Photosynthesis Research

, Volume 139, Issue 1–3, pp 227–238 | Cite as

Arbuscular Mycorrhizal fungi (AMF) protects photosynthetic apparatus of wheat under drought stress

  • Sonal Mathur
  • Rupal Singh Tomar
  • Anjana JajooEmail author
Original Article


Drought stress (DS) is amongst one of the abiotic factors affecting plant growth by limiting productivity of crops by inhibiting photosynthesis. Damage due to DS and its protection by Arbuscular Mycorrhizal fungi (AMF) was studied on photosynthetic apparatus of wheat (Triticum aestivum) plants in pot experiments. DS was maintained by limiting irrigation to the drought stressed (DS) and AMF + DS plants. Relative Water content (RWC) was measured for leaf as well as soil to ensure drought conditions. DS plants had minimum RWC for both leaf and soil. AMF plants showed increased RWC both for leaf and soil indicating that AMF hyphae penetrated deep into the soil and provided moisture to the plants. In Chl a fluorescence induction curve (OJIP), a declined J–I and I–P phase was observed in DS plants. Efficacy of primary photochemistry declined in DS plants as result of DS, while AMF plants showed maximum photochemistry. DS leads to declined quantum efficiency of PSI and PSII in DS plants while it was restored in AMF + DS plants. Electron transport (ETRI and ETRII) decreased while quantum yield of non-photochemical quenching Y(NPQ) increased as a result of drought stress. CEF around PSI increased in DS-stressed plants. Efficient PSI complexes decreased in DS plants while in case of AMF plants PSI complexes were able to perform PSI photochemistry significantly. Thus, it is concluded that drought stress-induced damage to the structure and function of PSII and PSI was alleviated by AMF colonization.


Arbuscular Mycorrhizal fungi (AMF) Drought Wheat Photosynthesis Photosystem II Photosystem I 



Arbuscular Mycorrhiza fungi


Drought stress


Linear electron flow


Maximal change in P700 signal


Photosystem I


Photosystem II


Relative water content


Quantum yield of PSI


Quantum yield of PSII


Quantum yield of non-photochemical energy dissipation due to acceptor-side limitation


Quantum yield of non-photochemical energy dissipation due to donor-side limitation


Yield of non-regulated energy dissipation.


Yield of regulated energy dissipation



SM acknowledges University Grants Commission, (UGC), India for awarding Post Doctoral Fellowship for Women (PDFWM-2014-15-GEMAD-23945). We would like to acknowledge Dr. S.V. Sai Prasad (Director, ICAR-IARI, Regional station, Indore) for providing wheat seeds and Dr. M.P. Sharma (PI, ICAR-IISR, Indore) for his kind support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdel-Salam E, Alatar A, El-Sheikh MA (2017) Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi J Biol Sci. Google Scholar
  2. Augé RM (2001) Water relations, drought and vesicular arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  3. Augé RM, Toler HD, Moore JL, Cho K, Saxton AM (2007) Comparing contributions of soil versus root colonization to variations in stomatal behavior and soil drying in mycorrhizal Sorghum bicolor and Cucurbita pepo. J Plant Physiol 164:1289–1299CrossRefGoogle Scholar
  4. Biermann BJ, Lindermann RQ (1981) Quantifying vesicular-arbuscular mycorrhizae: proposed method towards standardization. New Phytol 87:63–67CrossRefGoogle Scholar
  5. Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji HM, Allakhverdiev SI (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth Res 125:151–166CrossRefGoogle Scholar
  6. Ceppi MG, Oukarroum A, Cicek N, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288CrossRefGoogle Scholar
  7. 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 8:931CrossRefGoogle Scholar
  8. Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus-the protective role of polyamines. Biochim Biophys Acta 1767:272–280CrossRefGoogle Scholar
  9. Eichelmann H, Laisk A (2000) Cooperation of photosystems II and I in leaves as analysed by simultaneous measurements of chlorophyll fluorescence and transmittance at 800 nm. Plant Cell Physiol 41:138–147CrossRefGoogle Scholar
  10. Fernández-Lizarazo JC, Moreno-Fonseca LP (2016) Mechanisms for tolerance to water-deficit stress in plants inoculated with arbuscular mycorrhizal fungi. A review. Agrono Colomb 34:179–189CrossRefGoogle Scholar
  11. Haneef I, Faizan S, Perveen R, Kausar S (2013) Role of arbuscular mycorrhizal fungi on growth and photosynthetic pigments in (Coriandrum sativum L.) grown under cadmium stress. World J Agric Sci 9:245–250Google Scholar
  12. Huan L, Xie X, Zheng Z, Sun F, Wu S, Li M, Gao S, Gu W, Wang G (2014) Positive correlation between PSI response and oxidative pentose phosphate pathway activity during salt stress in an intertidal macroalga. Plant Cell Physiol 55:1395–1403CrossRefGoogle Scholar
  13. Huang W, Zhang SB, Cao KF (2010) Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. Plant Cell Physiol 51:1922–1928CrossRefGoogle Scholar
  14. 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 339:391–399CrossRefGoogle Scholar
  15. Huang W, Yang YJ, Hu H, Zhang SB (2015) Different roles of cyclic electron flow around photosystem I under sub-saturating and saturating light intensities in tobacco leaves. Front Plant Sci 6:923Google Scholar
  16. 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 7:42335CrossRefGoogle Scholar
  17. Ivanov AG, Hendrickson L, Krol M, Selstam E, Oquist G, Hurry V, Huner NPA (2006) Digalactosyl-Diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to Photosystem I acceptor-side limitations. Plant Cell Physiol 47:1146–1157CrossRefGoogle Scholar
  18. Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska IA, Cetner MD, Allakhverdiev SI, Goltsev V (2014) Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol Biochem 81:16–25CrossRefGoogle Scholar
  19. Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Lukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102CrossRefGoogle Scholar
  20. Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, Losciale P, Mishra VK, Misra AN, Nebauer SG, Pancaldi S, Penella C, Pollastrini M, Suresh MK, Tambussi E, Yanniccari M, Zivcak M, Cetner MD, Samborska IA, Stirbet A, Olsovska K, Kunderlikova K, Shelonzek H, Rusinowski S, Baba W (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:13–66CrossRefGoogle Scholar
  21. Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem-I quantum yield via P700+ absorbance changes at 830 nm. Planta 192:261–268CrossRefGoogle Scholar
  22. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488CrossRefGoogle Scholar
  23. Kramer DM, Avenson TJ, Kanazawa A, Cruz JA, Ivanov B, Edwards GE (2004) The relationship between photosynthetic electron transfer and its regulation. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 251–278CrossRefGoogle Scholar
  24. Maboko MM (2013) Effect of arbuscular mycorrhiza and temperature control on plant growth, yield, and mineral content of tomato plants grown hydroponically. HortScience 48:1470–1477CrossRefGoogle Scholar
  25. Mathur S, Jajoo A, Mehta P, Bharti S (2011) Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). Plant Biol 13:1–6CrossRefGoogle Scholar
  26. Mathur S, Sharma MP, Jajoo A (2018) Improved photosynthetic efficacy of maize (Zea mays) plants with Arbuscular mycorrhizal fungi (AMF) under high temperature stress. J Photochem Photobiol B 180:149–154CrossRefGoogle Scholar
  27. Miyake C, Miyata M, Shinzaki Y, Tomizawa K (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of chl fluorescence. Plant Cell Physiol 46:629–737CrossRefGoogle Scholar
  28. 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 7:644CrossRefGoogle Scholar
  29. Pebriansyah A, Karti PDMH, Permana AT (2012) Effect of drought stress and addition of Arbuscula mycorrhizal fungi (AMF) on growth and productivity of tropical grasses (Chloris gayana, Paspalum dilatatum, and Paspalum notatum). Pastura 2:41–48Google Scholar
  30. Percival GC, Hendersons A (2003) An assessment of the freezing tolerance of urban trees using chlorophyll fluorescence. J Hortic Sci Biotechnol 78:254–260CrossRefGoogle Scholar
  31. Pfündel E, Klughammer C, Ulrich S (2008) Monitoring the effects of reduced PS II antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system. PAM Appl Notes 1:21–24Google Scholar
  32. Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750CrossRefGoogle Scholar
  33. Rapparini F, Llusia J, Pen J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122CrossRefGoogle Scholar
  34. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317CrossRefGoogle Scholar
  35. Savitch LV, Ivanov AG, Gudynaite-Savitch L, Huner NP, Simmonds J (2011) Cold stress effects on PSI photochemistry in Zea mays: differential increase of FQR-dependent cyclic electron flow and functional implications. Plant Cell Physiol 52:1042–1054CrossRefGoogle Scholar
  36. Sharma MP, Singh S, Sharma SK, Ramesh A, Bhatia VS (2016) Co-inoculation of resident AM Fungi and soybean rhizobia enhanced nodulation, yield, soil biological parameters and saved Fertilizer inputs in vertisols under microcosm and field conditions. Soybean Res 14:39–53Google Scholar
  37. Shukla N, Awasthi RP, Rawat L, Kumar J (2012) Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol Biochem 54:78–88CrossRefGoogle Scholar
  38. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  39. Teskey R, Wertin T, Bauweraerts I, Ameye M, McGuire MA, Steppe K (2015) Responses of tree species to heat waves and extreme heat events. Plant Cell Environ 38:1699–1712CrossRefGoogle Scholar
  40. Tomar RS, Jajoo A (2015) Photomodified fluoranthene exerts more harmful effects as compared to intact fluoranthene by inhibiting growth and photosynthetic processes. Ecotoxicol Environ Saf 122:31–36CrossRefGoogle Scholar
  41. Tomar RS, Jajoo A (2017) PSI becomes more tolerant to fluoranthene through the initiation of cyclic electron flow. Funct Plant Biol 44:978–984CrossRefGoogle Scholar
  42. Tu W, Li Y, Liu W, Wu L, Xie X, Zhang Y, Wilhelm C, Yang C (2016) Spring ephemerals adapt to extremely high light conditions via an unusual stabilization of Photosystem II. Front Plant Sci 6:1189CrossRefGoogle Scholar
  43. Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366CrossRefGoogle Scholar
  44. Wang P, Liu JH, Xia RX, Wu QS, Wang MY, Dong T (2011) Arbuscular mycorrhizal development, glomalin-related soil protein (GRSP) content, andrhizospheric phosphatase activitiy in citrus orchards under different types of soil management. J Plant Nutr Soil Sci 174:65–72CrossRefGoogle Scholar
  45. Wężowicz K, Rozpądek P, Turnau K (2017) Interactions of arbuscular mycorrhizal and endophytic fungi improve seedling survival and growth in post-mining waste. Mycorrhiza 27:499–511CrossRefGoogle Scholar
  46. Wu QS, Levy Y, Zou YN (2009) Arbuscular mycorrhizae and water relations in citrus. In: Tennant P, Benkeblia N (eds) Citrus II. Tree and forstry science biotechnology 3(Special Issue):105–112Google Scholar
  47. Wu QS, Srivastava AK, Zou YN (2013) AMF- induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87CrossRefGoogle Scholar
  48. Yang Y, Tang M, Sulpice R, Chen H, Tian S, Ban Y (2014) Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. J Plant Growth Regul 33:612–625CrossRefGoogle Scholar
  49. Zhu J, Tremblay N, Liang Y (2012a) Comparing SPAD and at LEAF values for chlorophyll assessment in crop species. Can J Soil Sci 92:645 – 648CrossRefGoogle Scholar
  50. Zhu XC, Song FB, Liu SQ, Liu TD, Zhou X (2012b) Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ 58:186–191CrossRefGoogle Scholar
  51. Zhu XQ, Wang CY, Chen H, Tang M (2014) Effects of arbuscular mycorrhizal fungi on photosynthesis, carbon content, and calorific value of black locust seedlings. Photosynthetica 52:247–252CrossRefGoogle Scholar
  52. Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546CrossRefGoogle Scholar
  53. Zivcak M, Kalaji HM, Shao HB, Olsovska K, Brestic M (2014a) Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress. J Photochem Photobiol B 137:107–115CrossRefGoogle Scholar
  54. Zivcak M, Olsovska K, Slamka P, Galambosova J, Rataj V, Shao HB, Brestic M (2014b) Application of chlorophyll fluorescence performance indices to assess the wheat photosynthetic functions influencedby nitrogen deficiency. Plant Soil Environ 60:210–215CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Sonal Mathur
    • 1
  • Rupal Singh Tomar
    • 1
  • Anjana Jajoo
    • 1
    Email author
  1. 1.School of Life ScienceDevi Ahilya UniversityIndoreIndia

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