سازوکارهای وابستگی میکوریزایی: تحلیل فرآیندهای فیزیولوژیک و مولکولی مؤثر در برقراری همزیستی میکوریزا آربوسکولار

نوع مقاله : مقاله مروری

نویسنده

حبیب الله نادیان قمشه

دانشگاه علوم کشاورزی و منابع طبیعی خوزستان، اهواز، ایران

https://doi.org/10.22067/jsw.2026.99478.1560

چکیده

طیف گسترده‌ای از گیاهان قادرند با قارچ‌های میکوریزا آربسکولار رابطه همزیستی برقرار کنند. این همزیستی سودمند حاصل مجموعه‌ای از تعاملات مولکولی و بیوشیمیایی بسیار پیچیده میان گیاه و قارچ است. برقراری این همزیستی از طریق تبادل پیام‌های شیمیایی ویژه‌ای آغاز می‌شود که هر یک از دو طرف برای شناسایی و برقراری ارتباط با دیگری ترشح می‌کنند و در نهایت به ایجاد یک ارتباط کارآمد منجر می‌گردد. با وجود این، شدت وابستگی گیاهان به قارچ‌های میکوریزا بسیار متفاوت است. هر گونه اختلال در فرآیندهای پیچیده فیزیولوژیک، بیوشیمیایی و مولکولی میان دو همزیست، می‌تواند به کاهش وابستگی میکوریزایی یا ناقص ماندن مسیر پیام‌رسانی در برقراری رابطه همزیستی و در نهایت عدم تشکیل آربسکول، که به‌عنوان قلب این همزیستی شناخته می‌شود، منجر شود. در "گیاهان نا میزبان" مسیر پیام‌رسانی مشترک بین قارچ و گیاه، مشابه گیاهان میکوریزایی آغاز می‌شود و تا مراحلی پیش می‌رود، با این حال، این مسیر به‌صورت ناقص متوقف شده و تشکیل آربسکول رخ نمی‌دهد. پیشرفت‌های اخیر در زیست‌شناسی مولکولی نشان داده است که مجموعه‌ای از ژن‌ها موسوم به "ژن‌های مسیر همزیستی مشترک" در شناسایی و برقراری همزیستی‌ نقش اساسی دارند. هر چند پیشرفت‌های حاصل در فناوری‌های زیستی افق‌های تازه‌ای را برای بهبود و تقویت همزیستی میکوریزایی گشوده است، با وجود این، هنوز چالش‌های زیادی در شناخت، گسترش و کاربرد آن‌ها وجود دارند. مقاله مروری-تحلیلی حاضر با هدف ارائه یک دیدگاه جامع و یکپارچه به بررسی سازوکارهای مختلف بیوشیمیایی، مولکولی و فنوتیپی دخیل در میزان وابستگی میکوریزایی گیاهان می‌پردازد. چنین دیدگاهی می‌تواند نقش مهمی در پیش‌برد کشاورزی پایدار و استفاده بهینه از منابع طبیعی ایفا نماید.

کلیدواژه‌ها

استریگولاکتون

پاسخ رشد میکوریزایی

فاکتورهای قارچی

غیرمیزبان

معماری ریشه

موضوعات

• علوم خاک

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عنوان مقاله English

Mechanisms of Mycorrhizal Dependency: Analysis of the Physiological, and Molecular Processes Involved in the Establishment of Arbuscular Mycorrhizal Symbiosis

نویسنده English

H. Nadian Ghomsheh

Agricultural and Natural Resources University of Khozestan, Ahvaz, Iran

چکیده English

Introduction
Mycorrhizal symbiosis, particularly arbuscular mycorrhiza, is recognized as one of the most widespread and beneficial interactions between plants and soil microorganisms and has been extensively studied. This symbiosis plays a significant role in improving plant nutritional status, enhancing resistance to both biotic and abiotic stresses, reducing the impact of certain pathogens, and promoting synergistic interactions with other beneficial microbial communities. Ultimately, these effects contribute to improved crop health and productivity. One of the most important benefits of this association is the enhancement of plant nutrition. Mycorrhizal plants acquire nutrients either directly through their roots or indirectly via the hyphal network of symbiotic fungi. The predominance of either pathway depends on a complex set of biochemical and molecular mechanisms within the common symbiosis pathway, as well as phosphorus availability, plant phenotypic traits (especially root characteristics), and environmental conditions. Despite its importance, the degree of mycorrhizal dependency varies among plant species and cultivars. Mycorrhizal dependency is defined as the extent to which a plant relies on mycorrhizal fungi to achieve optimal growth or yield. It is determined by the interaction between plant genotype and phenotype in combination with environmental factors.
Mycorrhizal symbiosis is the result of a complex molecular dialogue between plant and fungus, involving the exchange of signals at cellular, molecular, and genetic levels. In the early stages of symbiosis, plants secrete compounds such as strigolactones from their roots, which stimulate spore germination and hyphal branching. This is followed by fungal signalling molecules, including chito-lipo-oligosaccharides, which act as key signals in the initiation and regulation of arbuscular mycorrhizal symbiosis. Disruption in this shared signalling pathway can lead to failure of symbiosis establishment or reduced mycorrhizal dependency.
Under high nutrient conditions, particularly high phosphorus availability, plant secretion of strigolactones is typically reduced. This illustrates how excess soil phosphorus can interfere with the common symbiosis signalling pathway and thereby decrease mycorrhizal dependency. The synthesis and secretion of strigolactones are regulated by the upregulation of genes such as D27, CCD7, CCD8, and MAX1.
Recent advances in plant molecular biology and genetics have identified a set of genes involved in the common symbiosis pathway that play essential roles in fungal signal recognition, activation of cellular responses, and the formation of fungal structures such as arbuscules. These genes, including SYMRK, CCaMK, and CYCLOPS, will be discussed in detail later. Depending on the upregulation or downregulation of these genes in the plant–fungus symbiotic pathway, a higher or lower degree of mycorrhizal dependency can be expected, respectively.

Materials and Methods
This analytical review integrates findings from researchers in this field by utilizing up-to-date studies on the intensity of plant–fungus symbiosis and the degree of mycorrhizal dependency from morphological, physiological, biochemical, and especially molecular dimensions. These studies are accessible through major international databases, including Web of Science and Scopus. In addition, Google Scholar provides an open-access platform for identifying recent publications, while specialized resources such as ScienceDirect, SpringerLink, and Taylor & Francis offer valuable journal articles, book chapters, and authoritative reference works related to mycorrhizal dependency and the underlying mechanisms involved, particularly from a molecular perspective.

Results
The results of numerous studies indicate that the establishment of symbiosis between plants and arbuscular mycorrhizal fungi requires a series of complex physiological, biochemical, and molecular interactions. This process is initiated by the secretion of Myc-LCO signalling molecules by the fungus, which are subsequently recognized by specific receptors in plant roots, including SYMRK (DMI2). Following recognition, the common symbiosis signalling pathway is activated, and the release of calcium ions (Ca²⁺) through DMI1 generates rhythmic calcium oscillations within plant cells. These oscillations function as informational codes that are decoded by the calcium and calmodulin-dependent protein kinase (CCaMK). The calcium signals are then translated into molecular responses, leading to the activation of the transcription factor CYCLOPS and the regulation of symbiosis-related gene expression, ultimately resulting in arbuscule formation. Any disruption or interruption in this signalling pathway may prevent arbuscule development, particularly in non-host plants. The degree of plant dependence on mycorrhizal fungi is influenced by a range of factors, including plant, fungal, and environmental characteristics. Among environmental factors, abiotic stresses such as drought play a critical role. Under drought conditions, the influx of Ca²⁺ into the plant cell cytosol decreases, leading to disturbances in cellular ion homeostasis. However, the presence of mycorrhizal fungi enhances the expression of calcium-sensing and signalling genes, including CBLs, CDPKs, and MAPKs, thereby activating Ca²⁺-dependent signalling pathways. This process regulates and reinforces the increase in cytosolic Ca²⁺ concentration, which acts as an important secondary messenger during the establishment and maintenance of mycorrhizal symbiosis. Furthermore, numerous studies have demonstrated a significant relationship between mycorrhizal dependency and root morphological characteristics. In general, plant species possessing a magnolioid root architecture exhibit a greater degree of dependence on arbuscular mycorrhizal fungi than species with non-magnolioid root systems.

Conclusions
Although many plant species can establish symbiosis with mycorrhizal fungi, the degree of dependency and effectiveness of this association varies considerably. These differences are largely determined by the complexity of signalling pathways and the regulation of symbiosis-related genes. A deeper understanding of the underlying molecular and cellular mechanisms is essential for improving mycorrhizal symbiosis, although significant challenges remain in its practical application.

کلیدواژه‌ها English

Myc-LCOs

Mycorrhizal growth response

Non-host plant

Root architecture

Sterigolactones

Authors retain the copyright. This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0)

 

مراجع

1.           Abdel-Salam, E., Alatar, A., & El-Sheikh, M.A. (2018). Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi Journal of Biological Sciences, 25(8), 1772-1780. https://doi.org/10.1016/j.sjbs.2017.10.015

2.           Ahmed, N., Li, J., Li, Y., Deng, L., Deng, L., Chachar, M., Chachar, Z., Chachar, S., Hayat, F., Raza, A., Umrani, J.H., Gong, L., & Tu, P. (2025). Symbiotic synergy: How arbuscular mycorrhizal fungi enhance nutrient uptake, stress tolerance, and soil health through molecular mechanisms and hormonal regulation.  International Mycological Association (IMA) Fungus, 16: e144989. https://doi.org/10.3897/imafungus.16.144989

3.           Akiyama, K., Matsuzaki, K.I., & Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi, Nature, 435(9), pp.824–827. https://doi.org/10.1038/nature03608

4.           Akiyama, K.,  & Hayashi, H. (2006). Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Annals Botany, 97(6), 925–931. https://doi.org/10.1093/aob/mcl063

5.           Al-Arjani, A.B.F., Hashem, A., & Abd-Allah, E.F. (2020). Arbuscular mycorrhizal fungi modulates dynamics tolerance expression to mitigate drought stress in Ephedra foliata Boiss. Saudi Journal of Biological Sciences, 27(1), 380-394. https://doi.org/10.1016/j.sjbs.2019.10.008

6.           Albornoz, F.E., Dixon, K.W., & Lambers, H. (2021). Revisiting mycorrhizal dogmas: Are mycorrhizas really functioning as they are widely believed to do? Soil Ecology Letters, 3, 73e82. https://doi.org/10.1007/s42832-020-0070-2

7.           Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., & Al-Babili, S. (2012). The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science, 16, 335(6074), 1348-51. https://doi.org/101126/science.1218094

8.           Al-karaki, G.N., & Al-Raddag, A. (1997). Effects of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Mycorrhiza, 7(2), 83–88. http:/doi.org/10.1007/s005720050166

9.           Allen, M.F., Allen, E.B., & Friese, C.F. (1989). Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular–arbuscular mycorrhizal fungi. New Phytologist, 111, 45-49. https://doi.org/10.1111/j.1469-8137.1989.tb04216.x

10.       Antolın-Llovera, M., Martina, K., Ried, M.K., & Parniske, M. (2014). Cleavage of the symbiosis receprorlike kinas ectodomain promotes complex formation with nod factor receptor. Current Biology, Cell Press, 24(4), 422-427. https://doi.org/10.1016/j.cub.2013.12.053

11.       Atkinson, E.M., Palcic, M.N., Hindsgaul, O., & Long, S.R. (1994). Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-asytletransferance activity. The Proceedings of the National Academy of Sciences, (18), 8418-22. https://doi.org/10.1073/pnas.91.18.8418

12.       Auge, R.M. (2001). Foliar dehydration tolerance of mycorrhizal cowpea, soybean and bush bean. New Phytologist, 151, 535–541. https://doi.org/10.1046/j.0028-646X.2001.00187.x

13.       Auge, R.M., Toler, H.D., & Saxton, A.M. (2015). Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza, 25(1), 13-24. https://doi.org/10.1007/s00572-014-0585-4

14.       Baylis, G.T.S. (1975). The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Endomycorrhizas (Eds. F. E. Sanders, B. Mosse and P. B. Tinker), pp 373-389, Academic Press, London. Recor ID: 44446a67-a05b-11d5-8aeb-0002a519b2f3.

15.       Bethlenfalvay, G.J., Pacovsky, R.W., Brown, M.S., & Fuller, G. (1982). Mycotrophic growth and mutualistic development of host plant and fungal endophyte in an endomycorrhizal symbiosis. Plant and Soil, 68, 43-54. https://doi.org/10.1007/BF02374726

16.       Bhoi, A., Yadu, B., Chandra, J., & Keshavkant, S. (2021). Contribution of strigolactone in plant physiology, hormonal interaction and abiotic stresses. Planta, 9:254(2), 28. https://doi.org/10.1007/s00425-021-03678-1

17.       Boan, J., Smith, S.E., & Alston, A.M. (1993). Mycorrhizal responses of barley cultivars differing in P efficiency. Plant and Soil, 157, 97–105. https://doi.org/10.1007/BF00038752

18.       Boyno, G., Rezaee Danesh, Y., Demir, S., Teniz, N., Mulet, J.M., & Porcel, R. (2023). The complex interplay between arbuscular mycorrhizal fungi and strigolactone: Mechanisms, sinergies, applications and future directions. International Journal of Molecular Science, 24, 16774. https://doi.org/10.3390/ijms242316774

19.       Brundrett, M.C., & Tedersoo, L. (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist, 220, 1108–1115. https://doi.org/10.1111/nph.14976

20.       Brundrett, M.C., & Kendrick, B. (1988). The mycorrhizal status, root anatomy and phenology of plants in a sugar maple forest. Canadian Journal of Botany, 66, 1153-1173. https://doi.org/10.1139/b88-166

21.       Brundrett, M.C. (1991). Mycorrhizas in natural ecosystems. Advances in Ecological Research 21, 171-313, Academic Press. htpps://doi.org/10.1016/S0065-2504(08)60099-9

22.       Brundrett, M.C. (2002). Coevolution of roots and mycorrhizas of land plants. New Phytologist, 154(2), 275-304. https://doi.org/10.1046/j.1469-8137.2002.00397.x

23.       Charpentier, M., Martins, T.V., Granqvist, E., Oldroyd, G.E.D., & Morris, R.J. (2013). The role of DMI1 in establishing Ca²⁺ oscillations in legume symbioses. Plant Signalling and Behaviour, 8(2), e22894. https://doi.org/10.4161/psb.22894

24.       Chen, J., Zhang, H., Zhang, X., & Tang, M. (2017). Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K⁺/Na⁺ homeostasis. Frontier Plant Science, 8, 1739. https://doi.org/10.3389/fpls.2017.01739

25.       Chen, J., Guo, J., Li, Z., Liang, X., You, Y., Li, M., He, Y., & Zhan, F. (2022). Effects of an arbuscular mycorrhizal fungus on the growth of and cadmium uptake in maize grown on polluted wasteland, farmland and slope land soils in a lead-zinc mining area. Toxics, 10, 359. https://doi.org/10.3390/ toxics10070359

26.       Cosme, M., Fernandez, I., Van er Heijden, M.G.A., & Pieterse, C.M.J. (2018). Non-mycorrhizal plants: the exceptions that prove the rule. Trends in Plant Science, 23, 577–587. https://doi.org/10.1016/j.tplants.2018.04.004

27.       Dastogeer, K.M.G., Zahan, M.I., Arif, M.T.U, Akter, M.A., & Okazaki, S. (2020). Plant salinity tolerance conferred by arbuscular mycorrhizal fungi and associated mechanisms: A Meta-analysis. Frontier in Plant Science, 9(11), 588550. https://doi.otg/10.3389/fpls.2020.588550

28.       Díaz, V., Villalobos, M., Arriaza, K., Flores, K., HernandezSaravia, L.P., & Velasquez, A. (2025). Decoding the dialog between plants and arbuscular mycorrhizal fungi: A molecular genetic perspective. Genes, 16, 143. https://doi.org/10.3390/genes16020143

29.       Dickson, A., Leaf, A.L., & Hosner, J.F. (1960). Quality appraisal of white spruce and white pine seedling stock in nurseries. Forestry Chronicle, 36(1), 10-13. https://doi.org/10.5558/tfc36010-1

30.       Ding, X., Jiang, Y., He, L., Zhou, Q., Yu, J., Hui, D., & Huang, D. (2016). Exogenous glutathione improves high root-zone temperature tolerance by modulating photosynthesis, antioxidant and osmolytes systems in cucumber seedlings. Scientific Reports, 6, 1–12. https://doi.org/10.1038/srep35424

31.       Dong, F., Wang, Y., Tao, J., Xu, T., & Tang, M. (2023). Arbuscular mycorrhizal fungi affect the expression of PxNHX gene family, improve photosynthesis and promote Populus simonii×P. nigra growth under saline-alkali stress. Frontier in Plant Science, 14, 1104095. https://doi.org/10.3389/fpls.2023.1104095

32.       Eo, J.K., & Eom, A.H. (2009). Differential growth response of various crop species to arbuscular mycorrhizal inoculation. Mycobiology 37(1), 72-76.

33.       Evelin, H., Devi, T.S., Gupta, S., & Kapoor, R. (2019). Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Frontier in Plant Science, 10, 470. https://doi.org/10.3389/fpls.2019.00470

34.       Fernandez, I., Cosme, M., Stringlis, I.A., Yul, K., de Jonge, R., van Wees, S.C.M., Pozo, M.J., Pieterse, C.M.J., & van der Heijiden, M.G.A. (2019). Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism. New Phytologist, 223, 867-881. https://doi.org/10.1111/nph.15798

35.       Fitter, A.H. (1989). An ecological flora. Bulletin of British Ecological Society, 20, 199-200.

36.       Fitter, A.H. (2004). Magnolioid roots – hairs, architecture and mycorrhizal dependency. New Phytologist, 164(1), 15-16. https://doi.10.1111/j.1469-8137.2004.01193.x

37.       Fitter, A.H., & Merryweather, J.W. (1992). Why are some plants more mycorrhizal than others? An ecological enquiry. In: Mycorrhizas in Ecosystems (Eds. D. J. Read, D. H. Lewis, A. H. Fitter and I. J. Alexander), pp 26-36, CAB International, Wellingford, UK.

38.       Gener, A., Chabaud, M., Balzergue, C., Puech-Pages, V., Novero, M., Rey, T., Fournier, J., Rochange, S., Becard, G., Bonfante P., & Barker D.G. (2013). Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca²⁺ spiking in Medicago truncatula roots and their production is enhanced by strigolactone production. New Phytologist, 198, 190–202. https://doi.org/10.1111/nph.12146

39.       Gerdemann, J.W. (1975). “Vesicular-arbuscular mycorrhiza. In: The Development and Function of Roots”, ed. J.G. Torrey and D.T. Clarkson. Academic Press, London, 575–592.

40.       Ghasemjokar, N., Nadian. H. Khalilimoghdam, B., Haydari, M., & Gharineh, M. (2016). Effect of myorrhizal colonization on plant growth and proline content in some genotype of leeks (Allium ampeloprasum ssp. persicum L, Allium porrum L.). Plant productions, 38(1), 15-26. (In Persian). https//doi.org/22055/ppd.2015.11115

41.       Ghasemjokar, N., Nadian. H. Khalilimoghdam, B., & Haydari, M. (2014). Effects of arbuscular mycorrhizal fungus and drought stress on plant root growth, accumulation of proline and uptake of some nutrients by three genotypes of leeks. Journal of Soil Biology. 1(2). (In Persian). https://doi.org/10.22092/sbj.2014.128410

42.       Ghosh, S., Kuila, D., & Verma, N.K. (2016). Arbuscular mycorrhizal dependency of plants. In book: Recent Trends in Biofertilizer, 174(1-24).

43.       Glenn, M.G., Chew, F.S., & Williams, P.H. (1985). Hyphal penetration of Brassica (Cruciferae) roots by a vesicular–arbuscular mycorrhizal fungus. New Phytologist, 99, 463–472, https://doi.org/doi.10.1111/j.1469-8137.1985.tb03673.x

44.       Grasso, S.V., Rayan, M.H., Albornoz, E.E., & Renton, M. (2025). A simple plant–mycorrhizal fungal resource trade co‐evolution model explains mutualism stability, extinction and transitory parasitism via fitness feedback. New Phytologist, 12;248(3), 1429–1441. https://doi.org/10.1111/nph.70540

45.       Guo, X., Wang, P., Wang, X., Li, Y., & Ji, B. (2022). Specific plant mycorrhizal responses are linked to mycorrhizal fungal species interactions. Frontiers in Plant Science, 13, 930069. https://doi.org/10.3389/fpls.2022.930069

46.       Haghighania, H., Nadian, H. Ragali, F., & Tavakoli, A.R. (2012). Effect of two species of arbuscular mycorrhizae on vegetative growth and P uptake by Mexican Lime Rootstock (Citrus aurantifolia) under drought stress. Journal of Seed and Plant Production, 28(4), 403-417. (In Persian). https://doi.org/10.22092/sppj.2017.110486

47.       Hany, A., Nadian, H., & Barzegar, A.R. (2007). Study of mycorrhizal dependency and yield of two clover species. Journal of Soil and Water Sciences, 21(2), 269-276. (In Persian).  

48.       He, J., Huang, R., & Xie, X. (2024). A gap in the recognition of two mycorrhizal factors: new insights into two LysM-type mycorrhizal receptors. Frontier in Plant Science, 15:14,18699. https://doi.org/10.3389/fpls.2024.1418699

49.       Hestrin, R., Hammer, E.C., Muller, C.W., & Lehman, J. (2019). Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Communications Biology, 2(1), 233. https://doi.org/10.1038/s42003-019-0481-8

50.       Hetrick, B.A.D., Kitt, D.G., & Willson, G.T. (1988). Mycorrhizal dependence and growth habit of warm-season and cool-season tallgrass prairie plants. Canadian Journal of Botany, 66(7). https://doi.org/10.1139/b88-193

51.       Hetrick, B.A.D., Wilson, G.W.T., & Cox, T.S. (1992). Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Canadian Journal of Botany, 70, 2032–2040. https://doi.org/10.1139/b92-253

52.       Hoeksema, J.D. (2010). Ongoing coevolution in mycorrhizal interactions. New Phytologist, 187, 286–300. https://doi.org/10.1111/j.1469-8137.2010.03305.x

53.       Holsters, M. (2008). SYMRK, an enigmatic receptor guarding and guiding microbial endosymbioses with plant roots. Proceedings of the National Academy of Sciences of the United States of America, 18;105(12), 4537–4538. htpps://doi.org/10.1073/pnas.0801270105

54.       Hull, R., Choi, J., & Paszkowski, U. (2021). Conditioning plants for arbuscular mycorrhizal symbiosis through DWARF14-LIKE signalling. Current Opinion in Plant Biology, 62, 102071. https://doiorg/10.1016/j.pbi.2021.102071

55.       Ho-Plagaro, T., & García-Garrido, J.M. (2022). Molecular regulation of arbuscular mycorrhizal symbiosis. International Journal of Molecular Science, 23(11), 5960. https://doi.org/10.3390/ijms23115960

56.       Hou, X., Zhou, S., Guan, Y., Shi, H., & Liu, W. (2026). Evolutionary analysis of MOCA1 gene in Arabidopsis thaliana and functional comparison with PGSIP7 and PGSIP8 genes. Frontier in Plant Science, 17, 1734646. https://doi.org/10.3389/fpls.2026.1734646

57.       Incesu, M., Cimen, B., Yilmaz, B., Yesiloglu, T., & Ortas, I. (2025). Influences of arbuscular mycorrhizal fungi on Diospyros lotus seedlings under salinity stress. Frontiers in Plant Science, 16, 1595144. https://doi.org/10.3389/fpls.2025.1595144

58.       Jakobsen, I., Abbott, L.K., & Robson, A.D. (1992). External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterranean L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist, 120, 371-380. https://doi.org/10.1111/j.1469-8137.1992.tb01077.x

59.       Janos, D.P. (1980). Vesicular-arbuscular mycorrhizae affect lowland tropical rain forest plant growth. Ecology, 61(1), 151–162. https://doi.org/10.2307/1937165

60.       Jiang, J., Zhou, X., Tao, M., Yuan, F., Liu, L., Wu, F., Wu, X., Xiang, Y., Niu, Y., Liu, F., Li, C., Ye, R., Byeon, B., Xue, Y., Zhoa, H., Wang, H.N., Crawford, B.M., Johnson, D.M., Hu,C., Pie, C., Zhou, W., Swift, G.B., Zhang, H., & Vo-Dinh, T. (2019). Plant cell-surface GIPC sphingolipids sense salt to trigger Ca²⁺ influx. Nature, 572, 341–346. http://doi.org/10.1038/s41586-019-1449-z

61.       Johnson, N.C., Graham, J.H., & Smith, F.A. (1997). Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist, 135, 575–585. https://doi.org/10.1046/j.1469-8137.1997.00729.x

62.       Klironomos, J.N. (2003). Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84(9), 2292–2301. https://doi.org/10.1890/02-0413

63.       Kodama, K., Rich, M.K., Yado, A., Shimazaki, S., Xie, X., Akiyama, K., Mizuno, Y., Komatsu, A., Luo, Y., Suzuki, H., Kameoka, H., Libourel, C., Keller, J., Sakakibara, K., Nishiyama, T., Nakagawa, T., Mashiguchi, K., Uchida, K., Yoneyama, K., Tanaka, Y., Yamaguchi, S., Shimamura, M., Delaux, P.M., Nomura, T., & Kyozuka, J. (2022). An ancestral function of strigolactones as symbiotic rhizosphere signals. Nature Commuication, 13, 3974. https://doi.org/10.1038/s41467-022-31708-3

64.       Lanfranco, L., Fiorilli, V., Venice, F., & Bonfante, P. (2018). Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. Journal of Experimental Botany, 69(9), 2175–2188. https://doi.org/10.1093/jxb/erx432

65.       Liang, S.M., Li, Q.S., Liu, M.Y., Hashem, A., Al-Arjani, A.B.F., Alenazi, M.M., Abd Allah, E.F., Muthuramalingam, P., & Wu, Q.S. (2022). Mycorrhizal effects on growth and expressions of stress-responsive genes (aquaporins and SOSs) of tomato under salt stress. Journal of Fungi, 8, 1305. https://doi.org/10.3390/jof8121305

66.       Liu, M.Y., Li, Q.S., Ding, W.Y., Dong, W.Y., Chen, J.H., Tian, X., Hashem, A., Fahad Al-Arjani, A.B, Alenazi, M.M., Fathi Abd-Allah, E. & Wu, Q.S. (2023). Arbuscular mycorrhizal fungi inoculation impacts expression of aquaporins and salt overly sensitive genes and enhances tolerance of salt stress in tomato. Nature Communications, Chemical and Biological Technologies in Agriculture, 10, 5. https//doi.10. 1186/ s4053 8-022-00368-2.

67.       Lopez-Obando, M., Ligerot Y., Bonhomme, S., Boyer, F.D., & Rameau, C. (2015). Strigolactone biosynthesis and signaling in plant development. Development, 142(21), 3615–3619. https://doi.org/10.1242/dev.120006

68.       Lu, Y., Yan, Y., Qin, J., Ou, L., Yang, X., Liu, F., & Xu, Y. (2023). Arbuscular mycorrhizal fungi enhance phosphate uptake and alter bacterial communities in maize rhizosphere soil. Frontier in Plant Science, 14, 1206870. https://doi.org/10.3389/fpls.2023.1206870

69.       Ma, X., Li, X., & Ludewig, U. (2021).  Arbuscular mycorrhizal colonization outcompetes root hairs in maize under low phosphorus availability. Annals of Botany, 2:127(1), 155–166. https://doi.org/10.1093/aob/mcaa159

70.       MacLean, A.M., Bravo, A., & Harrison, M.J. (2017). Plant signalling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. The Plant Cell, 29, 2319–2335. https://doi.org/10.1105/tpc.17.00555

71.       Mahherali, H. (2014). Is there an association between root architecture and mycorrhizal growth response? New Phytologist, 204(1), 192-200. https://doi.org/10.1111/nph.12927

72.       Maillet, F., Poinsot, V., Andre, O., Puech-Pages, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E.A., Driguez, H., Becard, G., & Denarie, J. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza, Nature, 7328(469), 58–63. https://doi.rog/10.1038/nature09622

73.       Marques-Galvez, J.E., Giovannini, L., Boccio, P.D., Sillo, F., Zampieri, E., Pagliarani, C., Walter Chitarra, W., De Rose, S., Vita, F., & Balestrini, R. (2025). Arbuscular mycorrhiza induce the regulation of Ca²⁺, ROS, and SOS pathways under salt stress in tomato roots. Physiologia Plantarum, 177:e70610 1 of 19, https://doi.org/10.1111/ppl.70610

74.       Mashiguchi, K., Seto, Y., & Yamaguch, S. (2021). Strigolactone biosynthesis, transport and perception. The Plant Journal, 10(2), 335-350. https://doi.org/10.1111/tpj.15059

75.       McHaffie, M.B., & Maherali, H. (2025). Variation in mycorrhizal growth response influences competitive interactions and mechanisms of plant species coexistence. Oecologia, 192(3), 755-765, https://doi.org/10.1007/s00442-020-04609-9

76.       Menge, J.A., Johnson, E.L.V., & Platt, R.G. (1978). Mycorrhizal dependency of several citrus cultivars under three nutrient regimes. New Phytologist, 81, 553–559. https://doiorg/10.1111/j.1469-8137.1978.tb01628.x

77.       Nadal, M., Sawers, R., Naseem, S., Bassin, B., Kulicke, C., Sharman, A., An, G., An, K., Ahern, K.R., Romag, A., Brutnell, T.P., Gutjahr, C., Geldner, N., Roux, C., Martinoia, E., Konopka, J.B., & Uta Paszkowski, U. (2017). An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nature Plants, 3, 17073. https://doi.10.1038/nplants.2017.73

78.       Nadian, H., Smith, S.E., Alston, A.M., & Murray, R.S. (1996). The effect of soil compaction on growth and P uptake by Trifolium subterraneum: Interactions with mycorrhizal colonization. Plant and Soil, 182, 39–49. https://doi.org/10.1046/j.1469-8137.1997.00653.x

79.       Nadian, H. (1997). Effects of soil compaction on growth and P uptake by Trifolium subterraneum colonized by AM fungi. Ph.D. thesis, Soil Science Department, Waite Campus, The University of Adelaide, Adelaide, Australia.

80.       Nadian, H. (2011). The effect of drought stress and mycorrhizal symbiosis on growth and phosphorus uptake by two different sorghum cultivars in root morphology. Journal of Water and Soil Science, Esfahan University of Technology, 57, 25-30. (In Persian)

81.       Nadian, H., Fathi, G., & Abdollahi, M. (2013a). Phosphorus inflow into two species of clover root with different morphology colonized by AM Fungi. Iran Agricultural Research, 32(1), 40-54. https://doi.org/10.1038/nplants.2017.73

82.       Nadian, H., Haydari, M., Gharineh, M.H., & Daneshvar, M.H. (2013b). Effect of NaCl and mycorrhizal colonization on growth and uptake of P, K and Na by saffron (Crocus sativus L.). Journal of Plant Production (Journal of Scientific Agricultural), 36(2), 49-59. (In Persian)

83.       Nadian, H. (2025). Phosphorus uptake and transport mechanism in symbiotic plants with arbuscular mycorrhizal fungi (knowns and unknowns), Journal of Soil Biology, 1(12), 155-190. (In Persian). https://doi.org/10.22092/SBJ.2024.366288.267

84.       Nadian, H. (2026). Plant-mycorrhiza responses to drought stress: Analysis of vital processes and defense mechanisms. Journal of Soil Biology, 14(1), (In Persian)

85.       Nagahashi, G., & Douds, D.D. (2011). The effects of hydroxy fatty acids on the hyphal branching of germinated spores of AM fungi. Fungal Biology, 115(4-5), 351–358. https://doi.org/10.1016/j.funbio.2011.01.006

86.       Navarro, J.M., Morte, A., & Pérez-Pérez, J.G. (2026). Mycorrhizal inoculation enhances drought resilience in citrus seedlings of two cultivars by modulating gas exchange and hormonal signalling. Plants, 15, 505. https://ui.adsabs.harvard.edu/link_gateway/2026Plnts.15.505N/doi:10.3390/plants15030505

87.       Olson, P.A., Thingstrub, I., Jakobsen, I., & Baath, E. (1999). Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biology and Biochemistry, 31, 1879–1887. https://doi.org/10.1016/S0038-0717(99)00119-4

88.       Peng, S., Eissenatat, D.M., Graham, J.H., Williams, K., & Hodge, N.C. (1993). Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiology, 101(3), 1063–1071. https://doi.org/10.1104/pp.101.3.1063

89.       Plenchette, C., Fortin, J.A., & Furlan, V. (1983). Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. I. Mycorrhizal dependency under field conditions. Plant and Soil, 70, 199-209. https://doi.org/10.1007/BF02374780

90.       Qi, J., Mao, Y., Cui, J., Lu, X., Xu, J., Liu, Y., Zhang, H., Yu, W., & Li, C. (2024). The role of strigolactones in resistance to environmental stress in plants. Physiologia Plantarum, 176(4), e14419, https://doi.org/10.1111/ppl.14419

91.       Qi, S., Wang, J., Wan, L., Dai, Z., da Silva Matos, D.M., Du, D., Egan, S., Bonser, S.P., Thomas, T., & Moles, A.T. (2022). Arbuscular mycorrhizal fungi contribute to phosphorous uptake and allocation strategies of Solidago canadensis in a phosphorous-deficient environment. Frontier in Plant Science, 13, 831654. https://doi.org/10.3389/fpls.2022.831654

92.       Romero, F., Argüello, A., de Bruin, S., & vander Heijden, M.G.A. (2023). The plant–mycorrhizal fungi collaboration gradient depends on plant functional group. Functional Ecology, 37, 2386–2398. https://doi.org/10.1111/1365-2435.14395

93.       Rui, R.F.D., Santos, S.C., Lourente, E.R.P., Scalon, S. P.Q., Schiavo, J.A., & Valim, W.C. (2021). Ecophysiology, quality, and mycorrhizal dependency in Musa spp. (cv. Grand naine) seedlings. Revista. Brasiliera de Frutichltura, 43(4), (e-097). https://doi.org/10.1590/0100-29452021097 

94.       Rush, T.A., Puech-Pagès, V., Bascaules, A., Jargeat, P., Maillet, F., Haouy, A., Maes, A.Q.M., Carriel, C.C., Khokhani, D., Keller-Pearson, M., Tannous, J., Cope, K.R., Garcia, K., Maeda, J., Johnson, C., Kleven, B., Choudhury, Q.J., Labbe, J., Swift, C., O’Malley, M.A., Bok, J.W., Cottaz, S., Fort, S., Poinsot, V., Sussman, M.R., Lefort, C., Nett, J., Keller, N.P., Becard, G., & Ane, J.M. (2020). Lipo-chitooligosaccharides as regulatory signals of fungal growth and development. Nature Communications, 4(11), 3897. https://doi.org/10.1038/s41467-020-17615-5

95.       Singh, S. (2001). Mycorrhizal dependency, Part. 1: Selection of efficient mycorrhizal fungi”. Mycorrhiza News, 11(1), 2–9.

96.       Singh, S., & Parniske, M. (2012). Activation of calcium- and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Current Opinion in Plant Biology, 14(4), 444-453. https://doi.org.10.1016/j.pbi.2012.04.002

97.       Smith, S.E. (1980). Mycorrhizas of autotrophic higher plants. Biological Reviews, 55, 475-510.

98.       Smith, S.E., Smith, F.A., & Jakobsen, I. (2003). Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology, 133,16–20. https://doi.org/10.1104/pp.103.024380

99.       Smith, S.E., Smith, F.A., & Jakobsen, I. (2004). Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist, 162, 511–524. https://doi.org/10.1111/j.1469-8137.2004.01039.x

100.     Smith, S.E., & Read, D.J. (2008). Mycorrhizal symbiosis. New York, NY, USA: Academic Press.

101.     Smith, F. & Smith, S. E. (2011). What is the significance of the arbuscular mycorrhizal colonization of many   economically important crop plants. Plant and Soil, 348, 63–79.

102.     Stanga, J.P., Smith, S.M., Brigges, W.R., & Nelson, D.C. (2013). Suppressor of more axillary growth controls seed germination and seedling development in Arabidopsis. Plant Physiology, 163, 318–330. https://doi.org/10.1104/pp.113.221259

103.     St Jhon, T.V. (1980). Root size, root hairs and mycorrhizal infection: a re-examination of Baylis’s hypothesis with tropical trees. New Phytologist, 84, 483-487. https://doi.org/10.1111/j.1469-8137.1980.tb04555.x

104.    Su, H., Wang, Q., Wang, L., & Cui, J. (2024). The Ca²⁺ regulated protein kinase CIPK1 modulates plant response to nitrate deficiency in Arabidopsis. Genes, 15, 1235. https://doi.org/10.3390/genes15091235

105.    Tanaka, S., Hashimoto, K., Kobayashi, Y., Yano, K., Maeda, T., Kameoka, H., Ezawa, T., Saito, K., Akiyama, K., & Kawaguchi, M. (2022). Asymbiotic mass production of the arbuscular mycorrhizal fungus Rhizophagus clarus. Communificatios Biology, 5, 43. https://doi.org/10.1038/s42003-021-02967-5

106.    Tian, H., Wang, R., Li, M., Dang, H., & Solaiman, Z.M. (2019). Molecular signal communication during arbuscular mycorrhizal formation induces significant transcriptional reprogramming of wheat (Triticum aestivum) roots. Annals of Botany, 124(6), 1109–1119. https://doi.org/10.1093/aob/mcz119

107.    Thirkell, T.J., Grimmer, M., James, L., Pastok, D., Allary, T., Elliott, A., Paveley, N., Daniell, T., & Field, K.J. (2022). Variation in mycorrhizal growth response among a spring wheat mapping population shows potential to breed for symbiotic benefit. Food and Energy Security, 11, e370. https://doi.org/10.1002/fes3.370

108.    Toro, K.S., & Brachmann, A. (2016). The effector candidate repertoire of the arbuscular mycorrhizal fungus Rhizophagus clarus. BMC Genomics, 17, 101. https://doi.10.1186/s12864-016-2422-y

109.    Wang, P., & Chen, Y. (2024). Protecting plants from pathogens through arbuscular mycorrhiza: Role of fungal diversity. Microbiology Reseach, 289, 127919. https://doi.org/10.1016/j.micres.2024.127919

110.    Wang, Y., He, X., & Yu, F. (2022). Non-host plants: Are they mycorrhizal networks players? Plant Diversity, 44(2), 127-134. https://doi.org/10.1016/j.pld.2021.06.005 

111.    Weinl, S., & Kudla, J. (2009). The CBL–CIPK Ca²⁺-decoding signalling network: function and perspectives. New Phytologist, 184, 517–528. https://doi.org/10.1111/j.1469-8137.2009.02938.x

112.    Wilson, G.W.T., & Hartnett, D.C. (1998). Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. American Journal of Botany, 85, 1732–1738. https://doi.org/10.2307/2446507

113.    Xu, W., & Huang, W. (2017). Calcium-dependent protein kinases in phytohormone signaling pathways. International Journal of Molecular Science, 18, 2436. https://doi.org/10.3390/ijms18112436

114.    Xu, P.J., Liu, S., Song, S., Guo, H., Tang, J., Yong, J.W.H., Ma, Y., & Chen, X. (2018). Arbuscular mycorrhizal fungi influence decomposition and the associated soil microbial community under different soil phosphorus availability. Soil Biology and Biochemestry, 120, 181-190. https://doi.org/10.1016/j.soilbio.2018.02.010  

115.    Yang, J., Lan, L., Jin, Y., Yu, N., Wang, D., & Wang, E. (2022). Mechanisms underlying legume–rhizobium symbioses. Journal of Integrative Plant Biology, 64, 244–267. https://doi.org/10.1111/jipb.13207

116.    Ye, Q., Wang, H., & Li, H. (2022). Arbuscular mycorrhizal fungi improve growth, photosynthetic activity, and chlorophyll fluorescence of Vitis vinifera L. cv. ecolly under drought stress. Agronomy, 12(7), 1563. https://doi.org/10.3390/agronomy12071563

117.    Yin, X., Zhang, W., Feng, Z., G., Zhu, H., & Yao, Q. (2024). Improved observation of colonized roots reveals the regulation of arbuscule development and senescence by drought stress in the arbuscular mycorrhizae of citrus. Horticultural Plant Journal, 10(2), 425e436. https://doi.org/10.1016/j.hpj.2023.04.006

118.    Yoneyama, K. (2019). How do strigolactones ameliorate nutrient deficiencies in plants? Cold Spring Harbor Perspectives in Biology, 11(8), a034686. https://doi.org/10.1101/cshperspect.a034686

119.    Yuan, P., Luo, F., Gleason, C., & Poovaiah, B.W. (2022). Calcium/ calmodulin-mediated microbial symbiotic interactions in plants. Frontier in Plant Science, 13, 984909. https://doi.org/10.3389/fpls.2022.984909

120.    Zangaro, W., Nishidate, F.R., Vandresen, J., Andrade, G., & Nogueira, M.A. (2007). Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in Southern Brazil. Journal of Tropical Ecology, 23, 53-62. https://doi.org/10.1017/S0266467406003713

121.    Zhang, W., Yin, X., Feng, Z., Liu, X., Zhu, F., Zhu, H., & Yao, Q. (2024). Drought stress reduces arbuscular mycorrhizal colonization of Poncirus trifoliata L. roots and plant growth promotion via lipid metabolism. Frontier and Plant Science, 15, 1452202. https://doi.org/10.3389/fpls.2024.1452202

122.    Zhang, Q., Yang,W., Wang, M., Chen, J., Zhang, Z., Wei, Y., Chang, Q., & Gong, M. (2025). Transcriptome analysis reveals the molecular mechanisms for mycorrhiza- enhanced drought tolerance in maize by regulating the Ca²⁺ signalling pathway. Journal of Fungi, 11, 375. https://doi.org/10.3390/jof11050375

123.    Wang, S., Yi, J., Li, Z., Wu, J., Xu, Y., Xue, R., Wang, Y., Duan, L., Zhao, L., & Pi, E. (2026). Functional overview of plant genes essential for arbuscular mycorrhizal symbiosis. Genes, 17(6), 686. https://doi.org/10.3390/qenes17060686