Abstract
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.
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Abbreviations
- AM:
-
Arbuscular mycorrhiza
- AMF:
-
Arbuscular mycorrhizal fungi
- E :
-
Transpiration rate
- g s :
-
Stomatal conductance
- Pn:
-
Photosynthetic rate
References
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 55:108–111
Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10:51–54
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 11:43–47
Al-Yassin A (2004) Influence of salinity on citrus: a review paper. J Cent Eur Agric 5:263–272
Asghari HR (2008) Vesicular-arbuscular (VA) mycorrhizae improve salinity tolerance in pre-inoculation subterranean clover (Trifolium subterraneum) seedlings. Int J Plant Product 2:243–256
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 273:245–256
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 25:243–249
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 16:647–652
Berta G, Fusconi A, Trotta A (1993) VA mycorrhizal infection and the morphology and function of root systems. Environ Exp Bot 33:159–173
Carvalho LM, Correia PM, Martins-Loução MA (2004) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14:165–170
Cerda A, Nieves M, Guillen MG (1990) Salt tolerance of lemon trees as affected by rootstock. Irrig Sci 11:245–249
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560
Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448
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 63:147–157
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 104:583–590
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 18:317–329
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 12:185–190
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 14:307–312
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 54:753–760
Hartmond U, Schaesberg NV, Graham JH, Syvertsen JP (1987) Salinity and flooding stress effects on mycorrhizal and non-mycorrhizal citrus rootstock seedlings. Plant Soil 104:37–43
Hasegawa P, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
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 59:128–133
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 44:654–658
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 24:1027–1034
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 55:45–53
Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 15:371–379
Kapoor R, Sharma D, Bhatnagar AK (2008) Arbuscular mycorrhizae in micropropagation systems and their potential applications. Sci Hortic 116:227–239
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 85:225–232
Levy Y, Syvertsen J (2004) Irrigation water quality and salinity effects in citrus trees. Hortic Rev 30:37–82
Locatelli LM, Vitovski CA, Lovato PE (2002) Root architecture of apple rootstocks inoculated with arbuscular mycorrhizal fungi. Pesq Agropec Bras 37:1239–1245
Lutts S, Kinet JM, Bouharmont J (1999) Improvement of rice callus regeneration in the presence of NaCl. Plant Cell Tissue Organ Cult 57:3–11
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 26:125–137
Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043
Murkute AA, Sharma S, Singh SK (2006) Studies on salt stress tolerance of citrus rootstock genotypes with arbuscular mycorrhizal fungi. Hortic Sci 33:70–76
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 15:347–357
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 75:255–259
Padilla IMG, Encina CL (2005) Changes in root morphology accompanying mycorrhizal alleviation of phosphorus deficiency in micropropagated Annona cherimola Mill. plants. Sci Hortic 106:360–369
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 95:9681–9686
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 55:158–161
Rabie GH (2005) Influence of arbuscular mycorrhizal fungi and kinetin on the response of mungbean plants to irrigation with seawater. Mycorrhiza 15:225–230
Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–222
Ruiz-Lozano JM, Azcón R, Gomez M (1996) Alleviation of salt stress by arbuscular mycorrhizal Glomus species in Lactuca sativa plants. Physiol Plant 98:767–772
Schroeder MS, Janos DP (2005) Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas, phosphorus fertilization, and intraspecific density. Mycorrhiza 15:203–216
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 18:287–296
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 289:369–383
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 51:87–98
Wu QS, Zou YN (2009) Adaptive responses of birch-leaved pear (Pyrus betulaefolia) seedlings to salinity stress. Not Bot Hort Agrobot Cluj 37:133–138
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 44:122–128
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):97–106
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 82:863–866
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 21:529–540
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The research was supported by a Doctoral Scientific Research Foundation (39210264) and an Undergraduate Research Program (091048923;02) from Yangtze University.
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Wu, QS., Zou, YN. & He, XH. Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plant 32, 297–304 (2010). https://doi.org/10.1007/s11738-009-0407-z
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DOI: https://doi.org/10.1007/s11738-009-0407-z