Abstract
The present work aimed to investigate the effect of potentially beneficial soil microorganisms in enhancing the tolerance of tomato plants against Verticillium wilt. The autochthonous mycorrhizal fungi "Rhizolive consortium" and plant growth-promoting rhizobacteria (PGPR) boost the growth and development of plants by providing well-adopted strategies and mechanisms to ensure good-quality production and protection to resist different pathogens including Verticillium dahliae. The application of these bio-agents alone and/or in combination with the pathogen was studied to evaluate their impact on tomato crops. In this study, eight treatments were applied: (i) Control, (ii) Rhizolive consortium (M), (iii) ER10 strain (B), (iv) combination of M and B (MB), (v) V. dahliae (V), (vi) Rhizolive consortium + V. dahliae (MV), (vii) ER10 strain + V. dahliae (BV), and (viii) Rhizolive consortium + ER10 strain + V. dahliae (MBV). Co-inoculation of Rhizolive consortium and ER10 strain significantly improved mycorrhizal frequency and intensity, growth and mineral nutrition of tomato plants. Furthermore, stomatal conductance and chlorophyll fluorescence were improved compared to the control. Moreover, the combination of these biostimulants reduced the disease severity and incidence by 26 and 28%, respectively, and the leaf damage index by 69% compared to plants inoculated with V. dahliae. In addition, the Rhizolive consortium alone or combined with ER10 strain resulted in improved antioxidant activities and stress markers. The synergistic interaction between Rhizolive consortium and ER10 strain promoted tomato yield and fruit quality compared to the control. The results highlight the importance of considering these beneficial soil microorganisms to promote plant resistance to Verticillium wilt disease.
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References
Aalipour H, Nikbakht A, Etemadi N, Rejali F, Soleimani M (2020) Biochemical response and interactions between arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria during establishment and stimulating growth of Arizona cypress (Cupressus arizonica G.) under drought stress. Sci Hortic 261:108923. https://doi.org/10.1016/j.scienta.2019.108923
Abouraïcha E, Alaoui-talibi Z, El Boutachfaiti R, El Petit E, Courtois B, Courtois J, El Modafar C (2015) Induction of natural defense and protection against Penicillium expansum and Botrytis cinerea in apple fruit in response to bioelicitors isolated from green algae. Sci Hortic 181:121–128. https://doi.org/10.1016/j.scienta.2014.11.002
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Aini N, Dwi-Yamika WS, Pahlevi RW (2019) The effect of nutrient concentration and inoculation of PGPR and AMF on the yield and fruit quality of hydroponic cherry tomatoes (Lycopersicon esculentum Mill. Var. cerasiforme). J Appl Hortic 21:116–122. https://doi.org/10.37855/jah.2019.v21i02.20
Ait Rahou Y, Ait-El-Mokhtar M, Anli M, Boutasknit A, Ben-Laouane R, Douira A, Benkirane R, El Modafar C, Meddich A (2020) Use of mycorrhizal fungi and compost for improving the growth and yield of tomato and its resistance to Verticillium dahliae. Arch Phytopathol Plant Prot 54:665–690. https://doi.org/10.1080/03235408.2020.1854938
Akhter A, Hage-Ahmed K, Soja G, Steinkellner S (2016) Potential of Fusarium wiltinducing chlamydospores, in vitro behavior in root exudates and physiology of tomato in biochar and compost amended soil. Plant Soil 406:425–440. https://doi.org/10.1007/s11104-016-2948-4
Alikhani HA, Saleh-Rastin N, Antoun H (2006) Phosphate solubilization activity of rhizobia native to Iranian soils. Plant Soil 287:35–41. https://doi.org/10.1007/s11104-006-9059-6
Armada E, Probanza A, Roldán A, Azcón R (2016) Native plant growth promoting bacteria Bacillus thuringiensis and mixed or individual mycorrhizal species improved drought tolerance and oxidative metabolism in Lavandula dentata plants. J Plant Physiol 192:1–12. https://doi.org/10.1016/j.jplph.2015.11.007
Amkraz N, Boudyach EH, Boubaker H, Bouizgarne B, Aoumar AAB (2010) Screening for fluorescent pseudomonades, isolated from the rhizosphere of tomato, for antagonistic activity toward Clavibacter michiganensis subsp. michiganensis. World J Microbio Biotechnol 26:1059–1065. https://doi.org/10.1007/s11274-009-0270-5
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant physiology 24:1–15
Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10. https://doi.org/10.1111/j.1462-2920.2005.00942.x
Avdiushko SA, Ye XS, Kuc J (1993) Detection of several enzymatic activities in leaf prints of cucumber plants. Physiol Mol Plant Pathol 42:441–454. https://doi.org/10.1006/pmpp.1993.1033
Babu AN, Jogaiah S, Ito SI, Nagaraj AK, Tran LSP (2015) Improvement of growth, fruit weight and early blight disease protection of tomato plants by rhizosphere bacteria is correlated with their beneficial traits and induced biosynthesis of antioxidant peroxidase and polyphenol oxidase. Plant Sci 231:62–73. https://doi.org/10.1016/j.plantsci.2014.11.006
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759
Baslam M, Qaddoury A, Goicoechea N (2014) Role of native and exotic mycorrhizal symbiosis to develop morphological, physiological and biochemical responses coping with water drought of date palm, Phoenix dactylifera. Trees 28:161–172. https://doi.org/10.1007/s00468-013-0939-0
Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051
Ben-Laouane R, Baslam M, Ait-El-Mokhtar M, Anli M, Boutasknit A, Ait-Rahou Y, ToubaliS MT, Oufdou K, Wahbi S, Meddich A (2020) Potential of native arbuscular mycorrhizal fungi, rhizobia, and/or green compost as alfalfa (Medicago sativa) enhancers under salinity. Microorganisms 8:1695. https://doi.org/10.3390/microorganisms8111695
Beyer WF, Fridovich, (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. https://doi.org/10.1016/0003-2697(87)90489-1
Bhardwaj D, Ansari M, Sahoo R, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fact 13:1–10. https://doi.org/10.1186/1475-2859-13-66
Boutaj H, Meddich A, Wahbi S, Moukhli A, El Alaoui-Talibi Z, Douira A, Filali-Maltouf A, El Modafar C (2019) Effect of Arbuscular Mycorrhizal Fungi on Verticillium wilt development of olive trees caused by Verticillium dahliae. Res J Biotechnol 14:79–88
Boutaj H, Meddich A, Chakhchar A, Wahbi S, El Alaoui-Talibi Z, Douira A, Filali Maltouf A, El Modafar C (2020) Arbuscular mycorrhizal fungi improve mineral nutrition and tolerance of olive tree to Verticillium wilt. Arch Phytopathol Plant Prot 53:673–689. https://doi.org/10.1080/03235408.2020.1792603
Boutaj H, Meddich A, Chakhchar A, Wahbi S, Alaoui-Talibi Z, DouiraA F-M, El Modafar C (2021) Induction of early oxidative events in mycorrhizal olive tree in response to Verticillium wilt. Arch Phytopathol Plant Prot 54:1323–1345
Cabanás CGL, Ruano-Rosa D, Legarda G, Pizarro-Tobías P, Valverde-Corredor A, Triviño JC, Roca A, Mercado-Blanco J (2018) Bacillales members from the olive rhizosphere are effective biological control agents against the defoliating pathotype of Verticillium dahliae. Agriculture 8:90. https://doi.org/10.3390/agriculture8070090
Cameron DD, Neal AL, Van Wees SA, Ton J (2013) Mycorrhiza-induced resistance: More than the sum of its parts? Trends Plant Sci 18:539–545. https://doi.org/10.1016/j.tplants.2013.06.004
Campbell CL, Madden LV (1990) Introduction to plant disease epidemiology. NewYork: Wiley, p. 532
Cappuccino JG, Sherman N (1992) Biochemical activities of microorganisms. Microbiology, a laboratory manual. 1st ed. Menlo park, California: The Benjamin/Cummings Publishing Co. p. 105–300
Chafi A, Benabbes R, Bouakka M, Hakkou A, Kouddane N, Berrichi A (2015) Pomological study of dates of some date palm varieties cultivated in Figuig oasis. J Mater Environ Sc 6:1266–1275
Chahdi AO, Chliyeh M, Mouria B, Dahmani J, Ouazzani A (2014) Invitro and in vivo effect of salinity on the antagonist potential of Trichodermaharzianum and sensitivity of tomato to Verticillium wilt. Int J Recent Sci Res 5:780–791
Chandrasekaran M, Chun SC, Oh JW, Paramasivan M, Saini RK, Sahayarayan JJ (2019) Bacillus subtilis CBR05 for tomato (Solanum lycopersicum) fruits in South Korea as a novel plant probiotic bacterium (PPB): Implications from total phenolics, flavonoids, and carotenoids content for fruit quality. Agronomy 9:838. https://doi.org/10.3390/agronomy9120838
Cheng F, Li G, Peng Y, Wang A, Zhu J (2020) Mixed bacterial fermentation can control the growth and development of Verticillium dahliae. Biotechnol Biotechnol Equip 34:58–69. https://doi.org/10.1080/13102818.2020.1713023
Chliyeh M, Chahdi AO, Selmaoui K, Touhami OA, Filali Maltouf A, El Modafar C, Moukhli A, Oukabli A, Benkirane R, Douira A (2014) Efect of Trichoderma harzianum and arbuscular mycorrhizal fungi against Verticillium wilt of tomato. Int J Recent Sci Res 5:449–459
Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 171:1009–1023. https://doi.org/10.1104/pp.16.00307
Dell’Amico J, Torrecillas A, Rodríguez P, Morte A, Sánchez-Blanco MJ (2002) Responses of tomato plants associated with the arbuscular mycorrhizal fungus Glomus clarum during drought and recovery. J Agric Sci 138:387–393. https://doi.org/10.1017/S0021859602002101
Diagne N, Ngom M, Djighaly PI, Fall D, Hocher V, Svistoonoff S (2020) Roles of arbuscular mycorrhizal fungi on plant growth and performance: Importance in biotic and abiotic stressed regulation. Diversity 12:370. https://doi.org/10.3390/d12100370
Dixit R, Agrawal L, Gupta S, Kumar M, Yadav S, Chauhan PS et al (2016) Southern blight disease of tomato control by 1-aminocyclopropane1-carboxylate (ACC) deaminase producing Paenibacillus lentimorbus B30488. Plant Signal Behav 11:e1113363. https://doi.org/10.1080/15592324.2015.1113363
Douira A, Benkirane R, Touhami Ouazzani A, Okeke B, Lahlou H (1993) Verticillium Wilt of Pepper (Capsicum annuum) in Morocco. J Phytophathol 143:467–470
Dvořák P, Krasylenko Y, Zeiner A, Šamaj J, Takáč T (2021) Signaling toward reactive oxygen species-scavenging enzymes in plants. Front Plant Sci 11:618835. https://doi.org/10.3389/fpls.2020.618835
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
El Kinany S, Achbani E, Faggroud M, Ouahmane L, El Hilali R, Haggoud A et al (2019) Effect of organic fertilizer and commercial arbuscular mycorrhizal fungi on the growth of micropropagated date palm cv. Feggouss J Saudi Soc Agric Sci 18:411–417. https://doi.org/10.1016/j.jssas.2018.01.004
El Said SH, Hegazi AA, Allatif AMA (2012) Resistance of some olive cultivars to Verticillium wilt. J Appl Sci Res 8:2758–2765
Eke P, Chatue Chatue G, Wakam LN, Kouipou RMT, Fokou PVT, Boyom FF (2016) Mycorrhiza consortia suppress the fusarium root rot (Fusarium solani f. sp. Phaseoli) in common bean (Phaseolus vulgaris L.). Biol Control 103:240–250. https://doi.org/10.1016/j.biocontrol.2016.10.001
FAOSTAT (2019). Available at: http://www.fao.org/faostat/en/#home. Accessed 15 April 2021
FAOSTAT (2020) FAOSTAT [WWW Document]. Available online at: http://www.fao.org/faostat/en/#data. Accessed 08 Jun 2020
Fradin EF, Thomma BP (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7(2):71–86. https://doi.org/10.1111/j.1364-3703.2006.00323.x
Fondio L, Djidji HA, N’Gbesso FPM, Kone D (2013) Evaluation de neuf variétés de tomate (Solanum Lycopersicum L.) par rapport au flétrissement bactérien et à la productivité dans le Sud de la Cote d’Ivoire. Int J Bio Chem Sci 7:1078. https://doi.org/10.4314/ijbcs.v7i3.15
Gharbi Y, Barkallah M, Bouazizi E, Hibar K, Gdoura R, Triki MA (2017) Lignification, phenols accumulation, induction of PR proteins and antioxidant-related enzymes are key factors in the resistance of Olea europaea to Verticillium wilt of olive. Acta Physiol Plant 39:43. https://doi.org/10.1007/s11738-016-2343-z
Geetha K, Rajithasri AB, Bhadraiah B (2014) Isolation of Plant growth promoting rhizobacteria from rhizosphere soils of green gram, biochemical characterization and screening for antifungal activity against pathogenic fungi. Int J Pharm Sci Invent 3:47–54
Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106–114. https://doi.org/10.1016/j.agwat.2012.11.007
Glick BR, Liu C, Ghosh S, Dumbroff EB (1997) Early development of canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239. https://doi.org/10.1016/S0038-0717(97)00026-6
Goicoechea N, Garmendia I, Sánchez-Díaz M, Aguirreolea J (2010) Arbuscular mycorrhizal fungi (AMF) as bioprotector agents against wilt induced by Verticillium spp. in pepper. Span J Agric Res 8:S25–S42
Gong S, Wang C, Jiang P, Hu L, Lei H, Chen Q (2018) Designing highly efficient dual-metal single-atom electrocatalysts for the oxygen reduction reaction inspired by biological enzyme systems. J Mater Chem A 6:13254–13262. https://doi.org/10.1039/c8ta04564j
Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500. https://doi.org/10.1080/23311932.2015.1127500
Hashem A, Abd-Allah EF, Alqarawi AA, Al-Huqail AA, Wirth S, Egamberdieva D (2016) The interaction between Arbuscular Mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1–15. https://doi.org/10.3389/fmicb.2016.01089
Hernández D, Ros M, Carmona F, Saez-Tovar JA, Pascual JA (2021) Composting spent mushroom substrate from Agaricus bisporus and Pleurotus ostreatus production as a growing media component for baby leaf lettuce cultivation under Pythium irregulare biotic stress. Horticulturae 7:13. https://doi.org/10.3390/horticulturae7020013
Hilares RT, Dos Santos JG, Shiguematsu NB, Ahmed MA, da Silva SS, Santos JC (2019) Low-pressure homogenization of tomato juice using hydrodynamic cavitation technology: effects on physical properties and stability of bioactive compounds. Ultrason Sonochem 54:192–197. https://doi.org/10.1016/j.ultsonch.2019.01.039
Hori K, Wada A, Shibuta T (1997) Changes in phenoloxidase activities of the galls on leaves of Ulmus davidana Formed by Tetraneura Fusiformis (Homoptera: Eriosomatidae). Appl Entomol Zoo l32:365–371. Doi: https://doi.org/10.1303/aez.32.365
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:1–10. https://doi.org/10.3389/fpls.2019.00800
Jimenez-Ruiz J, Leyva-Pérez MO, Schilirò E, Barroso JB, Bombarely A, Mueller L, Mercado-Blanco J, Luque F (2017) Transcriptomic analysis of Olea europaea L. roots during the Verticillium dahliae early infection process. Plant Genome 10:1–15. https://doi.org/10.3835/plantgenome2016.07.0060
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Kanayama Y (2017) Sugar metabolism and fruit development in the tomato. Horti J OKD-IR. https://doi.org/10.2503/hortj.OKD-IR01
Karagiannidis N, Bletsos F, Stavropoulos N (2002) Effect of Verticillium wilt (Verticillium dahliae Kleb.) and mycorrhiza (Glomus mosseae) on root colonization, growth and nutrient uptake in tomato and eggplant seedlings. Sci Hortic 94:145–156
Kaur R, Kaur S, Kaur N (2021) Phosphate solubilizing bacteria: a neglected bioresource for ameliorating biotic stress in plants. In: Plant-microbe dynamics: recent advances for sustainable agriculture (pp. 39–50).
Keller S, Schneider K, Suessmuth RD (2006) Structure elucidation of auxofuran, a metabolite involved in stimulating grwoth of fly agaric, produced by the mycorrhiza helper bacterial streptomyces AcH 505. J Antibiot 59:801–803. https://doi.org/10.1038/ja.2006.106
Khan N, Bano A (2018) Effects of exogenously applied salicylic acid and putrescine alone and in combination with rhizobacteria on the phytoremediation of heavy metals and chickpea growth in sandy soil. Int J Phytoremediation 20:405–414. https://doi.org/10.1080/15226514.2017.1381940
Kim YC, Anderson AJ (2018) Rhizosphere pseudomonads as probiotics improving plant health. Mole Plant Pathol 19:2349–2359. https://doi.org/10.1111/mpp.12693
Kohler J, Hernández JA, Caravaca F, Roldán A (2008) Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 35:141–151
Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47:39–62. https://doi.org/10.1146/annurev-phyto-080508-081748
Kumar AS, Bais HP (2012) Wired to the roots: impact of root-beneficial microbe interactions on aboveground plant physiology and protection. Plant Signal Behav 7:1598–1604. https://doi.org/10.4161/psb.22356
Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65:1474–1484. https://doi.org/10.1111/j.1365-2958.2007.05879.x
Li Y, Wang H, Zhang Y, Martin C (2018) Can the world’s favorite fruit, tomato, provide an effective biosynthetic chassis for high-value metabolites? Plant Cell Rep 37:1443–1450. https://doi.org/10.1007/s00299-018-2283-8
Liu H, Jiang W, Bi Y, Luo Y (2005) Postharvest BTH treatment induces resistance of peach (Prunus persica L. cv. Jiubao) fruit to infection by Penicillium expansum and enhances activity of fruit defense mechanisms. Postharvest Biol Technol 35:263–269. https://doi.org/10.1016/j.postharvbio.2004.08.006
Majeed A, Abbasi MK, Hameed S, Imran A, Rahim N (2015) Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Front Microbiol 6:198. https://doi.org/10.3389/fmicb.2015.00198
Martí R, Roselló S, Cebolla-Cornejo J (2016) Tomato as a source of carotenoids and polyphenols targeted to cancer prevention. Cancers 8:58. https://doi.org/10.3390/cancers8060058
Meddich A, Ait El Mokhtar M, Bourzik W, Mitsui T, Baslam M, Hafidi M (2018) Optimizing growth and tolerance of date palm (Phoenix dactylifera L.) to drought, salinity, and vascular fusarium-induced wilt (Fusarium oxysporum) by application of arbuscular mycorrhizal fungi (AMF). Springer, Cham. In: Root biology pp 239–258
Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:1–25. https://doi.org/10.3389/fpls.2017.00172
Meena M, Swapnil P, Nandan Y, Andleeb T, Meena M, Swapnil P, Divyanshu K, Kumar S, Tripathi YN, Zehra A, Marwal A, Upadhyay RS (2020a) PGPR-mediated induction of systemic resistance and physiochemical alterations in plants against the pathogens: current perspectives. J Basic Microbiol 60:828–861. https://doi.org/10.1002/jobm.202000370
Mekonnen H, Kibret M (2021) The roles of plant growth promoting rhizobacteria in sustainable vegetable production in Ethiopia. Chem Biol Technol Agric 8:1–11. https://doi.org/10.1186/s40538-021-00213-y
Mena-Violante HG, Olalde-Portugal V (2007) Alteration of tomato fruit quality by root inoculation with plant growth-promoting rhizobacteria (PGPR): Bacillus subtilis BEB-13bs. Sci Horti 113:103–106. https://doi.org/10.1016/j.scienta.2007.01.031
Meena M, Swapnil P, Divyanshu K, Kumar S, Tripathi YN, Zehra A, Upadhyay RS (2020b) PGPR-mediated induction of systemic resistance and physiochemical alterations in plants against the pathogens: Current perspectives. J Basic Microbiol 60:828–861. https://doi.org/10.1002/jobm.202000370
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant, Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
Mohamed I, Eid KE, Abbas MH, Salem AA, Ahmed N, Ali M, Fang C (2019) Use of plant growth promoting Rhizobacteria (PGPR) and mycorrhizae to improve the growth and nutrient utilization of common bean in a soil infected with white rot fungi. Ecotoxicol Environ Saf 171:539–548. https://doi.org/10.1016/j.ecoenv.2018.12.100
Nadal M, Sawers R, Naseem S, Bassin B, Kulicke C, Sharman A, Paszkowski U (2017) An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nat Plants 3:1–7. https://doi.org/10.1038/nplants.2017.73
Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448. https://doi.org/10.1016/j.biotechadv.2013.12.005
Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015) Systemic jasmonic acid modulationin mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. J Plant Biol 17:625–631. https://doi.org/10.1111/plb.12277Nasir
Nasir F, Tian L, Chang C, Li X, Gao Y, Tran LSP, Tian C (2018) Current understanding of pattern-triggered immunity and hormone-mediated defense in rice (Oryza sativa) in response to Magnaporthe oryzae infection. Semin Cell Dev Biol 83:95–105. https://doi.org/10.1016/j.semcdb.2017.10.020
Nguvo KJ, Gao X (2019) Weapons hidden underneath: bio-control agents and their potentials to activate plant induced systemic resistance in controlling crop Fusarium diseases. J Plant Dis Prot 126:177–190. https://doi.org/10.1007/s41348-019-00222-y
Oldroyd GE (2013) Speak, friend, enter: signaling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263. https://doi.org/10.1038/nrmicro2990
Ordookhani K, Khavazi K, Moezzi A, Rejali F (2010) Influence of PGPR and AMF on antioxidant activity, lycopene and potassium contents in tomato. Afr J Agric Res 5:1108–1116. https://doi.org/10.5897/AJAR.9000428
Ouledali S, Ennajeh M, Ferrandino A, Khemira H, Schubert A, Secchi F (2019) Influence of arbuscular mycorrhizal fungi inoculation on the control of stomata functioning by abscisic acid (ABA) in drought-stressed olive plants. S Afr J Bot 121:152–158. https://doi.org/10.1016/j.sajb.2018.10.024
Papadaki AM, Bletsos FA, Eleftherohorinos IG, Menexes G, Lagopodi AL (2017) Effectiveness of seven commercial rootstocks against verticillium wilt and their effects on growth, yield, and fruit quality of tomato. Crop Prot 102:25–31. https://doi.org/10.1016/j.cropro.2017.08.006
Pastori PL, Cintra-Figueiras RM, Hansen-Oster A, Goncalves-Barbosa M, da Silveira MRS, Paiva LGG (2017) Postharvest quality of tomato fruits sacked with nonwoven fabric (TNT). Rev Colomb Cienc Hortic 11:80–88. https://doi.org/10.17584/rcch.2017v11i1.5839
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Priyadharsini P, Muthukumar T (2016) Interactions between arbuscular mycorrhizal fungi and potassium-solubilizing microorganisms on agricultural productivity. In: Potassium solubilizing microorganisms for sustainable agriculture. Springer, New pp: 111–125, Delhi. https://doi.org/10.1007/978-81-322-2776-2_8
Raklami A, Bechtaoui N, Tahiri A, Anli M, Meddich A, Oufdou K (2019) Use of rhizobacteria and mycorrhizae consortium in the open field as a strategy for improving crop nutrition, productivity and soil fertility. Front Microbiol 10:1–11. https://doi.org/10.3389/fmicb.2019.01106
Remans R, Beebe S, Blair M, Manrique G, Tovar E, Rao I, Croonenborghs A, Torres-Gutierrez R, El-Howeity M, Michiels J (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161. https://doi.org/10.1007/s11104-007-9462-7
Rillig MC, Aguilar-Trigueros CA, Camenzind T, Cavagnaro TR, Degrune F, Hohmann P et al (2019) Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol 222:1171–1175. https://doi.org/10.1111/nph.15602
Sadashiva AT, Christopher MG, Krithika TK (2013) Genetic enhancement of tomato crop for abiotic stress tolerance. In Climate-Resilient Horticulture: Adaptation and Mitigation Strategies, H.C.P. Singh, N.K.S. Rao, and K.S. Shivashankar, eds. New Delhi, India: Springer p:113–124. https://doi.org/10.1007/978-81-322-0974-4_11
Sadler G, Davis J, Dezman D (1990) Rapid extraction of lycopene and β-carotene from reconstituted tomato paste and pink grapefruit homogenates. J Food Sci 55:1460–1461. https://doi.org/10.1111/j.1365-2621.1990.tb03958.x
Sharma PI, Sharma AK (2017) Co-inoculation of tomato with an arbuscular mycorrhizal fungus improves plant immunity and reduces root-knot nematode infection. Rhizosphere 4:25–28. https://doi.org/10.1016/j.rhisph.2017.05.008
Shen Z, Zhong S, Wang Y, Wang B, Mei X, Li R, Ruan Y, Shen Q (2013) Induced soil microbial suppression of banana fusarium wilt disease using compost and biofertilizers to improve yield and quality. Eur J Soil Biol 57:1–8. https://doi.org/10.1016/j.ejsobi.2013.03.006
Schubert R, Werner S, Cirka H, Rödel P, Tandron Moya Y, Mock HP, Hutter I, Kunze G, Hause B (2020) Effects of arbuscular mycorrhization on fruit quality in industrialized tomato production. Int J Mol Sci 21:7029. https://doi.org/10.3390/ijms21197029
Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G et al (2006) Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918. https://doi.org/10.1111/j.1365-3040.2005.01471.x
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56. https://doi.org/10.1016/0003-2697(87)90612-9
Singh A, Jain A, Sarma BK, Upadhyay RS, Singh HB (2013) Rhizosphere microbes facilitate redox homeostasis in Cicer arietinum against biotic stress. Ann Appl Biol 163:33–46. https://doi.org/10.1111/aab.12030
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic press, New York
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Sofy AR, Sofy MR, Hmed AA, El-Dougdoug NK (2019) Potential effect of plant growth-promoting rhizobacteria (PGPR) on enhancing protection against viral diseases. Field crops: sustainable management by PGPR. Springer, Champp, pp 411–445
Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786. https://doi.org/10.1007/978-3-030-30926-8_15
Tahmatsidou V, O’Sullivan J, Cassells AC, Voyiatzis D, Paroussi G (2006) Comparison of AMF and PGPR inoculants for the suppression of Verticillium wilt of strawberry (Fragaria ananassa cv. Selva). Appl Soil Ecol 32:316–324. https://doi.org/10.1016/j.apsoil.2005.07.008
Tang F, Fu YY, Ye JR (2015) The effect of methyl salicylate on the induction of direct and indirect plant defense mechanisms in poplar (Populus euramericana “nanlin 895”). J Plant Interact 10:93–100. https://doi.org/10.1080/17429145.2015.1020024
Teerachaichayut S, Ho HT (2017) Non-destructive prediction of total soluble solids, titratable acidity and maturity index of limes by near infrared hyperspectral imaging. Postharvest Biol Technol 133:20–25. https://doi.org/10.1016/j.postharvbio.2017.07.005
Tejera NA, Campos R, Sanjuan J, Lluch C (2004) Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropici isogenic strains with varying tolerance to salt stress. J Plant Physiol 161:329–338. https://doi.org/10.1078/0176-1617-01050
Tigist M, Workneh TS, Woldetsadik K (2013) Effects of variety on the quality of tomato stored under ambient conditions. J Food Sci Technol 50:477–486. https://doi.org/10.1007/s13197-011-0378-0
Topalović O, Hussain M, Heuer H (2020) Plants and associated soil microbiota cooperatively suppress plant-parasitic nematodes. Front Microbiol 11:313. https://doi.org/10.3389/fmicb.2020.00313
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. Physiol Genet Asp Mycorrhizae. INRA Press, pp 217–221
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 Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Verma PP, Shelake RM, Das S, Sharma P, Kim JY (2019) Plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF): potential biological control agents of diseases and pests. In: Microbial interventions in agriculture and environment. Springer, Singapore. pp. 281–311. https://doi.org/10.1007/978-981-13-8391-5_11
Visen A, Bohra M, Singh PN, Srivastava PC, Kumar S, Sharma AK, Chakraborty B (2017) Two pseudomonad strains facilitate AMF mycorrhization of litchi (Litchi chinensis Sonn.) and improving phosphorus uptake. Rhizosphere 3:196–202. https://doi.org/10.1016/j.rhisph.2017.04.006
Vos C, Tesfahun A, Panis B, De Waele D, Elsen A (2012) Arbuscular mycorrhizal fungi induce systemic resistance in tomato against the sedentary nematode Meloidogyne incognita and the migratory nematode Pratylenchus penetrans. Appl Soil Ecol 61:1–6. https://doi.org/10.1016/j.apsoil.2012.04.007
Wang X, Ding T, Li Y, Guo Y, Li Y, Duan T (2020) Dual inoculation of alfalfa (Medicago sativa L.) with Funnelliformis mosseae and Sinorhizobium medicae can reduce Fusarium wilt. J Appl Microbiol 129:665–679. https://doi.org/10.1111/jam.14645
Wu X, Song X, Qiu Z, He Y (2016) Mapping of TBARS distribution in frozen-thawed pork using NIR hyperspectral imaging. Meat Sci 113:92–96. https://doi.org/10.1111/jam.14645
Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang M (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS ONE 10:e0145726. https://doi.org/10.1371/journal.pone.0145726
Yooyongwech S, Samphumphuang T, Tisarum TC, Cha-um S (2016) Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 198:107–117. https://doi.org/10.1016/j.scienta.2015.11.002
Zhang Q, Gao X, Ren Y, Ding X, Qiu J, Li N, Zeng F, Chu Z (2018) Improvement of Verticillium wilt resistance by applying arbuscular mycorrhizal fungi to a cotton variety with high symbiotic efficiency under field conditions. IJMS 19:241. https://doi.org/10.3390/ijms19010241
Zhang S, Lehmann A, Zheng W, You Z, Rillig MC (2019) Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol 222:543–555. https://doi.org/10.1111/nph.15570
Zhang X, Bai L, Guo N, Cai B (2020) Transcriptomic analyses revealed the effect of Funneliformis mosseae on genes expression in Fusarium oxysporum. PLoS ONE 15:e0234448. https://doi.org/10.1371/journal.pone.0234448
Zou YN, Srivastava AK, Ni QD, Wu QS (2015) Disruption of mycorrhizal extraradical mycelium and changes in leaf water status and soil aggregate stability in root box-grown trifoliate orange. Front Microbiol 6:203. https://doi.org/10.3389/fmicb.2015.00203
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This research was supported by Socially Responsible Projects, Cadi Ayyad University (Marrakech, Morocco) UCAM/RSU 2018.
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Ait Rahou, Y., Boutaj, H., Ait-El-Mokhtar, M. et al. Effect of beneficial indigenous microorganisms on tomato growth performance, productivity, and protection against Verticillium dahliae. J Plant Dis Prot 129, 1163–1180 (2022). https://doi.org/10.1007/s41348-022-00616-5
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DOI: https://doi.org/10.1007/s41348-022-00616-5