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Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress

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Abstract

A pot experiment was conducted to examine the effect of the arbuscular mycorrhizal (AM) fungus, Glomus mosseae, on plant biomass and organic solute accumulation in maize leaves. Maize plants were grown in sand and soil mixture with three NaCl levels (0, 0.5, and 1.0 g kg−1 dry substrate) for 55 days, after 15 days of establishment under non-saline conditions. At all salinity levels, mycorrhizal plants had higher biomass and higher accumulation of organic solutes in leaves, which were dominated by soluble sugars, reducing sugars, soluble protein, and organic acids in both mycorrhizal and non-mycorrhizal plants. The relative abundance of free amino acids and proline in total organic solutes was lower in mycorrhizal than in non-mycorrhizal plants, while that of reducing sugars was higher. In addition, the AM symbiosis raised the concentrations of soluble sugars, reducing sugars, soluble protein, total organic acids, oxalic acid, fumaric acid, acetic acid, malic acid, and citric acid and decreased the concentrations of total free amino acids, proline, formic acid, and succinic acid in maize leaves. In mycorrhizal plants, the dominant organic acid was oxalic acid, while in non-mycorrhizal plants, the dominant organic acid was succinic acid. All the results presented here indicate that the accumulation of organic solutes in leaves is a specific physiological response of maize plants to the AM symbiosis, which could mitigate the negative impact of soil salinity on plant productivity.

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References

  • Abd-El Baki BGK, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase in Zea mays L. under salinity. Plant Cell Environ 23:515–521. doi:10.1046/j.1365-3040.2000.00568.x

    Article  CAS  Google Scholar 

  • Abdel-Fattah GM (2001) Measurement of the viability of arbuscular-mycorrhizal fungi using three different stains; relation to growth and metabolic activities of soybean plants. Microbiol Res 156:359–367. doi:10.1078/0944-5013-00121

    Article  CAS  PubMed  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258. doi:10.1126/science.285.5431.1256

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s11104-004-7942-6

    Article  CAS  Google Scholar 

  • Bao SD (2000) Soil agricultural chemistry analysis, 3rd edn. Agriculture, Beijing

    Google Scholar 

  • Berta G, Fusconi A, Trotta A, Scannerini S (1990) Morphogenetic modifications induced by the mycorrhizal fungus Glomus strain E3 in the root system of Allium porrum L. New Phytol 114:207–215. doi:10.1111/j.1469-8137.1990.tb00392.x

    Article  Google Scholar 

  • Cantrell IC, Linderman RG (2001) Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant Soil 233:269–281. doi:10.1023/A:1010564013601

    Article  CAS  Google Scholar 

  • Chollet R, Vidal J, O'Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47:273–298. doi:1040-2519/96/0601-0273

    Article  CAS  PubMed  Google Scholar 

  • Dinkelaker B, Hengeler G, Neumann G, Eltrop L, Marschner H (1997) Root exudates and mobilization of nutrients. In: Rennenberg H, Eschrich W, Ziegler H (eds) Trees-contributions to modern tree physiology. Backhuys, Leiden, pp 441–452

    Google Scholar 

  • 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. doi:10.1111/j.1469-8137.1986.tb00658.x

    Article  CAS  Google Scholar 

  • Feng G, Li X, Zhang F, Li S (2000) Effect of AM fungi on water and nutrition status of corn plants under salt stress. Chin J Appl Ecol 11:595–598. doi: CNKI:SUN:YYSB.0.2000-04-025

    CAS  Google Scholar 

  • 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. doi:10.1007/s00572-002-0170-0

    Article  CAS  PubMed  Google Scholar 

  • Francoise F, Daniel LR, John G (1991) Effects of salt stress on amino acid, organic acid and carbohydrate composition of root, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236. doi: 0032-0889/91/96/1228/09

    Article  Google Scholar 

  • Gao JF (2000) Techniques of plant physiology. World Publishing Corporation, Xi'an

    Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x

    Article  Google Scholar 

  • 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. doi:10.1007/s00572-003-0274-1

    Article  PubMed  Google Scholar 

  • 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. doi:10.1007/s00248-007-9239-9

    Article  CAS  PubMed  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190. doi:10.1146/annurev.arplant.59.032607.092911

    Article  CAS  Google Scholar 

  • Guo FQ, Zhou JM, Tang ZC (1999) Differences in the accumulation of some organic solutes and gene expression in leaves between the salt tolerant mutant and the wild type of wheat under NaCl stress. Acta Photophysiol Sin 25:263–268. cnki:ISSN:0257-4829.0.1999-03-009

    CAS  Google Scholar 

  • Guo LQ, Shi DC, Wang DL (2010) The key physiological response to alkali stress by the alkali-resistant halophyte Puccinellia tenuiflora is the accumulation of large quantities of organic acids and into the rhyzosphere. J Agron Crop Sci 196:123–135. doi:10.1111/j.1439-037X.2009.00397.x

    Article  CAS  Google Scholar 

  • Hajlaoui H, Ayeb NE, Garrec JP, Denden M (2010) Differential effects of salt stress on osmotic adjustment and solutes allocation on the basis of root and leaf tissue senescence of two silage maize (Zea mays L.) varieties. Ind Crops Prod 31:122–130. doi:10.1016/j.indcrop.2009.09.007

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Bio 51:463–499. doi:10.1146/annurev.arplant.51.1.463

    Article  CAS  Google Scholar 

  • Hatzig S, Kumar A, Neubert A, Schubert S (2010) PEP-carboxylase activity: a comparison of its role in a C4 and a C3 species under salt stress. J Agron Crop Sci 196:185–192. doi:10.1111/j.1439-037X.2009.00403.x

    Article  CAS  Google Scholar 

  • Hoffland E, Boogaard R, Nelemans J, Findenegg G (1992) Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol 122:675–680. doi:10.1111/j.1469-8137.1992.tb00096.x

    Article  CAS  Google Scholar 

  • Hoque MA, Okuma E, Banu Mst NA, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J Plant Physiol 164:553–561. doi:10.1016/j.jplph.2006.03.010

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s00248-007-9249-7

    Article  PubMed  Google Scholar 

  • Khaled LB, Gõmez AM, Ouarraqi EM, Oihabi A (2003) Physiological and biochemical responses to salt stress of mycorrhized and/or nodulated clover seedlings (Trifolium alexandrinum L.). Agronomie 23:571–580. doi:10.1051/agro:2003037

    Article  Google Scholar 

  • Li XL, Feng G (2001) Ecology and physiology of arbuscular mycorrhizae. Huawen, Beijing

    Google Scholar 

  • López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160:1–13. doi: S0168-9452(00)00347-2

    Article  PubMed  Google Scholar 

  • Neocleous D, Vasilakakis M (2007) Effects of NaCl stress on red raspberry (Rubus idaeus L. ‘Autumn Bliss’). Sci Hortic 112:282–289. doi:10.1016/j.scienta.2006.12.025

    Article  CAS  Google Scholar 

  • Neto ADA, Prisco JT, Gomes-Filho E (2009) Changes in soluble amino-N, soluble proteins and free amino acids in leaves and roots of salt-stressed maize genotypes. J Plant Interact 4:137–144. doi:10.1016/j.indcrop.2009.09.007

    Article  Google Scholar 

  • Ober ES, Sharp RE (1994) Proline accumulation in maize (Zea mays L.) primary roots at low water potentials (I. Requirement for increased levels of abscisic acid). Plant Physiol 105:981–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ Exp Bot 57:177–186. doi:10.1016/j.envexpbot.2005.05.011

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rabie GH (2005) Influence of arbuscular mycorrhizal fungi and kinetin on the response of mungbean plants to irrigation with seawater. Mycorrhiza 15:225–230. doi:10.1007/s00572-004-0345-y

    Article  CAS  PubMed  Google Scholar 

  • 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. http://www.academicjournals.org/AJB

    CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478. doi:10.1111/j.1399-3054.1995.tb00865.x

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Gómez M (1996) Alleviation of salt stress by arbuscular-mycorrhizal Glomus species in Lactuca sativa plants. Physiol Plant 98:767–772. doi:10.1111/j.1399-3054.1996.tb06683.x

    Article  CAS  Google Scholar 

  • Sannazzaro AI, Ruiz OA, Albertó EO, Menéndez AB (2006) Alleviation of salt stress in Lotus glaber by Glomus intraradices. Pant soil 285:279–287. doi:10.1007/s11104-006-9015-5

    CAS  Google Scholar 

  • Sengupta A, Chaudhuri S (1990) Vesicular-arbuscular mycorrhiza (VAM) in pioneer saline marsh plants of the Ganges River Delta in west Bengal (India). Plant Soil 122:111–113. doi:10.1007/BF02851917

    Article  Google Scholar 

  • Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151. doi:10.1016/j.jplph.2006.06.016

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s00572-008-0180-7

    Article  CAS  PubMed  Google Scholar 

  • Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2009) Influence of arbuscular mycorrhizae on root system of maize plants under salt stress. Can J Microbiol 55:879–886. doi:10.1139/W09-031

    Article  CAS  PubMed  Google Scholar 

  • Shi YL (1991) 1: 1000000 map of Chinese soil resource . Chinese People's University, Beijing

  • Szalai G, Janda T (2009) Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J Agric Crop Sci 195:165–171. doi:10.1111/j.1439-037X.2008.00352.x

    Article  CAS  Google Scholar 

  • Usha K, Saxena A, Singh B (2004) Rhizosphere dynamics influenced by arbuscular mycorrhizal fungus (Glomus deserticola) and related changes in leaf nutrient status and yield of Kinnow mandarin {King (Citrus nobilis) × Willow Leaf (Citrus deliciosa)}. Aust J Agric Res 55:571–576. doi:10.1071/AR03036

    Article  Google Scholar 

  • Wu QS, Zou YN, He XH (2009) 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. doi:10.1007/s11738-009-0407-z

    Article  Google Scholar 

  • Yang CW, Chong JN, Kim CM, Li CY, Shi DC, Wang DL (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294:263–276. doi:10.1007/s11104-007-9251-3

    Article  CAS  Google Scholar 

  • Yano-Melo AM, Saggin OJ, Maia LC (2003) Tolerance of mycorrhized banana (Musa sp. cv. Pacovan) plantlets to saline stress. Agric Ecosyst Environ 95:343–348. doi:10.1016/S0167-8809(02)00044-0

    Article  Google Scholar 

  • Zandavalli RB, Dillenburg LR, de Souza PVD (2004) Growth responses of Araucaria angustifolia (Araucariaceae) to inoculation with the mycorrhizal fungus Glomus clarum. Appl Soil Ecol 25:245–255. doi:10.1016/j.apsoil.2003.09.009

    Article  Google Scholar 

  • Zhang YF, Feng G, Li XL (2003) The effect of arbuscular mycorrhizal fungi on the components and concentrations of organic acids in the exudates of mycorrhizal red clover. Acta Ecol Sin 23:30–37. cnki:ISSN:1000-0933.0.2003-01-004

    Google Scholar 

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Acknowledgments

The study was supported by the Key Project of National Natural Science Foundation of China (30630054), the Program for Changjiang Scholars and Innovative Research Team in University of China (IRT0748), and the Ph.D. Program Foundation of Ministry of Education of China (20100204110033). We are indebted to Chantal Hamel, Semiarid Prairie Agricultural Research Centre, Agriculture and Agri-Food Canada, for editing this article.

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Correspondence to Ming Tang.

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Sheng, M., Tang, M., Zhang, F. et al. Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21, 423–430 (2011). https://doi.org/10.1007/s00572-010-0353-z

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