Verticillium wilt of tomato plants (Lycoperscum esculentum Mill.) and induction of antioxidant enzymes in response to Verticillium dahliae inoculation. 15 days old tomato plants were inoculated first with Rhizolive consortium for two months then infected with V. dahliae for three months. Our results showed that mycorrhization frequency of tomato root system was slightly affected in the presence of V. dahliae, while in the presence of Rhizolive consortium, mycorrhizal intensity was reduced by about 48%. The growth and yield of mycorrhizal plants were significantly improved compared to the control plants. Moreover, AMF reduced symptoms development as compared to infected tomatoes only by V. dahliae. The leaf alteration index of tomato plants was reduced in mycorrhiza-infected tomato plants by 58%. Mycorrhizal tomato pants significantly reduced Malonyldialdehyde accumulation in the presence of Verticillium dahliae by 20% and 38% in the leaves and roots tissue, respectively. In contrast, inoculated tomato plants with Rhizolive consortium alone significantly increased (p = .05) catalase, superoxide dismutase, peroxidase, polyphenoloxidase activities in the roots compared to other treatments. Subsequently, antioxidant enzyme activities were induced slightly in response to V. dahliae inoculation. These results showed clearly that AMF protect tomato plants and contributes to the suppression of V. dahliae.

Keywords:
Lycoperscum esculentum, mycorrhizal autochthonous consortium, verticillium wilt, tolerance, bioprotection

Article Details

How to Cite
AIT RAHOU, Y., BOUTAJ, H., BOUTASKNIT, A., DOUIRA, A., BENKIRANE, R., EL MODAFAR, C., & MEDDICH, A. (2021). COLONIZATION OF TOMATO ROOTS WITH ARBUSCULAR MYCORRHIZAL FUNGI CHANGES OF ANTIOXIDATIVE ACTIVITY AND IMPROVES TOLERANCE TO Verticillium dahliae. PLANT CELL BIOTECHNOLOGY AND MOLECULAR BIOLOGY, 22(53-54), 65-81. Retrieved from https://www.ikprress.org/index.php/PCBMB/article/view/7015
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Original Research Article

References

Fondio L, Djidji, HA, N’gbesso, FD, Koné D. Evaluation de neuf variétés de tomate (Solanum Lycopersicum L.) par rapport au flétrissement bactérien et à la productivité. International Journal of Biological and Chemical Sciences. 2013;7(3):1078–1086.

FAOSTAT http://www.fao.org/faostat/en/#data/QCL 2019 (accessed on 09/07/2021)

FAOSTAT. http://www.fao.org/faostat/en/#data/QCL 2019 (accessed on 09/07/2021).

Zare M, Ordookhani KO, Alizadeh O. Effects of PGPR and AMF on growth of two bred cultivars of tomato. Adv. Environment Biol. 2011;5(8):2177–2181

Berni R, Romi M, Cantini C, Hausman JF, Guerriero G, Cai G. Functional molecules in locally-adapted crops: The case study of tomatoes, onions, and sweet cherry fruits from Tuscany in Italy. Frontiers in plant science. 2019;9:1983.

Lin W, Lin M, Zhou H, Wu H, Li Z, Lin W. The effects of chemical and organic fertilizer usage on rhizosphere soil in tea orchards. PloS one. 2019;14:e0217018

Chen D, Yuan L, Liu Y, Ji J, Hou H. Long-term application of manures plus chemical fertilizers sustained high rice yield and improved soil chemical and bacterial properties. European Journal of Agronomy. 2017;90:34-42.

Noreika N, Pärtel M, Öpik M. Effects of mutualistic and pathogenic soil mycobiota on forest ecosystem functioning: herbaceous phytometer growth on natural and sterilised soils. Ecological Indicators, 2021;127:107792.

Porras-Soriano A, Marcilla-Goldaracena I, Soriano-Martin ML, Porras-Piedra A. Development and resistance to Verticillium dahliae of olive plantlets inoculated with mycorrhizal fungi during the nursery period. Journal of Agricultural Science. 2006;144:151–157.

Boutaj H, Meddich A, Wahbi S, Moukhli A, El Alaoui-Talibi Z, Douira A, Filali-Maltouf A, El Modafar C. Effect of Arbuscular Mycorrhizal Fungi on Verticillium wilt development of olive trees caused by Verticillium dahliae. Research Journal of Biotechnology. 2019;14:79–88.

Rowe RC, Powelson ML. Potato early dying: Management challenges in a changing production environment. Plant Disease. 2002;86:1184–1193.

Douira A, Benkirane R, Touhami A, Ouazzani T, Okeke B, Lahlou, H. Verticillium Wilt of Pepper (Capsicum annuum) in Morocco. Journal of Phytophathology. 1993;143:467–470.

Karagiannidis N, Bletsos F, Stavropoulos N. Effect of Verticillium wilt (Verticillium dahliae Kleb.) and mycorrhiza (Glomus mosseae) on root colonization, growth and nutrient uptake in tomato and eggplant seedlings. Scientia Horticulturae. 2002; 94(1-2):145-156.

Bahouq M, Douira A. Effect of endomycorrhizae on wilt disease of strawberry caused by Verticillium dahliae in morocco. Plant Cell Biotechnology and Molecular Biology. 2019;12:339–47.

Gayoso C, Pomar F, Novo-Uzal E, Merino F, de Ilárduya ÓM. The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biology. 2010; 10(1):1-19.

Garbaye J. La symbiose mycorhizienne: une association entre les plantes et les champignons. Editions Quae. 2013;259.

Kapoor R. Induced resistance in mycorrhizal tomato is correlated to concentration of jasmonic acid. Journal of Biological Sciences. 2008;8:49–56.

Mwangi MW, Monda EO, Okoth SA, Jefwa, JM. Inoculation of tomato seedlings with Trichoderma harzianum and arbuscular mycorrhizal fungi and their effect on growth and control of wilt in tomato seedlings. Brazilian Journal of Microbiology. 2011;42:508-513.

Song Y, Chen D, Lu K, Sun Z, Zeng R. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science. 2015;6:786.

García-Sánchez M, Palma JM, Ocampo JA, García-Romera I, Aranda E. Arbuscular mycorrhizal fungi alleviate oxidative stress induced by ADOR and enhance antioxidant responses of tomato plants. Journal of Plant Physiology. 2014;171:421–8.

Moons A. Osgstu3 and osgtu4, encoding tau class glutathione S-transferases, are heavy metal- and hypoxic stress-induced and differentially salt stress-responsive in rice roots 1. Febs Letters. 2003;55(3):427–32

Gerdemann JW, Nicolson TH. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society. 1963;46(2), 235-244.

Walker C, Mize CW, McNabb Jr HS. Populations of endogonaceous fungi at two locations in central Iowa. Canadian Journal of Botany. 1982;60(12):2518-2529.

Pérez Y, Schenck NC. A unique code for each species of VA mycorrhizal fungi. Mycologia. 1990;82(2):256-260.

Morton JB, Benny GL. Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): A new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon. 1990;37, 471-491.

Mukerji KG. Taxonomy of endomycorrhizal fungi. In: Advances in Botany. India: APH Publishing Corporation New Delhi. 1996:211–221.

Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C. An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza. 2013;23(7):515-531.

Kachkouch W, Touati J, Touhami A, Filali-maltouf A, El Modafar C, Moukhli A, Oukabli A, Benkirane R, Douira A. Diversity of arbuscular mycorrhizal fungi in the rhizosphere of Olea europea in three regions of Morocco (Tafilalt, Zagora and Taounate). International Journal of Pure & Applied Bioscience. 2014;2:178–195.

Boutaj H, Chakhchar A, Meddich A, Wahbi S, El Alaoui-Talibi Z, Douira A, Filali-Maltouf A, El Modafar C. Bioprotection of olive tree from Verticillium wilt by autochthonous endomycorrhizal fungi. Journal of Plant Diseases and Protection. 2020b;127(3):349-357.

Plenchette C, Furlan V, Fortin JA. Effects of different endomycorrhizalfungi on five host plants grown on calcine montmorillonite clay. J Am Soc Hort Sci. 1982;107:535–538.

Strullu DG. Micropropagation of chesnut and conditions of mycorrhizal synthesis in vitro. New Phytol. 1986;102:95–101.

Plenchette C, Perrin R, Duvert P. The concept of soil infectivity and a method for its determination as applied to endomycorrhizas. Canadian Journal of Botany. 1989;67(1):112-115.

Wang Y, Deng C, Tian L, Xiong D, Tian C, Klosterman SJ. The transcription factor VdHapX controls iron homeostasis and is crucial for virulence in the vascular pathogen Verticillium dahliae. Msphere. 2018;3(5):e00400-18.

Biessy A, Novinscak A, St-Onge R, Léger G, Zboralski A, Filion M. Inhibition of Three Potato Pathogens by Phenazine-Producing Pseudomonas spp. Is Associated with Multiple Biocontrol-Related Traits. Msphere. 2021;6(3):e00427-21.

Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc. 1970;55: 158–161.

Trouvelot A, Kouch J, Gianinazzi-Pearson V. Mesure du taux de mycorhization VA d’un système radiculaire: Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi S (Ed.), Les Mycorhizes: Physiologie et Génétique, 1er Séminaire Europeen sur les Mycorhizes, Dijon. INRA, Paris. 1986;217–221.

El Said SH, Hegazi AA, Allatif AMA. Resistance of some olive cultivars to verticillium wilt. ISSN 1819-544X. Journal of Applied Sciences Research. 2012; 8(5):2758–2765.

Boutaj H, Chakhchar A, Meddich A, Wahbi S, El Alaoui-Talibi Z, Douira A, Filali-Maltouf A, El Modafar C. Mycorrhizal autochthonous consortium induced defense-related mechanisms of olive trees against Verticillium dahliae. Journal of Plant Diseases and Protection. 2020c;128(1):225-237.

Douira A, Lahlou H. Variabilité de la spécificité parasitaire chez Verticillium albo-atrum Reinke et Berthold, forme à microsclérotes. Cryptogamie Mycologie. 1989;10:19–32.

Campbell CL, Madden V. Introduction to plant disease epidemiology. In New York. USA Wiley-Interscience. 1990;532.

Jing R, Li H, Hu X, Shang W, Shen R, Guo C, Subbarao KV. Verticillium wilt caused by Verticillium dahliae and V. nonalfalfae in potato in northern China. Plant disease. 2018;102(10):1958-1964.

Wu X, Song X, Qiu Z, He Y. Mapping of TBARS distribution in frozen thawed pork using NIR hyperspectral imaging. Meat Sci. 2016;113:92–96.

Benhiba L, Fouad MO, Essahibi A, Ghoulam C, Qaddoury A. Arbuscular mycorrhizal symbiosis enhanced growth and antioxidant metabolism in date palm subjected to long-term drought. Trees. 2015;29:1725–1733.

Beyer WF, Fridovich I. Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 1987;161:559–566.

Aebi H. Catalase in Vitro. Methods Enzymology. Academic Press. 1984;105:121–126.

Tejera NA, Campos R, Sanjuan J, Liuch C. Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropid isogenic strains with varying tolerance to salt stress. J Plant Physiol. 2004;161(3): 329-338.

Hori K, Wada A, Shibuta T. Changes in Phenoloxidase activities of the galls on leaves of Ulmusdavidana formed by Tetraneura fusiformis (Homoptera: Eriosomatidae). Appl Entomol Zool. 1997; 32(2):365–371.

Jaiti F, Meddich, A, El Hadrami I. Effectiveness of arbuscular mycorrhizal fungi in the protection of date palm (Phoenix dactylifera L.) against bayoud disease. Physiological and Molecular Plant Pathology. 2007;71(4-6):166-173.

Meddich A, Oihabi A, Jaiti F, Bourzik W, Hafidi M. Role of arbuscular mycorrhizal fungi on vascular wilt and drought tolerance in date palm (Phoenix dactylifera L.). Canadian Journal of Botany. 2015;93(6):369–377.

Caron M, Fortin A, Richard C. Effect of inoculation sequence on the interaction between Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes. Can J Plant Pathol. 1986; 8(1):12–16.

Zhang G, Raza W, Wang X, Ran W, Shen Q. Systemic modification of cotton root exudates induced by arbuscular mycorrhizalfungi and Bacillus vallismortis HJ-5 and their effects on Verticillium wilt disease. Appl Soil Ecol. 2012;61: 85–91.

Yadeta K, Thomma B. The xylem as battleground for plant hosts and vascular wilt pathogens. Frontiers in plant science. 2013;4:97.

Eke P, Chatue GC, Nana wakam L, Kouipou RMT, Tsouh Fokou PV, Fekam Boyom F. Mycorrhiza consortia suppress the fusarium root rot (Fusarium solani f. sp. Phaseoli) in common bean (Phaseolus vulgaris L.). Biol Control. 2016;103: 240–250.

Bartschi H, Gianinazzi-Pearson V, Vegh I. Vesicular arbuscular mycorrhiza formation and root disease (Phytophthora cinnamoni) development in Chamaecyparis lawsoniana. Phytopathol. 1981;102:213–218

Akköprü A, Demir S. Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria. Journal of Phytopathology. 2005;153:544–550.

El-Khallal SM. Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors. Australian Journal of Basic and Applied Sciences. 2007;1(4): 717–732.

Singh M. Interactions among arbuscular mycorrhizal fungi, Trichoderma harzianum, Aspergillus niger and biocontrol of wilt of tomato Arch. Phytopathol Plant Protection. 2015;48(3): 205–211.

Tayal P, Kapoor R, Bhatnagar AK. Functional synergism among Glomus fasciculatum, Trichoderma viride and Pseudomonas fluorescens on fusarium wilt in tomato. Journal of Plant Pathology. 2011;93(3):745–750.

Kobra N, Jalil K, Youbert G. Effects of three Glomus species as biocontrol agents against Verticillium-induced wilt in cotton. Journal of Plant Protection Research. 2009;49(2):185–189.

Zhu X, Song F, Xu H.. Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza. 2010;20:325–32.

Augé RM, Toler HD, Saxton AM. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza. 2015;25(1):13–24.

Evelin H, Devi TS, Gupta S, Kapoor R. Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: Current understanding and new challenges. Front Plant Sci. 2019;10:1–21.

Tahat MM, Al Momany AM. Bio-control characterization of two endo-mycorrhizal fungi against Verticillium wilt of cucumber. Fresenius Environ Bull., 2019;28:9627–9635.

Li F, Guo Y, Christensen MJ, Gao P, Li Y, Duan T. An arbuscular mycorrhizal fungus and Epichloëfestucae var. lolii reduce Bipolarissorokiniana disease incidence and improve perennialryegrass growth. Mycorrhiza. 2018;28(2):159–169.

Azcón-Aguilar C, Barea JM. Applying mycorrhiza biotechnology to horticulture: Significance and potentials. Scientia Horticulturae. 1997;68:1–24.

Smith S, Read Df. Mycorrhizal Symbiosis,3rd edition, SBN:9780123705266, eBook ISBN: 9780080559346, Academic Press. 2008; 769.

Tarraf, W, Ruta C, Tagarelli A, De Cillis F, De Mastro G. Influence of arbuscular mycorrhizae on plant growth, essential oil production and phosphorus uptake of Salvia officinalis L. Industrial Crops and Products. 2017;102:144-153.

Boutaj H, Meddich A, Wahbi S, Moukhli A, El Alaoui-Talibi Z, Douira A, Filali-Maltouf A, El Modafar C. Improvement of growth and development of olive tree by mycorrhizal autochthonous inoculum. Research Journal of Biotechnology. 2020a; 15:76–84.

Nafady NA, Hassan EA, Abd-Alla MH, Bagy MMK. Effectiveness of eco-friendly arbuscular mycorrhizal fungi biofertilizer and bacterial feather hydrolysate in promoting growth of Vicia faba in sandy soil. Biocatalysis and Agricultural Biotechnology 2018;16:140–147.

Cervantes-Gámez, RG, Bueno-Ibarra MA, Cruz-Mendívil A, Calderón-Vázquez CL, Ramírez-Douriet CM, Maldonado-Mendoza, IE, Villalobos-López MÁ, Valdez-Ortíz Á, López-Meyer M. Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA-seq analysis. Plant Molecular Biology reporter. 2015;34(1):89–102.

Kachroo A, Kachroo P. Salicylic acid-, jasmonic acid-and ethylenemediated regulation of plant defense signaling In Genetic Engineering. Springer Boston, MA. 2007;55–83.

Ismail Y, McCormick S, Hijri M. The arbuscular mycorrhizal fungus, Glomus irregulare, controls the mycotoxin production of Fusarium sambucinum in the pathogenesis of potato. FEMS Microbiol Lett. 2013;348(1):46–5.

Ismail Y, Hijri M. Arbuscular mycorrhisation with Glomus irregulare induces expression of potato PR homologues genes in response to infection by Fusarium sambucinum. Funct. Plant Biol. 2012;39(3):236–245.

Ismail Y, McCormick S, Hijri M. A fungal symbiont of plant-roots modulates mycotoxin gene expression in the pathogen Fusarium sambucinum. PLoSONE 2011;6 (3):e17990

Garmendia I, Goicoechea N, Aguirreolea J. Antioxidant Metabolism in Asymptomatic Leaves of Verticillium-infected Pepper Associated with an Arbuscular Mycorrhizal Fungus. Journal of Phytopathology. 2004; 152(11-12):593–599

Maldonado-Bonilla LD, Betancourt-Jiménez M, Lozoya-Gloria E. Local and systemic gene expression of sesquiterpene phytoalexin biosynthetic enzymes in plant leaves. European Journal of Plant Pathology. 2008;121(4):439–49.

Boutaj H, MeddichA, Chakhchar A, Wahbi S, Alaoui-Talibi ZE, Douira A, Filali-Maltouf A, El Modafar C. Induction of early oxidative events in mycorrhizal olive tree in response to Verticillium wilt. Archives of Phytopathology and Plant Protection. 2021;1-23.

Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B,. Ruiz-Lozano JM. Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza. 2016;26(2):141–52.

Goicoechea N, Garmendia I, Sánchez- Díaz M, Aguirreolea J. Arbuscular mycorrhizal fungi (AMF) as bioprotector agents against wilt induced by Verticillium spp. in pepper: A review. Spanish Journal of Agricultural Research. 2010;1(S1):25– 42

Yang Y, Han C, Liu Q, Lin B, Wang JW. Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiol Plant. 2008;30(4):433–440.

Guo J, Yan Yang Y, Wang G, Yang L, Sun X. Ecophysiological responses of Abies fabri seedlings to drought stress and nitrogen supply. Physiol Plant. 2010;139(4):335–347.

Murshed R, Lopez-Lauri F, Sallanon H. Effect of water stress on antioxidant systems and oxidative parameters in fruits of tomato (Solanum lycopersicon L, cv. Micro-tom). Physiology and Molecular Biology of Plants. 2013;19(3):363–78

Wang Y, Ke Y, Pan T. Effects of different mycorrhizal fungi on physiological metabolism of tobacco seedlings. Journal of Applied Ecology. 2002;13(1):87–90.

Zarik L, Meddich A, Hijri M, Hafidi M, Ouhammou A, Ouahmane L,. Duponnois R, Boumezzough A. The role of arbuscular mycorrhizal fungi on drought tolerance of Cupressus atlantica G. to water deficit. Compte rendu Journal des Biologies. 2016;339(5-6):185–196.

Gaspar TH, Thorpe T, Penel C, Greppin H.. Peroxidases 1970-1980. A survey of their Biochemical and Physiological Roles in Higher plants. Université de Genève. 1982;324.

Grabber JH, Ralph J, Hatfield RD. Model Studies of Ferulate-Coniferyl Alcohol Cross-Product Formation in Primary Maize Walls: Implications for Lignification in Grasses. Journal of Agricultural and Food Chemistry. 2002;50(21):6008–6016.

Price NJ, Pinheiro C, Soares CM, Ashford DA, Ricardo CP, Jackson PA. A biochemical and molecular characterization of LEP1, an extensin peroxidase from Lupin. J Biol Chem. 2003;278(42):41389–41399.

Cosgrove DJ. Wall structure and wall loosening. A look backwards and forwards. Plant Physiol. 2001;125(1):131–134.

Keren-Keiserman A, Tanami Z, Shoseyov O, Ginzberg I. Peroxidase activity associated with suberization processes of the muskmelon (Cucumis melo) rind. Physiol Plant. 2004;121(1):141–148.

Boerjan W, Ralph J, Baucher M. Lignin biosynthesis. Annu. Rev. Plant Biol. 2003;54(1):519–546.

Avdiushko SA, XS Ye, Kuc J. Detection of several enzymatic activities in leaf prints cucumber plant. Physiol. Mol. Plant Pathol. 1993;42(6):441–54.

El Modafar C. Mechanisms of date palm resistance to Bayoud disease: Current state of knowledge and research prospects. Physiological and Molecular Plant Pathology. 2010;74(5-6):287–294.