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RESEARCH ARTICLE (Open Access)

Morphological and molecular identification of indigenous arbuscular mycorrhizal fungi in the rhizosphere of chickpea (Cicer arietinum) and their role in nutrient uptake

Kamran Akbar A , Tabassum Yaseen A # , Banzeer Ahsan Abbasi B , Javed Iqbal A # , Badr Alharthi C , Sajid Fiaz https://orcid.org/0000-0001-9097-4359 D * , Salma Noureen A , Shumaila Ijaz E , Ejaz Aziz F and Rashid Iqbal G H
+ Author Affiliations
- Author Affiliations

A Department of Botany, Bacha Khan University, Charsadda24420, Khyber Pakhtunkhwa, Pakistan. Email: durrani_kamran0911@yahoo.com, tabassumyaseen@bkuc.edu.pk, javed89qau@gmail.com, salmanoreen738@gmail.com

B Department of Botany, Rawalpindi Women University, 6th Road, Satellite Town, Rawalpindi 46300, Pakistan. Email: benazirahsanabbasi786@gmail.com

C Department of Biology, University College of Al Khurmah, Taif University, PO. Box 11099, Taif 21944, Saudi Arabia. Email: b.harthi@tu.edu.sa

D Institute of Molecular Biology and Biotechnology (IMBB), The University of Lahore, Lahore 54590, Pakistan.

E Department of Burn and Plastic Surgery, Shenzhen Institute of Translational Medicine, The First Affiliated Hospital of Shenzhen University, School of Biomedical Engineering, Shenzhen University Medical School, Shenzhen University, Shenzhen 518035, China. Email: shumailaijaz1996@yahoo.com

F Department of botany GDC Khanpur Haripur, 22 650, Charsadda, Khyber Pakhthunkhw, Pakistan. Email: ejaz.aziz.qau@gmail.com

G Department of Agronomy, Faculty of Agriculture and Environment, The Islamia University of Bahawalpur Pakistan, Bahawalpur 63100, Pakistan. Email: rashid.iqbal@iub.edu.pk

H Department of Life Sciences, Western Caspian University, Baku, Azerbaijan.

* Correspondence to: sajidfiaz50@yahoo.com

# These authors contributed equally to this paper

Handling Editor: Muhammad Zaheer

Functional Plant Biology 52, FP24326 https://doi.org/10.1071/FP24326
Submitted: 30 December 2024  Accepted: 30 June 2025  Published: 21 July 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC)

Abstract

This study aimed to evaluate the effect of arbuscular mycorrhizal fungi (AMF) on the growth, nutrient uptake, and productivity of chickpea (Cicer arietinum). We investigated the diversity of indigenous AMF in their natural habitat and their effect on the plant and elemental characteristics of chickpea by analysing soil physicochemical properties, root colonisation, AMF spore diversity, and elemental composition of chickpea rhizosphere in two locations (Bhakkar and Khushab, Pakistan). Nitrogen levels of 5.47 g/kg and 4.51 g/kg were found in the rhizosphere soils of Bhakkar and Khushab, respectively. Root colonisation was higher (48.5%) in Khushab (Bhakkar, 35.5%), influencing phosphorus absorption in both regions. Molecular analysis identified 21 AMF taxa, with Glomus and Acaulospora being the most dominant genera. Variations in spore sizes were found, with Glomus measuring 10–191 μm, Acaulospora 125–152 μm, Sclerocystis 110–174 μm, and Gigaspora 65–184 μm. Plant analysis revealed that plant materials from Bhakkar had 1.72% ash, 1.16% fat, 3.78% fibre, and 13.05% protein; samples from Khushab had 1.90% ash, 1.25% fat, 3.24% fibre, and 11.5% protein. Elemental concentrations of chickpea plants from Bhakkar were N = 2.68%, P = 32.98 mg/kg, and K = 33.32 mg/kg, whereas those from Khushab were N = 1.94%, P = 1.17 mg/kg, and K = 43.06 mg/kg. Molecular analysis revealed AMF species with a range of 250–1100 bp. Root colonisation was inversely related to soil phosphorus levels but had a positive effect on plant moisture, fats, and carbohydrates. Morphological and molecular identification showed a relatively high AMF taxa in the rhizosphere of chickpea in both regions. Despite their benefits, the potential of AMF as biofertilisers has not been fully utilised due to prevailing agronomic practices.

Keywords: biofertilizer potential, elemental analysis, microbial activity, mycorrhization, root colonization, soil physicochemical properties, spore morphology.

Reference

Abdelaal K, Alaskar A, Hafez Y (2024) Effect of arbuscular mycorrhizal fungi on physiological, bio-chemical and yield characters of wheat plants (Triticum aestivum L.) under drought stress conditions. BMC Plant Biology 24(1), 1119.
| Crossref | Google Scholar | PubMed |

Alguacil MM, Hernández JA, Caravaca F, Portillo B, Roldán A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiologia Plantarum 118(4), 562-570.
| Crossref | Google Scholar |

Alimi A, Adeleke R, Moteetee A (2021) Soil environmental factors shape the rhizosphere arbuscular mycorrhizal fungal communities in South African indigenous legumes (Fabaceae). Biodiversitas Journal of Biological Diversity 22(5), 2466-2476.
| Crossref | Google Scholar |

Alrajhi K, Bibi S, Abu-Dieyeh M (2024) Diversity, distribution, and applications of arbuscular mycorrhizal fungi in the Arabian Peninsula. Saudi Journal of Biological Sciences 31(2), 103911.
| Crossref | Google Scholar |

Amir H, Crossay T (2024) Functional and practical importance of AMF-mixed inoculants for plant development. In ‘Arbuscular mycorrhizal fungi in sustainable agriculture: inoculum production and application’. (Eds M Parihar, A Rakshit, A Adholeya, Y Chen) pp. 319–331. (Springer) 10.1007/978-981-97-0296-1_14

AOAC (2005) ‘Official methods of analysis. The association of official analytical chemists.’ 17th edn. (AOAC: Arlington, Virginia, USA)

Arias MSB, Peña-Cabriales JJ, Alarcón A, Maldonado Vega M (2015) Enhanced Pb absorption by Hordeum vulgare L. and Helianthus annuus L. plants inoculated with an arbuscular mycorrhizal fungi consortium. International Journal of Phytoremediation 17(5), 405-413.
| Crossref | Google Scholar |

Bai J, Lin X, Yin R, Zhang H, Junhua W, Xueming C, Yongming L (2008) The influence of arbuscular mycorrhizal fungi on As and P uptake by maize (Zea mays L.) from As-contaminated soils. Applied Soil Ecology 38(2), 137-145.
| Crossref | Google Scholar |

Beleri P (2023) Microbial solutions to soil health: the role of biofertilizers in sustainable agriculture. Environmental Reports 5(2), 6-9.
| Crossref | Google Scholar |

Bhatt R, Singh P (2020) Soil fertility status of Punjab Agricultural University regional research station Kapurthala. Agricultural Research Journal 57(2), 260-265.
| Crossref | Google Scholar |

Blake GR (1965) Particle density. In ‘Methods of soil analysis: part 1 physical and mineralogical properties, including statistics of measurement and sampling, Vol. 9’. (Ed. CA Black) pp. 371–373. (American Society of Agronomy, Soil Science Society of America)

Bremner JM, Mulvaney CS (1982) Nitrogen—total. In ‘Methods of soil analysis: part chemical and microbiological properties, Vol. 9’. (Ed. AL Page) pp. 595–624. (American Society of Agronomy, Inc., Soil Science Society of America, Inc.)

Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist 220(4), 1108-1115.
| Crossref | Google Scholar | PubMed |

Ci D, Tang Z, Ding H, Cui L, Zhang G, Li S, Dai L, Qin F, Zhang Z, Yang J, Xu Y (2021) The synergy effect of arbuscular mycorrhizal fungi symbiosis and exogenous calcium on bacterial community composition and growth performance of peanut (Arachis hypogaea L.) in saline alkali soil. Journal of Microbiology 59, 51-63.
| Crossref | Google Scholar | PubMed |

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(10), 370.
| Crossref | Google Scholar |

Dobo B (2022) Effect of arbuscular mycorrhizal fungi (AMF) and Rhizobium inoculation on growth and yield of Glycine max L. varieties. International Journal of Agronomy 2022(1), 9520091.
| Crossref | Google Scholar |

Dos Passos JH, Maia LC, de Assis DMA, da Silva JA, Oehl F, da Silva IR (2021) Arbuscular mycorrhizal fungal community structure in the rhizosphere of three plant species of crystalline and sedimentary areas in the Brazilian dry forest. Microbial Ecology 82(1), 104-121.
| Crossref | Google Scholar | PubMed |

Droh G, Djezou KM, Tuo S, Touré M, Kouassi A-B (2023) Morphometric characterization of endomycorrhizal fungi (glomeraceae and acaulosporaceae) from the Bouaflé and Niellé Areas in Côte d’Ivoire. American Journal of BioScience 11(1), 1-10.
| Crossref | Google Scholar |

Duan H-X, Luo C-L, Zhu S-Y, Wang W, Naseer M, Xiong Y-C (2021) Density- and moisture-dependent effects of arbuscular mycorrhizal fungus on drought acclimation in wheat. Ecological Applications 31(8), e02444.
| Crossref | Google Scholar |

Egberongbe HO, Akintokun AK, Babalola OO, Bankole MO (2010) The effect of Glomus mosseae and Trichoderma harzianum on proximate analysis of soybean (Glycine max (L.) Merrill.) seed grown in sterilized and unsterilised soil. Journal of Agricultural Extension and Rural Development 2(4), 54-58.
| Google Scholar |

El Hazzat N, Artib M, Touati J, Chliyeh M, Selmaoui K, Ouazzani Touhami A, Benkirane R, Douira A (2018) Diversity of endomycorrhizal fungi in the rhizosphere of chickpea in Morocco. Acta Phytopathologica et Entomologica Hungarica 53(2), 181-193.
| Crossref | Google Scholar |

Ganguly R, Yun M, Lee C-S (2024) Integration of concentration gradient generator with competitive PCR in a droplet for rapid nucleic acid quantification. Process Biochemistry 147, 1-9.
| Crossref | Google Scholar |

Gee GW, Bauder JW (1986) ‘Maize research and production in Nigeria.’ (Institute of Agriculture University of Ife Moor Plantation: Ibadan, Nigeria)

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

Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84(3), 489-500.
| Crossref | Google Scholar |

Goldmann K, Boeddinghaus RS, Klemmer S, Regan KM, Heintz-Buschart A, Fischer M, Prati D, Piepho H-P, Berner D, Marhan S, Kandeler E, Buscot F, Wubet T (2020) Unraveling spatiotemporal variability of arbuscular mycorrhizal fungi in a temperate grassland plot. Environmental Microbiology 22(3), 873-888.
| Crossref | Google Scholar | PubMed |

Goswami BR, Parakhia MV, Golakiya BA, Kothari CR (2018) Morphological and molecular identification of arbuscular mycorrhizal (AM) fungi. International Journal of Current Microbiology and Applied Sciences 7(1), 2336-2347.
| Crossref | Google Scholar |

Hashem A, Kumar A, Al-Dbass AM, Alqarawi AA, Al-Arjani ABF, Singh G, Farooq M, Abd_Allah EF (2019) Arbuscular mycorrhizal fungi and biochar improves drought tolerance in chickpea. Saudi Journal of Biological Sciences 26(3), 614-624.
| Crossref | Google Scholar | PubMed |

Hassaan MA, Alishba H, Aslam S, Danyal M, Abbas Z, Ullah A, Babar MM, Haider Z, Iqbal A (2024) Crop rotation as an economic strategy for small-scale farmers: evidence from Punjab, Pakistan. Journal of Oasis Agriculture and Sustainable Development 6(02), 31-39.
| Crossref | Google Scholar |

Hipólito-Piedras RP, Méndez-Cortés H, Ramírez-Tobías HM, Olalde-Portugal V (2024) Glomus nanolumen (Glomeraceae), un hongo micorrízico arbuscular en México. Acta Botanica Mexicana 131, e2226.
| Crossref | Google Scholar |

Houngnandan P, Yemadje RGH, Kane A, Boeckx P, Van Cleemput O (2009) Impact of agricultural practices on the dynamics of soil carbon pools in West Africa: a case study in Benin. Agricultural Systems 100(1), 38-46.
| Google Scholar |

Jacquemyn H, Merckx V, Brys R, Tyteca D, Cammue BPA, Honnay O, Lievens B (2011) Analysis of network architecture reveals phylogenetic constraints on mycorrhizal specificity in the genus Orchis (Orchidaceae). New Phytologist 192(2), 518-528.
| Crossref | Google Scholar | PubMed |

Khalid Chaudhry U, Shahzad S, Nadir Naqqash M, Saboor A, Yaqoob S, Salim M, Khalid M (2016) Integration of biochar and chemical fertilizer to enhance quality of soil and wheat crop (Triticum aestivum L.). PeerJ PrePrints 4, 1631v1.
| Crossref | Google Scholar |

Khan Z (2023) Root colonization and spore population of AM fungi in cultivated crops. International Journal of Science and Research Archive 10(1), 984-989.
| Crossref | Google Scholar |

Koul B, Sharma K, Sehgal V, Yadav D, Mishra M, Bharadwaj C (2022) Chickpea (Cicer arietinum L.) biology and biotechnology: from domestication to biofortification and biopharming. Plants 11(21), 2926.
| Crossref | Google Scholar | PubMed |

Krishnamoorthy R, Kim C-G, Subramanian P, Kim K-Y, Selvakumar G, Sa T-M (2015) Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS ONE 10(6), e0128784.
| Crossref | Google Scholar | PubMed |

Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiology Ecology 65(2), 339-349.
| Crossref | Google Scholar | PubMed |

Lester D (2009) Buying and applying mycorrhizal fungi. Max. Yield, USA.

Liu W, Zhang Y, Jiang S, Murray PJ, Liao L, Li X, Zhang J (2019) Spatiotemporal differences in the arbuscular mycorrhizal fungi communities in soil and roots in response to long-term organic compost inputs in an intensive agricultural cropping system on the North China Plain. Journal of Soils and Sediments 19, 2520-2533.
| Crossref | Google Scholar |

Madurapperuma WS, Kumaragamage D (1999) Evaluation of AB-DTPA extractant for the estimation of plant available macro and micro nutrients in acidic and neutral soils. Journal of the Soil Science Society of Sri Lanka 11, 29-36.
| Google Scholar |

Maffo AF, Ngonkeu ELE, Chaintreuil C, Temegne CN, Ntsomboh-Ntsefong G, Fall F, Youmbi E (2022) Morphological and molecular diversity of arbuscular mycorrhizal fungi associated to Carica papaya L. rhizosphere in two agro-ecological zones in Cameroon. African Journal of Agricultural Research 18(8), 632-646.
| Crossref | Google Scholar |

Mahmoudi N, Cruz C, Mahdhi M, Mars M, Caeiro MF (2019) Arbuscular mycorrhizal fungi in soil, roots and rhizosphere of Medicago truncatula: diversity and heterogeneity under semi-arid conditions. PeerJ 7(7), e6401.
| Crossref | Google Scholar |

Makkar A, Chatli AS, Sharma A, Kaur P, Kaur N, Goswami E (2018) Analysis of soil samples from various areas of Punjab. International Journal of Research in Engineering, Science and Management 1(11), 496-498.
| Google Scholar |

Manoharan PT, Pandi M, Shanmugaiah V, Gomathinayagam S, Balasubramanian N (2008) Effect of vesicular arbuscular mycorrhizal fungus on the physiological and biochemical changes of five different tree seedlings grown under nursery conditions. African Journal of Biotechnology 7(19), 3431-3436.
| Google Scholar |

Marizal S, Syariyah A (2017) The diversity of arbuscular mycorrhiza fungus (AMF) indigenous in peanuts (Arachis hypogea L.) rhizosphere under different elevation. Journal of Tropical Soils 21(2), 109-114.
| Crossref | Google Scholar |

McLean EO (1983) Soil pH and lime requirement. In ‘Methods of soil analysis. Part 2: chemical and microbiological properties.’ 2nd edn. (Ed. AL Page) (American Society of Agronomy: Madison, WI) pp. 199–224.

Mehrvarz S, Chaichi MR (2008) Effect of phosphate solubilizing microorganisms and phosphorus chemical fertilizer on forage and grain quality of barely (Hordeum vulgare L.). American-Eurasian Journal of Agricultural & Environmental Sciences 3(6), 855-860.
| Google Scholar |

Melo CD, Walker C, Krüger C, Borges PAV, Luna S, Mendonça D, Machado AC, Fonseca HMAC, Machado AC (2019) Environmental factors driving arbuscular mycorrhizal fungal communities associated with endemic woody plant Picconiaazorica on native forest of Azores. Annals of Microbiology 69, 1309-1327.
| Crossref | Google Scholar |

Meng EM (2023) Investigating the ecological role of arbuscular mycorrhizal fungi (AMF) in natural ecosystems. International Journal of Science and Research Archive 10(02), 524-534.
| Crossref | Google Scholar |

Mulyadi , Jiang L (2023) The combined application of biochar and arbuscular mycorrhizal fungi (AMF) enhanced the physical and chemical properties of soil and rice productivity in Indonesia. Sustainability 15(12), 9782.
| Crossref | Google Scholar |

Naderi NM, Alizadeh O, Nasr AH (2010) Some macro nutrients uptake optimizing by effect of mycorrhizae fungi in water stress condition in sorghum plant. In ‘Proceedings of the 2010 International Conference on Environmental Engineering and Applications,’ 10–12 September 2010, Singapore. pp. 160–164. (IEEE)

Nahar K, Bovill B, McDonald G (2021) Mycorrhizal colonization in bread wheat varieties differing in their response to phosphorus. Journal of Plant Nutrition 44(1), 29-45.
| Crossref | Google Scholar |

Nair VD, Sollenberger LE (2022) Final report for: evaluating soil phosphorus bioavailability in florida soils of variable composition. FDACS Contract #: 27155.

Ndeko AB, Chuma GB, Chokola GM, Kulimushi PZ, Mushagalusa GN (2024) Soil properties shape the arbuscular mycorrhizal status of common bean (Phaseolus Vulgaris) and soil mycorrhizal potential in kabare and walungu territories, Eastern DR Congo. Agricultural Research 13, 287-299.
| Crossref | Google Scholar |

Noreen S, Yaseen T, Iqbal J, Abbasi BA, Farouk Elsadek M, Eldin SM, Ijaz S, Ali I (2023) Morphological and molecular characterizations of arbuscular mycorrhizal fungi and their influence on soil physicochemical properties and plant nutrition. ACS Omega 8(36), 32468-32482.
| Crossref | Google Scholar | PubMed |

Ogoma BO, Omondi SF, Ngaira J, Kimani JW (2021) Molecular diversity of arbuscular mycorrhizal fungi (AMF) associated with Carissa edulis, an endangered plant species along Lake Victoria Basin of Kenya. International Journal of Forestry Research 2021(1), 7792282.
| Google Scholar |

Pakistan Ministry of Agriculture Works. Planning Unit (1970) Agricultural statistics of Pakistan (No. 6). Manager, Print. Corporation of Pakistan.

Pellegrino E, Bedini S (2014) Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry 68, 429-439.
| Crossref | Google Scholar |

Pepe A, Giovannetti M, Sbrana C (2016) Different levels of hyphal self-incompatibility modulate interconnectedness of mycorrhizal networks in three arbuscular mycorrhizal fungi within the Glomeraceae. Mycorrhiza 26(4), 325-332.
| Crossref | Google Scholar | PubMed |

Perez Y, Schenck NC (1989) The international culture collection of VA mycorrhizal fungi (Ietvam). In ‘Developments in soil science, Vol. 18’. (Eds V Vančura, F Kunc) pp. 171–175. (Elsevier)

Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55(1), 158-161.
| Crossref | Google Scholar |

Ramakrishnan K, Selvakumar G (2012) Influence of AM fungi on plant growth and nutrient content of tomato (Lycopersicum esculentum Mill). International Journal of Research in Botany 2(4), 24-26.
| Google Scholar |

Rehman MMU, Zhu Y, Abrar M, Khan W, Wang W, Iqbal A, Khan A, Chen Y, Rafiq M, Tufail MA, Ye J-S, Xiong Y-C (2024) Moisture- and period-dependent interactive effects of plant growth-promoting rhizobacteria and AM fungus on water use and yield formation in dryland wheat. Plant and Soil 502(1), 149-165.
| Crossref | Google Scholar |

Rożek K, Rola K, Błaszkowski J, Leski T, Zubek S (2020) How do monocultures of fourteen forest tree species affect arbuscular mycorrhizal fungi abundance and species richness and composition in soil? Forest Ecology and Management 465, 118091.
| Crossref | Google Scholar |

Saeed M, Khan I, Hameed A, Ullah I, Chaudhry MS, Naveed-Ul-Haq A, Kaleem S (2020) Arbuscular mycorrhizal fungi (AMF) and soil chemical heterogeneity significantly alters nutritional value of tomato fruit. Pakistan Journal of Botany 54(1), 187-193.
| Crossref | Google Scholar |

Sajedi NA, Rejali F (2011) Effects of drought stress, Zinc application and mycorrhiza inoculation on uptake of micro nutrients in maize. Journal of Soil Research 25(2), 83-92.
| Crossref | Google Scholar |

Samanhudi YA, Pujiasmanto B, Rahayu M (2014) Application of organic manure and mycorrhizal for improving plant growth and yield of temulawak (Curcuma xanthorrhiza Roxb). Scientific Research Journal 2(5), 11-16.
| Google Scholar |

Sarah S, Burni T (2013) Symbiotic response of three tropical sorghum varieties to arbuscular mycorrhizal fungal inoculation in marginal soil. International Journal of Agriculture Innovations and Research 1(4), 116-121.
| Google Scholar |

Sasvári Z, Hornok L, Posta K (2011) The community structure of arbuscular mycorrhizal fungi in roots of maize grown in a 50-year monoculture. Biology and Fertility of Soils 47, 167-176.
| Crossref | Google Scholar |

Saurabh Jha S, Songachan LS (2023) The usage of arbuscular mycorrhizal fungi (Amf) as a biofertilizer. Available at https://doi.org/10.21203/rs.3.rs-2559546/v1

Schulte EE, Hoskins B (1995) Recommended soil organic matter tests. In ‘Recommended soil testing procedures for the North Eastern USA.’ (Eds EE Schulte, B Hoskins) pp. 63–73. (Northeastern Regional Publication)

Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi. Journal of Plant Physiology 164(9), 1144-1151.
| Crossref | Google Scholar | PubMed |

Šmilauer P, Košnar J, Kotilínek M, Šmilauerová M (2020) Contrasting effects of host identity, plant community, and local species pool on the composition and colonization levels of arbuscular mycorrhizal fungal community in a temperate grassland. New Phytologist 225(1), 461-473.
| Crossref | Google Scholar | PubMed |

Smith SE, Read DJ (2010) ‘Mycorrhizal symbiosis.’ (Academic press)

Solangi F, Zhu X, Khan S, Rais N, Majeed A, Sabir MA, Iqbal R, Ali S, Hafeez A, Ali B, Ercisli S, Kayabasi ET (2023) The global dilemma of soil legacy phosphorus and its improvement strategies under recent changes in agro-ecosystem sustainability. ACS Omega 8(26), 23271-23282.
| Crossref | Google Scholar | PubMed |

Solangi F, Zhu X, Solangi KA, Iqbal R, Elshikh MS, Alarjani KM, Elsalahy HH (2024) Responses of soil enzymatic activities and microbial biomass phosphorus to improve nutrient accumulation abilities in leguminous species. Scientific Reports 14(1), 11139.
| Crossref | Google Scholar | PubMed |

Sparks DL, Page AL, Helmke PA, Loeppert RH (Eds) (2020) ‘Methods of soil analysis, part 3: chemical methods, Vol. 14.’ (John Wiley & Sons)

Stahl PD, Christensen M (1982) Mycorrhizal fungi associated with Bouteloua and Agropyron in wyoming sagebrush-grasslands. Mycologia 74(6), 877-885.
| Crossref | Google Scholar |

Subramanian KS, Bharathi C, Jegan A (2008) Response of maize to mycorrhizal colonization at varying levels of zinc and phosphorus. Biology and Fertility of Soils 45, 133-144.
| Crossref | Google Scholar |

Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. Applied Soil Ecology 26(2), 143-148.
| Crossref | Google Scholar |

Trejo-Aguilar D, Banuelos J (2020) Isolation and culture of arbuscular mycorrhizal fungi from field samples. Methods in Molecular Biology 2146, 1-18.
| Crossref | Google Scholar |

Wang Q, Ma M, Jiang X, Guan D, Wei D, Cao F, Kang Y, Chu C, Wu S, Li J (2020) Influence of 37 years of nitrogen and phosphorus fertilization on composition of rhizosphere arbuscular mycorrhizal fungi communities in black soil of northeast China. Frontiers in Microbiology 11, 539669.
| Crossref | Google Scholar | PubMed |

Wang W, Li M-Y, Zhu S-G, Khan A, Tao X-P, Huang G-F, Liu H-Y, Zhang W, Tao H-Y, Gong D-S, Song C, Xiong YC (2023) Plant facilitation improves carbon production efficiency while reducing nitrogen input in semiarid agroecosystem. CATENA 230, 107247.
| Crossref | Google Scholar |

Wu Q-S, Xia R-X, Zou Y-N (2006) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. Journal of Plant Physiology 163(11), 1101-1110.
| Crossref | Google Scholar | PubMed |

Xia Y-S, Chen B-D, Christie P, Andrew SF, Wang Y-S, Li X-L (2007) Arsenic uptake by arbuscular mycorrhizal maize (Zea mays L.) grown in an arsenic-contaminated soil with added phosphorus. Journal of Environmental Sciences 19(10), 1245-1251.
| Crossref | Google Scholar |

Xie K, Ren Y, Chen A, Yang C, Zheng Q, Chen J, Wang D, Li Y, Hu S, Xu G (2022) Plant nitrogen nutrition: the roles of arbuscular mycorrhizal fungi. Journal of Plant Physiology 269, 153591.
| Crossref | Google Scholar | PubMed |

Yaseen T, Khan Y, Rahim F, Wali S, Ahmad I, Begum HA, Ghani SS (2016) Arbuscular mycorrhizal fungi spores diversity and AMF infection in some medicinal plants of District Charsadda KPK. Pure and Applied Biology 5(4), 1176-1182.
| Crossref | Google Scholar |

Zhang M, Shi Z, Yang M, Lu S, Cao L, Wang X (2021) Molecular diversity and distribution of arbuscular mycorrhizal fungi at different elevations in Mt. Taibai of Qinling Mountain. Frontiers in Microbiology 12, 609386.
| Crossref | Google Scholar | PubMed |

Zhao J, Chen J, Beillouin D, Lambers H, Yang Y, Smith P, Zeng Z, Olesen JE, Zang H (2022) Global systematic review with meta-analysis reveals yield advantage of legume-based rotations and its drivers. Nature Communications 13(1), 4926.
| Crossref | Google Scholar |