Signals and Machinery for Mycorrhizae and Cereal and Oilseed Interactions towards Improved Tolerance to Environmental Stresses
Abstract
:1. Introduction
2. Building Resilience: Harnessing Mycorrhizal Symbiosis for Enhanced (a)biotic Stress Tolerance in Cereal and Oilseed Crops
2.1. Cereal Mycorrhizal Responses to Stressed Environments
2.1.1. Cereal Mycorrhizal Responses to Abiotic Stresses
2.1.2. Cereal Mycorrhizal Responses to Biotic Stresses
2.2. Oilseed Mycorrhizal Responses to Stressed Environments
2.2.1. Oilseed Mycorrhizal Responses to Abiotic Stresses
Stress | Plant | AMF Species | AMF Colonization Effects | Ref. |
---|---|---|---|---|
Drought | ||||
Soybean (Glycine max) | R. irregularis | - Enhanced TSS, proline content, and MAPK transcripts. | [94] | |
Flax (Linum usitatissimum) | F. mosseae, R. intraradices | - Enhanced leaf P content and oil yield. | [100] | |
Sesame (Sesamum indicium) | F. mosseae, R. intraradices | - Improved Chl index, and N, P, K, Zn, Fe, and Cu content. | [98] | |
Soybean (Glycine max) | R. intraradices, R. clarus, R. aggregatum, S. deserticola, F. mosseae, O. etunicatum | - Improved biomass, Chl content, gs, leaf water relations, and N, P, K, S, Mn, and Cu content. | [97] | |
Flax (Linum usitatissimum) | F. mosseae, R. intraradices | - Improved vesicle diameter, yield, and SOD, APX, and POX activity. | [101] | |
Sesame (Sesamum indicum) | F. mosseae, R. intraradices | - Improved TSP, P, Chl, flavonoid contents, and seed/oil yield. | [99] | |
Soybean (Glycine max) | P. occulum, G. gigantea, F. mosseae, C. etunicatum, R. clarus | - Higher growth traits (pod number, seed number, and seed DM) and oilseed proline. | [95] | |
Soybean (Glycine max) | G. clarum, G. mosseae, Gigaspora margarita | - Enhanced yield, and seed CAT and POX activity. - Decreased MDA and proline contents. - Up-regulated CAT and POX expression and down-regulated proline metabolism genes (P5CS, P5CR, PDH, and P5CDH). | [112] | |
Sesame (Sesamum indicum) | R. intraradices, F. mosseae | - Improved grain yield, oil content, and N and P content. | [103] | |
Soybean (Glycine max) | G. mosseae | - Improved glucose exudation, and β-glucosidase and acid phosphomonoesterase. | [113] | |
Soybean (Glycine max) | R. clarus | - Improved plant height, water potential, WUE, Fv/Fm, and N and K content. | [102] | |
Salinity | ||||
Sunflower (Helianthus annuus) | R. irregularis | - Lower Na+ and MDA content. - Improved biomass and nutritional profile (K+, Mg2+, Ca2+, N, P), soil enzyme activities (CAT, dehydrogenase, phosphatase, fluorescein diacetate hydrolysis). | [104] | |
Safflower (Carthamus tinctorius) | R. intraradices, F. moseae | - Improved shoot and root DM, stem and root heights, proline, pigment, P, N, Mg contents, and antioxidant enzyme activity. | [105] | |
Soybean (Glycine max) | F. mosseae, R. intraradices, C. etunicatum | - Improved nitrogenase and IAA synthesis, and lower H2O2 and MDA content. | [108] | |
Iberian dragon’head (Lallemantia iberica) | F. mosseae | - Ameliorated seeds’ oil and mucilage composition. | [106] | |
Groundnut (Arachis hypogaea) | R. irregularis, F. mosseae | - Reduced MDA content. - Improved An, RWC, plant height, osmolyte production, SOD, POX, CAT, APX, protein, and pod yielding. | [107] | |
Heavy Metals | ||||
Sunflower (Helianthus annuus) | G. intraradices | - Enhanced P, Chl, carotenoid, SOD, and PPO. - Reduced MDA, As, Cr, and Ni translocation. | [109] | |
Soybean (Glycine max) | R. intraradices | - Lowered Cd accumulation in roots. - Promoted P and Fe abundance in roots. | [110] | |
Soybean (Glycine max) | F. mosseae | - Boosted growth, yield, and P assimilation. - Decreased Cu, Pb, and Zn translocation. | [111] | |
Soybean (Glycine Max) | R. Intraradices | - Improved growth, P acquisition, and grain yield under Cu, Pb, and Zn soil pollution. - Reduced translocation of the HMs. | [111] |
2.2.2. Oilseed Mycorrhizal Responses to Biotic Stresses
3. Molecular Strategies Contributing to Cereal and Oilseed Tolerance to Environmental Stresses
3.1. Molecular Mechanisms behind Cereal Mycorrhiza Responses
3.1.1. Molecular Mechanisms behind Cereal Mycorrhiza Responses to Abiotic Stresses
3.1.2. Molecular Mechanisms behind Cereal Mycorrhiza Responses to Biotic Stresses
3.2. Molecular Mechanisms behind Oilseed Mycorrhiza Responses to Stressed Environments
3.2.1. Molecular Mechanisms behind Oilseed Mycorrhiza Responses to Abiotic Stresses
3.2.2. Molecular Mechanisms behind Oilseed Mycorrhiza Responses to Biotic Stresses
4. Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Stress | Crops | AMF | AMF Colonization Effects | Ref |
---|---|---|---|---|
Drought | ||||
Maize (Zea mays) | Rhizoglomus intraradices | - Improved growth traits, P, fresh leaf moisture content, WUE, and reduced C/P and N/P. | [30] | |
Maize (Zea mays) | R. intraradices | - Amelioration of maize growth, water status, and Pi concentration. - Down-regulation of aldehyde oxidase expression and induced ABA signal transduction gene expression (D-myo-inositol-3-phosphate synthase and 14-3-3-like protein GF14). | [74] | |
Wheat (Triticum Aestivum) | R. intraradices | - Improved leaf area, RWC, and WUE. - Enhanced N and P content and grain yielding. | [75] | |
Maize (Zea mays) | Rhizophagus irregularis | - Ameliorated PSII efficiency and membrane stability and decreased lipids’ oxidative damage. -TSS overaccumulation and aquaporin gene expression (down-regulated ZmPIP1;1, ZmPIP1;3, ZmPIP1;4, ZmPIP1;6, ZmPIP2;2, ZmPIP2;4, ZmTIP1;1, and ZmTIP2;3 and up-regulated ZmTIP4;1). | [34] | |
Sorghum (Sorghum bicolor) | F. mosseae | - Improved biomass and SLA and extended plant lifetime duration. | [47] | |
Finger Millet (Eleusinecoracana) | R. intraradices | - Decreased EL, MDA, and hydrogen peroxide content. - Improved PRO, TSS, total phenol, and flavonoid content and antioxidant enzyme activities. | [50] | |
Sorghum (Sorghum bicolor) | R. arabicus, R. irregularis | - Ameliorated transpiration efficiency and N and P acquisition. | [44] | |
Wheat (Triticum Aestivum) | Glomus intraradices | - Improved RWC, flag leaf SLA, WUE, and mineral assimilation, particularly P. | [76] | |
Maize (Zea mays) | G. versiforme | - Improved PH, SDM, and chlorophyll content. - Enhanced PRO, glycine betaine, TSS, free AAa, and phenols. - Decreased stress marker levels and improved GSH, CAT, POX, and SOD activities. | [51] | |
Wheat (Triticum aestivum) | F. mosseae | - Enhanced SFW and SDW, N in roots, C/N ratio, and WUE. - Regulated plant secondary, oxidative stress metabolisms, and phytohormones’ crosstalk. | [35] | |
Wheat (Triticum aestivum) | R. irregularis, F. mosseae | - Improved growth traits and N assimilation. - Regulated miR167, miR5384-3p, and miR156e-3p, influencing trafficking functionalities and cellular redox homeostasis. | [77] | |
Maize (Zea mays) | R. irregularis | - Enhanced SFW and Pi acquisition - Moderated gs, transpiration, and WUE. | [45] | |
Wheat (Triticum aestivum) | R. intraradices, F. mosseae, F. geosporum | - Improved plant and soil RWC. - Improved PSI and PSII quantum efficiency and photochemistry. | [43] | |
Barley (Hordeum vulagre) | R. intraradices, F. mossea, C. claroideum, | - Improved plant growth traits. | [78] | |
Rice (Oryza sativa) | F. mosseae, F. geosporus, R. irregularis, G.microaggregatum, C. claroideum | - Maintained rice growth and improved P acquisition. - Ameliorated nutrient, ABA, and IAA balance. - Higher grain yield, Chl fluorescence, and gs. | [42] | |
Wheat (Triticum aestivum) | F. mosseae | - Enhanced plant shoot, root, and spike FW. - De-regulated transcriptional profiling, cell wall, and its membrane components. - Induced carbohydrate and lipid metabolism, cellulose synthase activity, membrane transport systems, N compound metabolic, and chitinase activity genes’ expression. | [37] | |
Sorghum (Sorghum bicolor) | G. mosseae | - Ameliorated Chl a, b, and total Chl content, WUE, RWC, N, soluble proteins, and proline. - Enhanced yield, panicle length, number of panicles per plant, number of grains per panicle, and 1000-grain weight, and reduced EL and water saturation. | [36] | |
Maize (Zea mays) | F. mosseae | - Enhanced Chl content, the net rate of photosynthesis, gs, rate of transpiration, and WUE. | [46] | |
Wheat (Triticum aestivum) | F. mosseae | - Up-regulated water stress response-related genes (TdsHN1 and TdDRF1). | [79] | |
Salinity | ||||
Maize (Zea mays) | G. etunicatum | - Improved dry biomass and nutrient content and decreased Na+ assimilation. | [60] | |
Wheat (Triticum aestivum) | G. intraradices | - Reduced shoot Na+ and enhanced N, P, K+, proline, Chl, protein, SA content, and total grain yielding. | [58] | |
Rice (Oryza sativa) | C. etunicatum | - Improved SDW and root length. - Ameliorated gs and PSII efficiency, P and K+ content, K+/Na+ in shoots and reduced it in the roots. - Up-regulated OsNHX3, OsSOS1, OsHKT2;1, and OsHKT1;5. | [63] | |
Maize (Zea mays) | R. intraradices | - Improved SDW and mineral uptake (P and N) and reduced leaf proline levels. | [52] | |
Maize (Zea mays) | C. lamellosum Gigaspora margarita | - Ameliorated SDW, RDW, and nutrient content. - Reduced proline in the shoots and Na+ in the roots and higher K+/Na+ in roots. - Higher ZmAKT2, ZmSOS1, and ZmSKOR gene expression, sustaining K+ and Na+ homeostasis. | [61] | |
Sorghum (Sorghum bicolor) | Acaulospora mellea | - Increased biomass, minerals, K+/Na+, leaf TSS content, and SOD, POX, CAT activities. | [67] | |
Wheat (Triticum aestivum) | R. irregularis, F. mosseae, F. geosporum, C. claroideum | - Upgraded net photosynthesis rate, gs, reduced intrinsic WUE. - Higher carbon use efficiency and grain yielding. | [53] | |
Maize (Zea mays) | R. irregulare | - Decreased Na+ level in root and its roots-to-shoots translocation. - K+ accumulation and Mg2+ reduction in roots. - Ca2+ fluctuation interacting with salinity. | [62] | |
Rice (Oryza sativa) | R. irregularis | - Reduced H2O2 and enhanced CAT activity and leaf N content. - Enhanced tiller, panicle, grain number, and yield. | [54] | |
Rice (Oryza sativa) | F. mosseae, A. laevis, G. margarita | - Improved total Chl, shoot K+/Na+ ratio, and grain yield. - Decreased shoot Na+/root Na+. | [64] | |
Rice (Oryza sativa) | G. etunicatum, G. geosporum, G. mosseae | - Lower Na+/K+ ratio. - Maintained sucrose in flag leaf tissues and fructose and free proline overaccumulation. - Regulated cyanidin-3-glucoside and peonidin-3-glucosi.de in salt-sensitive rice. | [65] | |
Maize (Zea mays) | F. mosseae | - Improved WUE, Chl, An, CAT, SOD, APX, and GSH activities - Decreased EL, MDA, and H2O2. | [80] | |
Wheat (Triticum aestivum) | F. geosporum, F. mosseae, R. clarus, Scutellospora persica | - Promoted N, P, and K+ acquisition, Chl content, and K+/Na+ ratio. - Reduced Na+, Cl−, PRO, and MDA content. | [59] | |
Maize (Zea mays) | G. mosseae | - Improved PH, leaf number, and plant FW and DW. - Enhanced nutrient content (N, P, and K+), and increased antioxidant enzyme activities. - Improved palmitoleic, oleic, linoleic, and linolenic acid contents. | [56] | |
Sorghum (Sorghum bicolor) | F. mosseae, F. geosporum | - Improved PH, FW, DW, P, K+/Na+, and glomalin in soil. - Enhanced dehydrogenase and alkaline phosphatase activity. | [66] | |
Maize (Zea mays) | R. irregularis | - Improved SDW, RDW, and RWC. | [57] | |
Heavy Metals | ||||
Wheat (Triticum aestivum) | Glomus sp. | - Reduced Zn content in shoots. | [81] | |
Rice (Oryza sativa) | R. intraradices, F. mosseae | - Reduced Cd concentration in shoots and roots. | [31] | |
Maize (Zea mays) | F. mosseae, Diversispora sphurcum | - Enhanced biomass, Chl, SOD, and CAT activities, and T-AOC and reduced H2O2, and MDA levels. - Limited Pb, Zn, and Cd transfer and contents in shoots. | [71] | |
Rice (Oryza sativa) | F. mosseae, R. intraradices | - Reduced Cd concentrations in shoots and roots. - Iduced Nramp5 and HMA3 expression in roots. | [70] | |
Sorghum (Sorghum bicolor) | C. etunicatum | - Enhanced biomass, PSII efficiency, and P, N, and S assimilation, and Mo accumulation. | [72] | |
Maize (Zea mays) | C. etunicatum | - Increased SDW and SFW, and K+, P, Ca2+, Mg2+ in shoots. - Reduced lanthanum concentration in shoot and root. | [69] | |
Wheat (Triticum aestivum) | R. intraradices | - Ameliorated growth and reduced Ni assimilation. | [73] |
AMF | Biotic Stress Agent | Plant | AMF Colonization Effects | Ref. |
---|---|---|---|---|
F. mosseae R. irregularis | Blumeria graminis f. sp. tritici | Wheat (Triticum aestivum) | - Reduced pathogenic fungus’ conidia number. - Overaccumulation of polyphenolic compounds. | [82] |
C. claroideum, F. mosseae, R. irregulare | Oscinella frit | Wheat (Triticum aestivum) | - Ameliorated plant health status and production under pest’s heavy infestation. | [86] |
F. mosseae | B. graminis f. sp. tritici | Wheat (Triticum aestivum) | - Decreased foliar biotrophic pathogen infection. - ISR and phenolic components’ overproduction. | [83] |
F. mosseae | Xanthomonas translucens | Wheat (Triticum aestivum) | - Higher biomass, yield, and protein oxidation levels and decreased lesion area. - Up-regulated CYP enzymes, NTRs genes, and disease resilience genes. | [84] |
R. intraradices | Magnaporthe oryzae | Rice (Oryza sativa) | - Induced IAA-/SA-related genes, key in pathogenesis-related protein synthesis. - Enriched JA, α-linolenic acid-, phenol-, and terpenoid syntheses-related genes. | [91] |
F. mosseae, R. intraradices | M. oryzae | Rice (Oryza sativa) | - Improved Pi content and grain yield. - Higher resilience to the rice blast fungus. | [89] |
R. irregulare | Sitobion avenae | Wheat (Triticum aestivum) | - Better harvest index and lower aphid population size. | [87] |
R. intraradices | Spodoptera frugiperda | Rice (Oryza sativa) | - ISR activation and higher PPO and POX activity. | [92] |
Enthropospora sp., Gigaspora sp., Glomus sp. | Peronosclerospora spp. | Maize (Zea mays) | - Enhanced SDM. - Attenuated downy mildew. - Expanded incubation period. | [90] |
R. intraradices | Fusarium pseudograminearum | Wheat (Triticum aestivum) | - Improved biomass, spikes number, and height. - Enhanced antioxidant enzyme activity and reduced lipid peroxidation levels. - Decreased F. pseudograminearum density (76%) and disease severity (40%). | [88] |
F. mosseae | X. translucens | Wheat (Triticum aestivum) | - Higher N acquisition, photosynthesis, and glucose and amino acid content. - Elicited defense-related proteins, immune response, and JA biosynthesis. | [85] |
R. irregularis | Rhopalosiphum padi | Wheat (Triticum aestivum) | - Boosted root growth and P and N assimilation. | [93] |
AMF | Biotic Stress Agent | Plant | AMF Colonization Effects | Ref. |
---|---|---|---|---|
R. intraradices, G. mosseae, G. etunicatum, G. claroideum, G. microaggregatum, G. geosporum | Sclerotinia sclerotiorum | Sunflower (Helianthus annuus) | - Hinder pathogenic hyphae development. - Localized and systemic resistance to white rot. | [120] |
R. intraradices | Macrophomina phaseolina | Soybean (Glycine max) | - Reduced charcoal rot in soybean. | [119] |
R. irregularis | M. phaseolina | Soybean (Glycine max) | - Up-regulated secondary metabolism genes. - Repressed genes encoding fasciclin-like arabinogalactan-protein, SKU5 similar 5, endo-chitinase, MYB, and POX. | [121] |
R. irregularis | F. virguliforme | Soybean (Glycine max) | - Up-regulated defense-related genes like disease resistance proteins, WRKY, auxins, receptor kinases, proteases, thaumatin-like protein, pleiotropic drug resistance proteins/genes. - Down-regulated cell wall and POX genes. | [115] |
R. intraradices | F. virguliforme | Soybean (Glycine max) | - Improved growth and P, K, Na, and S. - Decreased death syndrome severity. | [116] |
R. intraradices | M. phaseolina | Soybean (Glycine max) | - Ameliorated biomass and greenness index. | [114] |
G. etunicatum | Heterodera glycines | Soybean (Glycine max) | - Improved plant height and root system. - Decreased female nematodes in roots. | [117] |
R. irregularis | Aphis glycines | Soybean (Glycine max) | - Improved biomass, nodulation, and N and C content. | [118] |
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Slimani, A.; Ait-El-Mokhtar, M.; Ben-Laouane, R.; Boutasknit, A.; Anli, M.; Abouraicha, E.F.; Oufdou, K.; Meddich, A.; Baslam, M. Signals and Machinery for Mycorrhizae and Cereal and Oilseed Interactions towards Improved Tolerance to Environmental Stresses. Plants 2024, 13, 826. https://0-doi-org.brum.beds.ac.uk/10.3390/plants13060826
Slimani A, Ait-El-Mokhtar M, Ben-Laouane R, Boutasknit A, Anli M, Abouraicha EF, Oufdou K, Meddich A, Baslam M. Signals and Machinery for Mycorrhizae and Cereal and Oilseed Interactions towards Improved Tolerance to Environmental Stresses. Plants. 2024; 13(6):826. https://0-doi-org.brum.beds.ac.uk/10.3390/plants13060826
Chicago/Turabian StyleSlimani, Aiman, Mohamed Ait-El-Mokhtar, Raja Ben-Laouane, Abderrahim Boutasknit, Mohamed Anli, El Faiza Abouraicha, Khalid Oufdou, Abdelilah Meddich, and Marouane Baslam. 2024. "Signals and Machinery for Mycorrhizae and Cereal and Oilseed Interactions towards Improved Tolerance to Environmental Stresses" Plants 13, no. 6: 826. https://0-doi-org.brum.beds.ac.uk/10.3390/plants13060826