Acta Physiologiae Plantarum

, Volume 32, Issue 2, pp 297–304 | Cite as

Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress

  • Qiang-Sheng Wu
  • Ying-Ning Zou
  • Xin-Hua He
Original Paper


A pot study was conducted to determine the effects of arbuscular mycorrhizal (AM) fungi (Glomus mosseae and Paraglomus occultum) and salt (NaCl) stress on growth, photosynthesis, root morphology and ionic balance of citrus (Citrus tangerine Hort. ex Tanaka) seedlings. Eighty-five-day-old seedlings were exposed to 100 mM NaCl for 60 days to induce salt stress. Mycorrhizal colonization of citrus seedlings was not affected by salinity when associated with P. occultum, but significantly decreased when with G. mosseae. Compared with the non-mycorrhizal controls, mycorrhizal seedlings generally had greater plant height, stem diameter, shoot, root and total plant biomass, photosynthetic rate, transpiration rate and stomatal conductance under the 0 and 100 mM NaCl stresses. Root length, root projected area and root surface area were also higher in the mycorrhizal than in the non-mycorrhizal seedlings, but higher root volume in seedlings with G. mosseae. Leaf Na+ concentrations were significantly decreased, but leaf K+ and Mg2+ concentrations and the K+/Na+ ratio were increased when seedlings with both G. mosseae and P. occultum. Under the salt stress, Na+ concentrations were increased but K+ concentrations decreased in the mycorrhizal seedlings. Under the salt stress, Ca2+ concentrations were increased in the seedlings with P. occultum or without AM fungi (AMF), but decreased with G. mosseae. Ratios of both Ca2+/Na+ and Mg2+/Na+ were also increased in seedlings with G. mosseae under the non-salinity stress, while only the Mg2+/Na+ ratio was increased in seedlings with P. occultum under the salt stress. Our results suggested that salt tolerance of citrus seedlings could be enhanced by associated AMF with better plant growth, root morphology, photosynthesis and ionic balance.


Arbuscular mycorrhiza Citrus Ionic balance Photosynthesis Root morphology Salt stress 



Arbuscular mycorrhiza


Arbuscular mycorrhizal fungi


Transpiration rate


Stomatal conductance


Photosynthetic rate



The research was supported by a Doctoral Scientific Research Foundation (39210264) and an Undergraduate Research Program (091048923;02) from Yangtze University.


  1. Aguin O, Mansilla JP, Vilarino A, Sainz MJ (2004) Effects of mycorrhizal inoculation on root morphology and nursery production of three grapevine rootstocks. Am J Enol Vitic 55:108–111Google Scholar
  2. Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10:51–54CrossRefGoogle Scholar
  3. Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47CrossRefGoogle Scholar
  4. Al-Yassin A (2004) Influence of salinity on citrus: a review paper. J Cent Eur Agric 5:263–272Google Scholar
  5. Asghari HR (2008) Vesicular-arbuscular (VA) mycorrhizae improve salinity tolerance in pre-inoculation subterranean clover (Trifolium subterraneum) seedlings. Int J Plant Product 2:243–256Google Scholar
  6. Asghari HR, Marschner P, Smith SE, Smith FA (2005) Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant Soil 273:245–256CrossRefGoogle Scholar
  7. Ashraf MY, Akhtar K, Sarwar G, Ashraf M (2005) Role of the rooting system in salt tolerance potential of different guar accessions. Agron Sustain Dev 25:243–249CrossRefGoogle Scholar
  8. Azcón-Aguilar C, Padilla IMG, Encina CL, Azcón R, Barea MG (1996) Arbuscular mycorrhizal inoculation enhances plant growth and changes root system morphology in micropropagated Annona cherimola Mill. Agronomie 16:647–652CrossRefGoogle Scholar
  9. Berta G, Fusconi A, Trotta A (1993) VA mycorrhizal infection and the morphology and function of root systems. Environ Exp Bot 33:159–173CrossRefGoogle Scholar
  10. Carvalho LM, Correia PM, Martins-Loução MA (2004) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14:165–170CrossRefPubMedGoogle Scholar
  11. Cerda A, Nieves M, Guillen MG (1990) Salt tolerance of lemon trees as affected by rootstock. Irrig Sci 11:245–249CrossRefGoogle Scholar
  12. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560CrossRefPubMedGoogle Scholar
  13. Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448Google Scholar
  14. da Silva EC, Nogueira RJMC, de Araújo FP, de Melo NF, de Azevedo Neto AD (2008) Physiological responses to salt stress in young umbu plants. Environ Exp Bot 63:147–157CrossRefGoogle Scholar
  15. Duke ER, Johnson CR, Koch KE (1986) Accumulation of phosphorus, dry matter and betaine during NaCl stress of split-root citrus seedlings colonized with vesicular-arbuscular mycorrhizal fungi on zero, one or two halves. New Phytol 104:583–590CrossRefGoogle Scholar
  16. Echeverria M, Scambato AA, Sannazzaro AI, Maiale S, Ruiz OA, Menéndez AB (2008) Phenotypic plasticity with respect to salt stress response by Lotus glaber: the role of its AM fungal and rhizobial symbionts. Mycorrhiza 18:317–329CrossRefPubMedGoogle Scholar
  17. Feng G, Zhang FS, Li XL, Tian CY, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190CrossRefPubMedGoogle Scholar
  18. Giri B, Mukerji KG (2004) Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312CrossRefPubMedGoogle Scholar
  19. Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760CrossRefPubMedGoogle Scholar
  20. Hartmond U, Schaesberg NV, Graham JH, Syvertsen JP (1987) Salinity and flooding stress effects on mycorrhizal and non-mycorrhizal citrus rootstock seedlings. Plant Soil 104:37–43CrossRefGoogle Scholar
  21. Hasegawa P, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499CrossRefPubMedGoogle Scholar
  22. He ZQ, He CX, Zhang ZB, Zou ZR, Wang HS (2007) Changes in antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B Biointerfaces 59:128–133CrossRefPubMedGoogle Scholar
  23. Hirrel MC, Gerdemann JW (1980) Improved growth of onion and bell pepper in saline soils by two vesicular-arbuscular mycorrhizal fungi. Soil Sci Soc Am J 44:654–658Google Scholar
  24. Iglesias DJ, Levy Y, Gómez-Cadenas A, Tadeo FR, Primo-Millo E, Talon M (2004) Nitrate improves growth in salt-stressed citrus seedlings through effects on photosynthetic activity and chloride accumulation. Tree Physiol 24:1027–1034PubMedGoogle Scholar
  25. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53CrossRefPubMedGoogle Scholar
  26. Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 15:371–379CrossRefGoogle Scholar
  27. Kapoor R, Sharma D, Bhatnagar AK (2008) Arbuscular mycorrhizae in micropropagation systems and their potential applications. Sci Hortic 116:227–239CrossRefGoogle Scholar
  28. Khan M, Ungar I, Showalters A (2000) Effects of salinity on growth water relation and ion accumulation of the subtropical perennial halophyte, Atriplex griffithii var. stocksii. Ann Bot 85:225–232CrossRefGoogle Scholar
  29. Levy Y, Syvertsen J (2004) Irrigation water quality and salinity effects in citrus trees. Hortic Rev 30:37–82Google Scholar
  30. Locatelli LM, Vitovski CA, Lovato PE (2002) Root architecture of apple rootstocks inoculated with arbuscular mycorrhizal fungi. Pesq Agropec Bras 37:1239–1245Google Scholar
  31. Lutts S, Kinet JM, Bouharmont J (1999) Improvement of rice callus regeneration in the presence of NaCl. Plant Cell Tissue Organ Cult 57:3–11CrossRefGoogle Scholar
  32. Mohammad MJ, Malkawi HI, Shibli R (2003) Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. J Plant Nutr 26:125–137CrossRefGoogle Scholar
  33. Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043CrossRefPubMedGoogle Scholar
  34. Murkute AA, Sharma S, Singh SK (2006) Studies on salt stress tolerance of citrus rootstock genotypes with arbuscular mycorrhizal fungi. Hortic Sci 33:70–76Google Scholar
  35. Nandy P, Das S, Ghose M, Spooner-Hart R (2007) Effects of salinity on photosynthesis, leaf anatomy, ion accumulation and photosynthetic nitrogen use efficiency in five Indian mangroves. Wetlands Ecol Manage 15:347–357CrossRefGoogle Scholar
  36. Ojala JC, Jarrell WM, Menge JA, Johnson ELV (1983) Influence of mycorrhizal fungi on the mineral nutrition and yield of onion in saline soil. Agron J 75:255–259CrossRefGoogle Scholar
  37. Padilla IMG, Encina CL (2005) Changes in root morphology accompanying mycorrhizal alleviation of phosphorus deficiency in micropropagated Annona cherimola Mill. plants. Sci Hortic 106:360–369CrossRefGoogle Scholar
  38. Pardo JM, Reddy MP, Yang S, Maggio A, Huh GH, Matsumoto T, Coca MA, Paino-D’Urzo M, Koiwa H, Yun DJ, Watad AA, Bressan RA, Hasegawa PM (1998) Stress signaling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc Natl Acad Sci USA 95:9681–9686CrossRefPubMedGoogle Scholar
  39. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  40. Rabie GH (2005) Influence of arbuscular mycorrhizal fungi and kinetin on the response of mungbean plants to irrigation with seawater. Mycorrhiza 15:225–230CrossRefPubMedGoogle Scholar
  41. Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–222Google Scholar
  42. Ruiz-Lozano JM, Azcón R, Gomez M (1996) Alleviation of salt stress by arbuscular mycorrhizal Glomus species in Lactuca sativa plants. Physiol Plant 98:767–772CrossRefGoogle Scholar
  43. Schroeder MS, Janos DP (2005) Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas, phosphorus fertilization, and intraspecific density. Mycorrhiza 15:203–216CrossRefPubMedGoogle Scholar
  44. Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296CrossRefPubMedGoogle Scholar
  45. Teakle NL, Real D, Colmer TD (2006) Growth and ion relations in response to combined salinity and waterlogging in the perennial forage legumes Lotus corniculatus and Lotus tenuis. Plant Soil 289:369–383CrossRefGoogle Scholar
  46. van Hoorn JW, Katerji N, Hamdy A, Mastrorilli M (2001) Effect of salinity on yield and nitrogen uptake of four grain legumes and on biological nitrogen contribution from the soil. Agric Water Manage 51:87–98CrossRefGoogle Scholar
  47. Wu QS, Zou YN (2009) Adaptive responses of birch-leaved pear (Pyrus betulaefolia) seedlings to salinity stress. Not Bot Hort Agrobot Cluj 37:133–138Google Scholar
  48. Wu QS, Xia RX, Zou YN (2008) Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. Eur J Soil Biol 44:122–128CrossRefGoogle Scholar
  49. Yi LP, Ma J, Li Y (2007) Impact of salt stress on the features and activities of root system for three desert halophyte species in their seedlings stage. Sci China Ser D Earth Sci 50(Suppl I):97–106CrossRefGoogle Scholar
  50. Zai XM, Qin P, Wan SW, Zhao FG, Wang G, Yan DL, Zhou J (2007) Effects of arbuscular mycorrhizal fungi on the rooting and growth of beach plum (Prunus maritima) cuttings. J Hortic Sci Biotechnol 82:863–866Google Scholar
  51. Zangaro W, Nishidate FR, Camargo FRS, Romagnoli GG, Vandressen J (2005) Relationships among arbuscular mycorrhizas, root morphology and seedlings growth of tropical native woody species in southern Brazil. J Trop Ecol 21:529–540CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2009

Authors and Affiliations

  1. 1.College of Horticulture and GardeningYangtze UniversityJingzhouPeople’s Republic of China
  2. 2.School of Plant Biology (M084)University of Western AustraliaCrawleyAustralia

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