Abstract
Purpose
Drought is becoming one of the most important environmental stresses and is causing the metabolic imbalance in plants as a result of reactive oxygen species (ROS) accumulation, and a substantial reduction in agriculture productivity. It has been reported for several decades that when plants are inoculated with arbuscular mycorrhizal fungi (AMF), the extent of ROS accumulation due to drought stress is reduced and AMF-inoculated plants have greater antioxidant defense mechanisms. Nevertheless, a comprehensive description of correlating drought stress and antioxidant enzymatic roles in mitigation remains unraveled.
Methods
In the present study, we used meta-analysis in evaluating the AMF inoculation and the prospective antioxidant enzyme responses in alleviating drought stress.
Results
Overall analysis showed that AMF inoculation significantly increased the drought stress alleviation by 17% more than the non-mycorrhizal controls. In addition, antioxidant enzymes analysis showed that SOD enzyme activity increased significantly by 32%, followed by CAT (23%), POD (28%), and APX (27%) across all studies compared to non-inoculated controls whereas the accumulation of H2O2 reduced significantly by 20%. Moreover, the beneficial effects of AMF differed depending on the identity of the host plant, AMF species, and level of drought stress.
Conclusion
Thus, our meta-analysis study suggests that AMF plays a pivotal role in the elimination of H2O2 through the upregulation of antioxidant enzymes but it depends upon the identity of AMF and plant species under drought stress conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
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
Abdel Latef AA (2011) Influence of arbuscular mycorrhizal fungi and copper on growth, accumulation of osmolyte, mineral nutrition and antioxidant enzyme activity of pepper (Capsicum annuum L.). Mycorrhiza 21:495–503. https://doi.org/10.1007/s00572-010-0360-0
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175. https://doi.org/10.3109/07388550903524243
Al-Arjani AF, Hashem A, Abd Allah EF (2020) Arbuscular mycorrhizal fungi modulate dynamics tolerance expression to mitigate drought stress in Ephedra foliata Boiss. Saudi J Biol Sci 27(1):380–394
Amiri R, Nikbakht A, Etemadi N (2015) Alleviation of drought stress on rose geranium Pelargonium graveolen L Herit. In terms of antioxidant activity and secondary metabolites by mycorrhizal inoculation. Sci Hort 197:373–380. https://doi.org/10.1016/j.scienta.2015.09.062
Augé RM (2001) Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42. https://doi.org/10.1007/s005720100097
Augé RM, Saxton AM, Toler HD (2014) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24. https://doi.org/10.1007/s00572-014-0585-4
Bahadur A, Batool A, Nasir F, Jiang S, Mingsen Q, Zhang Q, Pan J, Liu Y, Feng H (2019) Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. Int J Mol Sci 20(17):4199
Begum N, Ahanger MA, Su Y, Lei Y, Mustafa NSA, Ahmad P, Zhang L (2019) Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications. Plants 8:579
Begum N, Ahanger MA, Zhang L (2020) AMF inoculation and phosphorus supplementation alleviates drought induced growth and photosynthetic decline in Nicotiana tabacum by up-regulating antioxidant metabolism and osmolyte accumulation. Environ Exp Bot 176:104088
Bonfante P (2018) The future has roots in the past: the ideas and scientists that shaped mycorrhizal research. New Phytol 220:982–995
Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13(9):492–498. https://doi.org/10.1016/j.tplants.2008.07.001
Chandrasekaran M, Sonia B, Hu S, Oh SH, Sa T (2014) A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza 24:611–625. https://doi.org/10.1007/s00572-014-0582-7
Chen W, Meng P, Feng H, Wang C (2020) Effects of arbuscular mycorrhizal Fungi on growth and physiological performance of Catalpa bungei C.a.Mey. Under drought stress. Forests. 11(10):1117
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90(5):856–867
Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3(3):156–165. https://doi.org/10.4161/psb.3.3.5536
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053
Dumanović J, Nepovimova E, Natić M, Kuča K, Jaćević V (2021) The significance of reactive oxygen species and antioxidant defense system in plants: a concise overview. Front Plant Sci 11:552969. https://doi.org/10.3389/fpls.2020.552969
Gill SS, Tuteja N (2012) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gong M, You X, Zhang Q (2015) Effects of Glomus intraradices on the growth and reactive oxygen metabolism of foxtail millet under drought. Ann Microbiol 65:595–602
Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants. 9(8):681. https://doi.org/10.3390/antiox9080681
He F, Sheng M, Tang M (2017) Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Front Plant Sci 8:183. https://doi.org/10.3389/fpls.2017.00183
He JD, Zou YN, Wu QS, Kuča K (2020) Mycorrhizas enhance drought tolerance of trifoliate orange by enhancing activities and gene expression of antioxidant enzymes. Sci Hortic 262:108745. https://doi.org/10.1016/j.scienta.2019.108745
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156. https://doi.org/10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2
Huang Z, Zou Z, He C, He Z, Zhang Z, Li J (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil 339(1):391–399
Huang YM, Zou YN, Wu QS (2017) Alleviation of drought stress by mycorrhizas is related to increased root H2O2 efflux in trifoliate orange. Sci Rep 7:423–435
Jadrane I et al (2021) Inoculation with selected indigenous mycorrhizal complex improves Ceratonia siliqua’s growth and response to drought stress. Saudi J Biol Sci 28:825–832
Laxa M, Liebthal M, Telman W, Chibani K, Dietz KJ (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants (Basel, Switzerland) 8(4):94. https://doi.org/10.3390/antiox8040094
Li J, Meng B, Chai H, Yang X, Song W, Li S et al (2019) Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Front Plant Sci 10:499. https://doi.org/10.3389/fpls.2019.00499
Liu C, Ravnskov S, Liu F, Rubæk GH, Andersen MN (2018) Arbuscular mycorrhizal fungi alleviate abiotic stresses in potato plants caused by low phosphorus and deficit irrigation/partial root-zone drying. J Agric Sci 156:46–58. https://doi.org/10.1017/S0021859618000023
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
Mittler R (2002) Oxidative stress, antioxidants, and stress tolerance. Trends Plant Sci 7:405–410
Mo Y, Wang Y, Yang R, Zheng J, Liu C, Li H, Ma J, Zhang Y, Wei C, Zhang X (2016) Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Front Plant Sci 7:1–15
Rosenberg NJ, Adams DC, Gurevitch J (2000) Meta-win: statistical software for Meta-analysis version 2.0. Sinauer, Sunderland
Ruiz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869. https://doi.org/10.1016/j.jplph.2010.01.018
Schneider JR, Caverzan A, Chavarria G (2018) Water deficit stress, ROS involvement, and plant performance. Arch Agron Soil Sci 65:1160–1181. https://doi.org/10.1080/03650340.2018.1556789
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidant defence mechanism in plants under stressful conditions. J Bot 2012:217037. https://doi.org/10.1155/2012/217037
Sun Y, Wang C, Chen H, Ruan H (2020) Response of plants to water stress: a Meta-analysis. Front Plant Sci 11:978. https://doi.org/10.3389/fpls.2020.00978
Van der Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423
Wu QS, Zou YN, Xia RX, Wang MY (2007) Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot Stud 48(2):147–154
Yang Q, Zhao Z, Bai Z, Hou H, Yuan Y, Guo A, Li Y (2019) Effects of mycorrhizae and water conditions on perennial ryegrass growth in rare earth tailings. RSC Adv 9(19):10881–10888
Zhang Y, Yao Q, Li J et al (2015) Contributions of an arbuscular mycorrhizal fungus to growth and physiology of loquat (Eriobotrya japonica) plants subjected to drought stress. Mycol Progress 14:84
Zou YN, Huang YM, Wu QS, He XH (2015) Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2 effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza. 25(2):143–152. https://doi.org/10.1007/s00572-014-0598-z
Author information
Authors and Affiliations
Contributions
MC-Conceptulation; Formal analysis; Writing and Supervision; MC and MP-Revision and Editing.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Responsible Editor: Janusz J. Zwiazek.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chandrasekaran, M., Paramasivan, M. Arbuscular mycorrhizal fungi and antioxidant enzymes in ameliorating drought stress: a meta-analysis. Plant Soil 480, 295–303 (2022). https://doi.org/10.1007/s11104-022-05582-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05582-3