Abstract
The use of arbuscular mycorrhizal (AM) fungi is considered as an effective approach to enhance plants’ growth; nevertheless, its efficacy may vary with the type of inoculum and its application method. The present study, for the first time, investigates the effects of different mycorrhizal species applied through different methods on morpho-physiological growth, root system architecture, nutrient uptake, and root exudates of maize. Four AM fungi species viz., Claroideoglomus etunicatum (C.E), Rhizophagus intraradices (R.I), Funneliformis mosseae (F.M), and Diversispora versiformis (D.V) were applied to maize through seed coating, soil application, or seed coating+ soil application. A control without AM fungi was maintained for comparison. All the thirteen treatments were arranged in completely randomized design with three replications. Application of C.E, R.I, F.M, and D.V through different methods triggered the growth performance of maize by improving morpho-physiological characteristics and root morphology, modulating AM fungi colonization, enhancing the nutrient (N, P, K) uptake, and reducing the root exudates (oxalic, malonic, fumaric, malic, citric, and T-aconitic) compared with control. Among the different mycorrhizal species, F.M applied particularly through seed coating+ soil application was more effective in regulating maize growth as compared with C.E, R.I, or D.V species owing to better root system, higher root colonization, and greater nutrient uptake in this treatment. Interestingly, seed coating of F.M recorded statistically similar or higher shoot and root growth attributes compared with soil application particularly at 30 days after sowing. In crux, F.M applied through seed coating + soil application performed better than that of other mycorrhizal species. The obtained results also suggest that seed coating can be a cheap, viable, and efficient delivery system of AM fungi particularly for large scale application, as AM fungi seed coating had faster and greater effect on maize growth compared with soil application during early growth stages.
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References
Anderson D, Henderson L (1988) Comparing sealed chamber digestion with other digestion methods used for plant tissue analysis. Agron J 80:549–552. https://doi.org/10.2134/agronj1988.00021962008000030031x
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068
Bowles TM, Barrios-Masias FH, Carlisle EA, Cavagnaro TR, Jackson LE (2016) Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci Total Environ 566:1223–1234. https://doi.org/10.1016/j.scitotenv.2016.05.178
Chapman HD, Pratt PF (1962) Methods of analysis for soils, plants and waters. Soil Sci 93:68
Chen M, Yang G, Sheng Y, Li P, Qiu H, Zhou X, Huang L, Chao Z (2017) Glomus mosseae inoculation improves the root system architecture, photosynthetic efficiency and flavonoids accumulation of liquorice under nutrient stress. Front Plant Sci 8:931. https://doi.org/10.3389/fpls.2017.00931
Choi J, Lee T, Cho J, Servante EK, Pucker B, Summers W, Bowden S, Rahimi M, An K, An G, Bouwmeester HJ, Wallington EJ, Oldroyd G, Paszkowski U (2020) The negative regulator SMAX1 controls mycorrhizal symbiosis and strigolactone biosynthesis in rice. Nat Commun 11:1–13. https://doi.org/10.1038/s41467-020-16021-1
Coninx L, Martinova V, Rineau F (2017) Mycorrhiza-assisted phytoremediation. In: Advances in botanical research, vol 83. Elsevier, pp 127–188
Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617. https://doi.org/10.1146/annurev-cellbio-101512-122413
Howden SM, Soussana J-F, Tubiello FN, Chhetri N, Dunlop M, Meinke H (2007) Adapting agriculture to climate change. Proc Natl Acad Sci U S A 104:19691–19696. https://doi.org/10.1073/pnas.0701890104
Huang D, Ma M, Wang Q, Zhang M, Jing G, Li C, Ma F (2020) Arbuscular mycorrhizal fungi enhanced drought resistance in apple by regulating genes in the MAPK pathway. Plant Physiol Biochem 149:245–255. https://doi.org/10.1016/j.plaphy.2020.02.020
Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, Wang E (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Sci 356:1172–1175. https://doi.org/10.1126/science.aam9970
Lenoir I, Fontaine J, Sahraoui AL-H (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochem 123:4–15. https://doi.org/10.1016/j.phytochem.2016.01.002
Lipper L et al. (2014) Climate-smart agriculture for food security Nat Clim Chang 4:1068-1072
Ma Y et al (2014) Ectomycorrhizas with P axillus involutus enhance cadmium uptake and tolerance in P opulus× canescens. Plant Cell Environ 37:627–642. https://doi.org/10.1111/pce.12183
Ma Y, Látr A, Rocha I, Freitas H, Vosátka M, Oliveira RS (2019b) Delivery of inoculum of Rhizophagus irregularis via seed coating in combination with Pseudomonas libanensis for cowpea production. Agron 9:33. https://doi.org/10.3390/agronomy9010033
Ma Y, Vosátka M, Freitas H (2019a) Beneficial microbes alleviate climatic stresses in plants. Front Plant Sci 10:595. https://doi.org/10.3389/fpls.2019.00595
McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Oliveira RS, Rocha I, Ma Y, Vosátka M, Freitas H (2016) Seed coating with arbuscular mycorrhizal fungi as an ecotechnologicalapproach for sustainable agricultural production of common wheat (Triticum aestivum L.). J Toxicol Environ Health Part A 79:329–337. https://doi.org/10.1080/15287394.2016.1153448
Phillips JM, Hayman D (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
Pimprikar P, Gutjahr C (2018) Transcriptional regulation of arbuscular mycorrhiza development. Plant Cell Physiol 59:678–695. https://doi.org/10.1093/pcp/pcy075
Qiang-Sheng W, Guo-Huai L, Ying-Ning Z (2011) Improvement of root system architecture in peach (Prunus persica) seedlings by arbuscular mycorrhizal fungi, related to allocation of glucose/sucrose to root. Not Bot Horti Agrobot Cluj Napoca 39:232–236. https://doi.org/10.15835/nbha3926232
Quiroga G, Erice G, Aroca R, Zamarreño ÁM, García-Mina JM, Ruiz-Lozano JM (2018) Arbuscular mycorrhizal symbiosis and salicylic acid regulate aquaporins and root hydraulic properties in maize plants subjected to drought. Agric Water Manag 202:271–284. https://doi.org/10.1016/j.agwat.2017.12.012
Ren A-T, Zhu Y, Chen Y-L, Ren H-X, Li J-Y, Abbott LK, Xiong Y-C (2019) Arbuscular mycorrhizal fungus alters root-sourced signal (abscisic acid) for better drought acclimation in Zea mays L. seedlings. Environ Exp Bot 167:103824. https://doi.org/10.1016/j.envexpbot.2019.103824
Rillig MC, Aguilar-Trigueros CA, Camenzind T, Cavagnaro TR, Degrune F, Hohmann P, Lammel DR, Mansour I, Roy J, Heijden MGA, Yang G (2019) Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol 222:1171–1175. https://doi.org/10.1111/nph.15602
Ryan M, Tibbett M, EDMONDS-TIBBETT T, Suriyagoda L, Lambers H, Cawthray G, Pang J (2012) Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant Cell Environ 35:2170–2180. https://doi.org/10.1111/j.1365-3040.2012.02547.x
Ryan MH, Graham JH (2018) Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol 220:1092–1107. https://doi.org/10.1111/nph.15308
Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125. https://doi.org/10.1007/s11104-004-2725-7
Sivasankar S, Oaks A (1995) Regulation of nitrate reductase during early seedling growth (a role for asparagine and glutamine). Plant Physiol 107:1225–1231. https://doi.org/10.1104/pp.107.4.1225
Srivastava P, Saxena B, Giri B (2017) Arbuscular mycorrhizal fungi: green approach/technology for sustainable agriculture and environment. In: Mycorrhiza-nutrient uptake. Biocontrol, Ecorestoration. Springer, pp 355–386
Szmigielska AM, Van Rees KCJ, Cieslinski G, Huang PM (1996) Low molecular weight dicarboxylic acids in rhizosphere soil of durum wheat. J Agric Food Chem 44:1036–1040. https://doi.org/10.1021/jf950272z
Wu Q-S (2017) Arbuscular mycorrhizas and stress tolerance of plants. Springer
Zhang H et al (2018) Arbuscular mycorrhizal fungi (Glomus mosseae) improves growth, photosynthesis and protects photosystem II in leaves of Lolium perenne L. in cadmium contaminated soil. Front Plant Sci 9:1156. https://doi.org/10.3389/fpls.2018.01156
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
Zhao R, Guo W, Bi N, Guo J, Wang L, Zhao J, Zhang J (2015) Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Appl Soil Ecol 88:41–49. https://doi.org/10.1016/j.apsoil.2014.11.016
Acknowledgements
We are thankful to Dr. Zhang Lin (Beijing Key Laboratory of Biodiversity and Organic Farming, China Agricultural University, Beijing), Prof. Wang Yaosheng, and Dr. Li Tao (Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of Agricultural Sciences, Beijing, China) for their guidance and support during experimentation.
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Financial support for this paper was provided by the National Natural Science Foundation of China (41977072) and Science and Technology Innovation Project of Chinese Academy of Agricultural Sciences.
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Hussain, H.A., Qingwen, Z., Hussain, S. et al. Effects of Arbuscular Mycorrhizal Fungi on Maize Growth, Root Colonization, and Root Exudates Varied with Inoculum and Application Method. J Soil Sci Plant Nutr 21, 1577–1590 (2021). https://doi.org/10.1007/s42729-021-00463-7
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DOI: https://doi.org/10.1007/s42729-021-00463-7