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Arbuscular mycorrhizal fungi enhanced the growth, photosynthesis, and calorific value of black locust under salt stress

  • Original Paper
  • Published:
Photosynthetica

Abstract

Saline soils spread wildly in the world, therefore it is important to develop salt-tolerant crops. We carried out a pot study in order to determine effects of arbuscular mycorrhizal fungi (AMF) (Rhizophagus irregularis and Glomus versiforme) in black locust seedlings under salt (NaCl) stress. The results showed that AMF enhanced in seedlings their growth, photosynthetic ability, carbon content, and calorific value. Under salt stress, the biomass of the seedlings with R. irregularis or G. versiforme were greater by 151 and 100%, respectively, while a leaf area increased by 197 and 151%, respectively. The seedlings colonized by R. irregularis exhibited a higher chlorophyll content, net photosynthetic rate, intercellular CO2 concentration, stomatal conductance, and transpiration rate than that of the nonmycorrhizal seedlings or those colonized by G. versiforme. Both R. irregularis and G. versiforme significantly enhanced a carbon content, calorific value, carbon, and energy accumulations of black locust under conditions of 0 or 1.5 g(NaCl) kg–1(growth substrate). Our results suggested that AMF alleviated salt stress and improved the growth of black locust.

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Abbreviations

AMF:

arbuscular mycorrhizal fungi

CE:

carboxylation efficiency

Chl:

chlorophyll

C i :

intercellular CO2 concentration

E :

transpiration rate

g s :

stomatal conductance

LA:

leaf area

LDM:

leaf dry mass

LSA:

leaf special area

NM:

nonmycorrhizal

NS:

not salt-stressed

P N :

net photosynthetic rate

S:

salt stress

WUEi :

intrinsic water-use efficiency

References

  • Arafat A.H.A.L., He C.X.: Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. — Sci. Hortic.-Amsterdam 127: 228–233, 2011.

    Article  Google Scholar 

  • Balat M.: Bio-oil production from pyrolysis of black locust (Robinia pseudoacacia) wood. — Energ. Explor. Exploit. 28: 173–186, 2010.

    Article  CAS  Google Scholar 

  • Bao S.D.: [Soil and agricultural chemistry analysis.] — In: Bao S.D. (ed.): [Soil and Agricultural Chemistry Analysis.] 3rd ed. Pp. 14–114, China Agricult. Press, Beijing 2000. [In Chinese]

    Google Scholar 

  • Barrett R.P., Mebrahtu T., Hanover J.W.: Black locust: a multipurpose tree species for temperate climates. — In: Janick J., Simon J.E. (ed.): Advances in New Crops. Pp. 278–283. Timber Press, Portland 1990.

    Google Scholar 

  • Bongarten B.C., Huber D.A., Apsley D.K.: Environmental and genetic influences on short rotation biomass production of black locust (Robinia pseudoacacia L.) in the Geogia Piedmont. — Forest Ecol. Manage. 55: 315–331, 1992.

    Article  Google Scholar 

  • Bruce R.J., West C.A.: Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. — Plant Physiol. 91: 889–897, 1989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carpenter S.B., Eigel R.A.: Reclaiming southern Appalachian surface mines with black locust fuel plantations. — In: Carpenter S.B. (ed.): Symposium on Surface Mining Hydrology, Sedimentology, and Reclamation. Pp. 221–227. University of Kentucky, Lexington 1979.

    Google Scholar 

  • Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. — Ann. Bot.-London 103: 551–560, 2009.

    Article  CAS  Google Scholar 

  • Demirbas A.: Potential applications of renewable energy sources, biomass combustion problems in boiler power systems and combustion related environmental issues. — Prog. Energ. Combust. 31: 171–192, 2005.

    Article  CAS  Google Scholar 

  • Estrada B., Aroca R., Maathuis F.J.M. et al.: Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. — Plant Cell Environ. 36: 1771–1782, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Evelin H., Giri B., Kapoor R.: Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. — Mycorrhiza 23: 71–86, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Evelin H., Kapoor R.: Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum-graecum plants. — Mycorrhiza 24: 197–208, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Evelin H., Kapoor R., Giri B.: Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. — Ann. Bot.-London 104: 1263–1280, 2009.

    Article  CAS  Google Scholar 

  • Fang S.Z., Zhai X.C., Wan J., Tang L.Z.: Clonal variation in growth, chemistry and calorific value of new poplar hybrids at nursery stage. — Biomass Bioenerg. 54: 303–311, 2013.

    Article  CAS  Google Scholar 

  • Gao J.F.: [Leaf area measurement method.] — In: Gao J.F. (ed.): [Experimental Guidance for Plant Physiology.] Pp. 88. High Educ. Press, Beijing 2006. [In Chinese]

    Google Scholar 

  • Gasol C.M., Brun F., Mosso A. et al.: Economic assessment and comparison of acacia energy crop with annual traditional crops in Southern Europe. — Energ. Policy 38: 592–597, 2010.

    Article  Google Scholar 

  • Geyer W.A., Walawender W.P.: Biomass properties and gasification behavior of young black locust. — Wood Fiber Sci. 26: 354–359, 1994.

    CAS  Google Scholar 

  • González-García S., Gasol C.M., Moreira M.T. et al.: Environmental assessment of black locust (Robinia pseudoacacia L.)-based ethanol as potential transport fuel. — Int. J. Life Cycle Assess. 16: 465–477, 2011.

    Article  Google Scholar 

  • González-García S., Moreira M.T., Feijoo G., Murphy R.J.: Comparative life cycle assessment of ethanol production from fast-growing wood crops (black locust, eucalyptus and poplar). — Biomass Bioenerg. 39: 378–388, 2012.

    Article  Google Scholar 

  • Grünewald H., Brandt B.K.V., Schneider B.U. et al.: Agroforestry systems for the production of woody biomass for energy transformation purposes. — Ecol. Eng. 29: 319–328, 2007.

    Article  Google Scholar 

  • Grünewald H., Böhm C., Quinkenstein A. et al.: Robinia pseudoacacia L.: a lesser known tree species for biomass production. — Bioenerg. Res. 2: 123–133, 2009.

    Article  Google Scholar 

  • Hajiboland R., Aliasgharzadeh N., Laiegh S.F., Poschenrieder C.: Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. — Plant Soil 331: 313–327, 2010.

    Article  CAS  Google Scholar 

  • Hameed A., Dilfuza E., Abd-Allah E.F. et al.: Salinity stress and arbuscular mycorrhizal symbiosis in plants. — In: Miransari M. (ed.): Use of Microbes for the Alleviation of Soil Stresses, Vol. 1. Pp. 139–159. Springer, New York 2014.

    Chapter  Google Scholar 

  • Huang C.Y. (ed.): [Soil Science.] Pp. 267–300. China Agricult. Press, Beijing 2000. [In Chinese]

    Google Scholar 

  • Jongen M., Fay P., Jones M.B.: Effects of elevated carbon dioxide and arbuscular mycorrhizal infection on Trifolium repens. — New Phytol. 132: 413–423, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Kaschuk G., Kuyper T.W., Leffelaar P.A. et al.: Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? — Soil Biol. Biochem. 41: 1233–1244, 2009.

    Article  CAS  Google Scholar 

  • Krüger M., Krüger C., Walker C. et al.: Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. — New Phytol. 193: 970–984, 2012.

    Article  PubMed  Google Scholar 

  • Kumar R., Pandey K.K., Chandrashekar N., Mohan S.: Study of age and height wise variability on calorific value and other fuel properties of Eucalyptus hybrid, Acacia auriculaeformis and Casuarina equisetifolia. — Biomass Bioenerg. 35: 1339–1344, 2011.

    Article  CAS  Google Scholar 

  • Lamlom S.H., Savidge R.A.: A reassessment of carbon content in wood: variation within and between 41 North American species. — Biomass Bioenerg. 25: 381–388, 2003.

    Article  CAS  Google Scholar 

  • Luo Z.B., Polle A.: Wood composition and energy content in a poplar short rotation plantation on fertilized agricultural land in a future CO2 atmosphere. — Glob. Change Biol. 15: 38–47, 2009.

    Article  Google Scholar 

  • Peng J., Li Y., Shi P. et al.: The differential behavior of arbuscular mycorrhizal fungi in interaction with Astragalus sinicus L. under salt stress. — Mycorrhiza 21: 27–33, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Phillips J.M., Hayman D.S.: Improved procedure for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. — T. Brit. Mycol. Soc. 55: 158–161, 1970.

    Article  Google Scholar 

  • Porcel R., Aroca A., Ruiz-Lozano J.M.: Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. — Agron. Sustain. Dev. 32: 181–200, 2012.

    Article  CAS  Google Scholar 

  • Prakash C.B., Murray F.E.: A review on wood waste burning. — Pulp Pap.-Canada 73: 70–75, 1972.

    Google Scholar 

  • Rewald B., Holzer L., Göransson H.: Arbuscular mycorrhiza inoculum reduces root respiration and improves biomass accumulation of salt-stressed Ulmus glabra seedlings. — Urban For. Urban Gree. 14: 432–437, 2015.

    Article  Google Scholar 

  • Ruiz-Lozano J.M., Porcel R., Azcón C., Aroca R.: Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. — J. Exp. Bot. 63: 4033–4044, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Selvakumar G., Kim K., Hu S., Sa T.: Effect of salinity on plants and the role of arbuscular mycorrhizal fungi and plant growthpromoting rhizobacteria in alleviation of salt stress. — In: Ahmad P., Wani M.R. (ed.): Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Pp. 115–144. Springer, New York 2014.

    Chapter  Google Scholar 

  • Sheng M., Tang M., Zhang F., Huang Y.H.: Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. — Mycorrhiza 21: 423–430, 2011.

    Article  PubMed  Google Scholar 

  • Sheng M., Tang M., Chen H. et al.: Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. — Mycorrhiza 18: 287–296, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Smith S.E., Read D.J.: Arbuscular mycorrhizas. — In: Smith S.E., Read D.J. (ed.): Mycorrhizal Symbiosis. 3rd ed. Pp. 31–134. Academic Press, New York 2008.

    Google Scholar 

  • Sun X.G., Tang M.: Comparison of four routinely used methods for assessing root colonization by arbuscular mycorrhizal fungi. — Botany 90: 1073–1083, 2012.

    Article  Google Scholar 

  • Takai T., Kondo M., Yano M., Yamamoto T.: A quantitative trait locus for chlorophyll content and its association with leaf photosynthesis in rice. — Rice 3: 172–180, 2010.

    Article  Google Scholar 

  • Wicke B., Smeets E., Dornburg V. et al.: The global technical and economic potential of bioenergy from salt-affected soils. — Energ. Environ. Sci. 4: 2669–2681, 2011.

    Article  Google Scholar 

  • Wu Q.S., Zou Y.N., He X.H.: 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.

    Article  Google Scholar 

  • Yang C.W., Xu H.H., Wang L.L. et al.: Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. — Photosynthetica 47: 79–86, 2009.

    Article  CAS  Google Scholar 

  • Zai X.M., Zhu S.N., Qin P. et al.: Effect of Glomus mosseae on chlorophyll content, chlorophyll fluorescence parameters, and chloroplast ultrastructure of beach plum (Prunus maritima) under NaCl stress. — Photosynthetica 50: 323–328, 2012.

    Article  CAS  Google Scholar 

  • Zhang J.F.: Coastal Saline Soil Rehabilitation and Utilization Based on Forestry Approaches in China. Pp. 145–164. Springer, Berlin–Heidelberg 2014.

    Book  Google Scholar 

  • Zhang J.F., Chen G.C., Xing S. et al.: Carbon sequestration of black locust forests in the Yellow River Delta region, China. — Int. J. Sust. Dev. World 17: 475–480, 2010.

    Article  Google Scholar 

  • Zhang J.F., Song Y.M., Xing S.J. et al.: [Saline soil amelioration and forestation techniques.] — J. Northeast Forest. Univ. 30: 124–129, 2002a. [In Chinese]

    CAS  Google Scholar 

  • Zhang S.Z., Li Y., Jiang G.B. et al.: [Studies on genetic variation, correlation and selection of salinity tolerance traits of Robinia pseudoacacia families.] — J. Beijing Forest. Univ. 24: 12–17, 2002b. [In Chinese]

    Google Scholar 

  • Zhu X.Q., Wang C.Y., Chen H., Tang M.: Effects of arbuscular mycorrhizal fungi on photosynthesis, carbon content, and calorific value of black locust seedlings. — Photosynthetica 52: 247–252, 2014.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. College of Forestry, Northwest A&F University, Yangling, 712100, China

    X. Q. Zhu, M. Tang & H. Q. Zhang

  2. Key Laboratory of Plant-Microbe Interactions, Shangqiu Normal University, Shangqiu, 476000, China

    X. Q. Zhu

Authors
  1. X. Q. Zhu
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  2. M. Tang
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  3. H. Q. Zhang
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Correspondence to H. Q. Zhang.

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Acknowledgments: This research was supported by Special Fund for Forest Scientific Research in the Public Welfare (201404217), the National Natural Science Foundation of China (31270639, 31170567), the Program for Changjiang Scholars and Innovative Research Team in University of China (IRT1035), the General Financial Grand from the China Postdoctoral Science Foundation (2016M592849), and Natural Science Foundation of Henan Province (142102110185).

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Zhu, X.Q., Tang, M. & Zhang, H.Q. Arbuscular mycorrhizal fungi enhanced the growth, photosynthesis, and calorific value of black locust under salt stress. Photosynthetica 55, 378–385 (2017). https://doi.org/10.1007/s11099-017-0662-y

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  • DOI: https://doi.org/10.1007/s11099-017-0662-y

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