Skip to main content
SpringerLink
Log in

Colonization with arbuscular mycorrhizal fungus affects growth, drought tolerance and expression of stress-responsive genes in Poncirus trifoliata

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The objective of this study was to investigate the effects of arbuscular mycorrhizal fungus (AMF) inoculation on growth and drought tolerance of Poncirus trifoliata seedlings. The seedlings were inoculated with or without Glomus mosseae before exposure to a short-term (3 days) water depletion, and relevant physiological and biochemical parameters (plant height, chlorophyll content, relative water content, activity of antioxidant enzymes) and expression patterns of several stress-responsive genes were examined. Inoculation with G. mosseae led to growth promotion of the seedlings, as revealed by larger plant height and higher relative water and chlorophyll contents. When subjected to drought treatment, the AMF-inoculated (AM) plants showed better tolerance than the nonmycorrhizal (NAM) plants. Under drought, the AM plants exhibited higher level of proline and activity of two antioxidant enzymes, superoxide dismutase (SOD) and peroxidase (POD). In addition, mRNA abundance of four genes involved in reactive oxygen species homeostasis and oxidative stress battling was higher in the AM plants when compared with the NAM plants. These results indicate that AMF inoculation stimulated growth and enhanced drought tolerance of the seedlings, which may be due to activation of an arsenal of physiological, biochemical and molecular alterations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AMF:

Arbuscular mycorrhizal fungus

EL:

Electrolyte leakage

POD:

Peroxidase

ROS:

Reactive oxygen species

RT-PCR:

Reverse transcriptase PCR

RWC:

Relative water content

SOD:

Superoxide dismutase

References

  • Alvarez M, Huygens D, Olivares E, Saavedra I, Alberdi M, Valenzuela E (2009) Ectomycorrhizal fungi enhance nitrogen and phosphorus nutrition of Nothofagus dombeyi under drought conditions by regulating assimilative enzyme activities. Physiol Plant 136:426–436

    Article  PubMed  CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular mycorrhizal fungi symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Bolandnazar S (2009) The effect of mycorrhizal fungi on onion (Allium cepa L.) growth and yield under three irrigation intervals at field condition. J Food Agric Environ 7:360–362

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Bressano M, Curetti M, Giacheroa L, Gil SV, Cabello M, March G, Ducasse DA, Luna CM (2010) Mycorrhizal fungi symbiosis as a strategy against oxidative stress in soybean plants. J Plant Physiol 167:1622–1626

    Article  PubMed  CAS  Google Scholar 

  • Cavagnaro TR, Dickson S, Smith FA (2010) Arbuscular mycorrhizas modify plant responses to soil zinc addition. Plant Soil 329:307–313

    Article  CAS  Google Scholar 

  • Cho EJ, Lee DJ, Wee CD, Kim HL, Cheong YH, Cho JS, Sohn BK (2009) Effects of AMF inoculation on growth of Panax ginseng C.A. Meyer seedlings and on soil structures in mycorrhizosphere. Sci Hortic 122:633–637

    Article  CAS  Google Scholar 

  • Cuming AC, SuH Cho, Kamisugi Y, Graham H, Quatrano RS (2007) Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss, Physcomitrella patens. New Phytol 176:275–287

    Article  PubMed  CAS  Google Scholar 

  • Debiane D, Garçon G, Verdin A, Fontaine J, Durand R, Shirali P, Ferjani AG, Sahraoui AL (2009) Mycorrhization alleviates benzo[a]pyrene-induced oxidative stress in an in vitro chicory root model. Phytochemistry 70:1421–1427

    Article  PubMed  CAS  Google Scholar 

  • Endres S, Tenhaken R (2009) Myoinositol oxygenase controls the level of myoinositol in Arabidopsis, but does not increase ascorbic acid. Plant Physiol 149:1042–1049

    Article  PubMed  CAS  Google Scholar 

  • Estrada-Luna AA, Davies FT Jr (2003) Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J Plant Physiol 160:1073–1083

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  PubMed  CAS  Google Scholar 

  • Hassine AB, Ghanem ME S, Bouzid LuttsS (2008) An inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycine betaine in response to salinity and water stress. J Exp Bot 59:1315–1326

    Article  PubMed  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  PubMed  CAS  Google Scholar 

  • Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230

    Article  PubMed  Google Scholar 

  • Kytöviita MM, Ruotsalainen AL (2007) Mycorrhizal benefit in two low Arctic herbs increases with increasing temperature. Am J Bot 94:1309–1315

    Article  PubMed  Google Scholar 

  • Latef AA, He CX (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 127:228–233

    Article  Google Scholar 

  • Llorente F, López-Cobollo RM, Catalá R, Martínez-Zapater JM, Salinas J (2002) A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance. Plant J 32:13–24

    Article  PubMed  CAS  Google Scholar 

  • López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601

    Article  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–457

    Article  PubMed  CAS  Google Scholar 

  • Molinari HB, Marur CJ, Daros E, Marilia Campos KF, Carvalho JF, Filho JC, Pereira LF, Vieira LG (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plant 130:218–229

    Article  CAS  Google Scholar 

  • Navarro A, Sánchez-Blanco MJ, Mortec A, Bañón S (2009) The influence of mycorrhizal inoculation and paclobutrazol on water and nutritional status of Arbutus unedo L. Environ Exp Bot 66:362–371

    Article  CAS  Google Scholar 

  • Poerwanto R, Inoue H, Kataoka I (1989) Effects of temperature on the morphology and physiology of the roots of trifoliate orange budded with Satsuma mandarin. J Jpn Soc Hortic Sci 58:267–274

    Article  Google Scholar 

  • 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 55:1743–1750

    Article  PubMed  CAS  Google Scholar 

  • Porcel R, Aroca R, Azcón R, Ruiz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60:389–404

    Article  PubMed  CAS  Google Scholar 

  • Porras-Soriano A, Soriano-Martin ML, Porras-Piedra A, Azcón R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359

    Article  PubMed  CAS  Google Scholar 

  • Posada RH, Franco LA, Ramos C, Plazas LS, Suarez JC, Alvarez F (2008) Effect of physical, chemical and environmental characteristics on arbuscular mycorrhizal fungi in Brachiaria decumbens (Stapf) pastures. J Appl Microbiol 104:132–140

    PubMed  CAS  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  PubMed  CAS  Google Scholar 

  • Rueda-Puente EO, Amador BM, Cervantes Hernández TL, Herrera MA, Medina SM, Barrera LE (2010) Effects of plant growth promoting bacteria and mycorrhizal on Capsicum annuum L. var. aviculare ([Dierbach] D’Arcy and Eshbaugh) germination under stressing abiotic conditions. Plant Physiol Biochem 48:724–730

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

  • Ruiz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM (2010) Arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869

    Article  PubMed  Google Scholar 

  • Shi S, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, Elsevier, London

    Google Scholar 

  • Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323

    Article  PubMed  CAS  Google Scholar 

  • Tian C, Kasiborski B, Koul R, Lammers PJ, Bücking H, Shachar-Hill Y (2010) Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol 153:1175–1187

    Article  PubMed  CAS  Google Scholar 

  • Valentine AJ, Osborne BA, Mitchell DT (2001) Interactions between phosphorus supply and total nutrient availability on mycorrhizal colonization, growth and photosynthesis of cucumber. Sci Hortic 88:177–189

    Article  CAS  Google Scholar 

  • Vallino M, Martino E, Boella F, Murat C, Chiapello M, Perotto P (2009) Cu, Zn superoxide dismutase and zinc stress in the metal-tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn. FEMS Microbiol Lett 293:48–57

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Sun PP, Chen CL, Wang Y, Fu XZ, Liu JH (2011) An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J Exp Bot 62:2899–2894

    Google Scholar 

  • Yao Q, Wang LR, Zhu HH, Chen JZ (2009) Effect of arbuscular mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Sci Hortic 121:458–461

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China, the Ministry of Education of China (20090146110010), Hubei Provincial Natural Science Foundation (2009CDA080), the Fok Ying Tong Education Foundation (No. 114034). The authors are grateful to Peng Wang for technical assistance.

Author information

Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology (MOE), National Key Laboratory of Crop Genetic Improvement, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China

    Qi-Jun Fan & Ji-Hong Liu

Authors
  1. Qi-Jun Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ji-Hong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ji-Hong Liu.

Additional information

Communicated by J. Zwiazek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fan, QJ., Liu, JH. Colonization with arbuscular mycorrhizal fungus affects growth, drought tolerance and expression of stress-responsive genes in Poncirus trifoliata . Acta Physiol Plant 33, 1533–1542 (2011). https://doi.org/10.1007/s11738-011-0789-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-011-0789-6

Keywords

Search

Navigation