Skip to main content
SpringerLink
Log in

Arbuscular Mycorrhizal Fungus Alleviates Chilling Stress by Boosting Redox Poise and Antioxidant Potential of Tomato Seedlings

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The universal symbiotic associations between arbuscular mycorrhizal fungi (AMF) and plant roots remarkably stimulate plant growth, nutrient uptake, and stress responses. The present study investigated the stress ameliorative potential of the AM fungus Funneliformis mosseae against chilling in tomato seedlings. AMF-inoculated tomato seedlings exhibited significantly higher fresh weight and dry weight than non-AMF control plants under both control (25/15 °C) and low temperature (8 °C/4 °C) treatments. Under chilling stress, AMF inoculation significantly reduced the level of MDA, H2O2, and O ·−2 along with increased calcium precipitates in the apoplast and vacuole of root cells compared with the non-AMF control. Furthermore, AMF inoculation induced activities of antioxidant enzymes and transcripts of related genes under chilling stress. Notably, AMF inoculation resulted in reduced redox state in root cells as evident by significantly increased content of reduced ascorbate, reduced glutathione, redox ratio, and the activity of l-galactono-1,4-lactone dehydrogenase in the tomato roots both under control and low temperature. Taken together, these results indicate that AMF could play an important role in optimizing chilling resistance by maintaining redox poise and calcium balance in tomato seedlings.

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
Fig. 7

Similar content being viewed by others

References

  • Abdel Latef AAH, He CX (2011) Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol Plant 33:1217–1225

    Article  CAS  Google Scholar 

  • Adriano S, Angelo CT, Bartolomeo D, Cristos X (2005) Influence of water deficit and rewatering on the components of the ascorbate–glutathione cycle in four interspecific Prunus hybrids. Plant Sci 169:403–412

    Article  Google Scholar 

  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, Del Rio LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295

    Article  CAS  PubMed  Google Scholar 

  • Alqarawi AA, Abd Allah EF, Hashem A (2014) Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J Plant Interact 9:802–810

    Article  Google Scholar 

  • Atherton JG, Rudich J (1986) The Tomato Crop. Chapman and Hall Ltd, New York

    Book  Google Scholar 

  • Azcón R, Perálvarez MC, Biró B, Roldán A, Ruíz-Lozano JM (2009) Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multicontaminated soil amended with treated lignocellulosic agrowaste. Appl Soil Ecol 41:168–177

    Article  Google Scholar 

  • Batistič O, Kudla J (2012) Analysis of calcium signaling pathways in plants. BBA Gen Subj 1820:1283–1293

    Article  Google Scholar 

  • Begcy K, Mariano E, Mattiello L, Nunes AV, Mazzafera P, Maia IG, Menossi M (2011) An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants. PLoS ONE 6:e23776

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bian SM, Jiang YW (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic 120:264–270

    Article  CAS  Google Scholar 

  • Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:895–904

    Article  PubMed Central  PubMed  Google Scholar 

  • Bunn R, Lekberg Y, Zabinski C (2009) Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants. Ecology 90:1378–1388

    Article  PubMed  Google Scholar 

  • Chen SC, Jin WJ, Liu AR, Zhang SJ, Liu DL, Wang FH, Lin XM, He CX (2013) Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Sci Hortic 160:222–229

    Article  CAS  Google Scholar 

  • Chen LJ, Xiang HZ, Miao Y, Zhang L, Guo ZF, Zhao XH, Lin JW, Li TL (2014) An overview of cold resistance in plants. J Agron Crop Sci 200:237–245

    Article  CAS  Google Scholar 

  • Das R, Pandey A (2014) Role of calcium/calmodulin in plant stress response and signaling. In: Das R, Pandey A, Pandey GK (eds) Approaches to plant stress and their management. Springer, New Delhi, pp 53–84

    Chapter  Google Scholar 

  • Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiol 114:1031–1037

    PubMed Central  CAS  PubMed  Google Scholar 

  • El-Tohamy W, Schnitzler WH, El-Behairy U, El-Beltagy MS (1999) Effect of VA mycorrhiza on improving drought and chilling tolerance of bean plants (Phaseolus vulgaris L). J Appl Bot 73(5–6):178–183

    CAS  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium-chloride-simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Faltin Z, Holland D, Velcheva M, Tsapovetsky M, Roeckel-Drevet P, Handa AK, Abu-Abied M, Friedman-Einat M, Eshdat Y, Perl A (2010) Glutathione peroxidase regulation of reactive oxygen species level is crucial for in vitro plant differentiation. Plant Cell Physiol 51:1151–1162

    Article  CAS  PubMed  Google Scholar 

  • Fester T, Hause G (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15:373–379

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  PubMed  Google Scholar 

  • Fusconi A, Berta G (2012) Environmental stress and role of arbuscular mycorrhizal symbiosis. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants. Springer, New York, pp 197–214

    Chapter  Google Scholar 

  • Garcia-Sanchez M, Palma JM, Ocampo JA, Garcia-Romera I, Aranda E (2014) Arbuscular mycorrhizal fungi alleviate oxidative stress induced by ADOR and enhance antioxidant responses of tomato plants. J Plant Physiol 171:421–428

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microb Biot 27:1231–1240

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Huang YM, Srivastava AK, Zou YN, Ni QD, Han Y, Wu QS (2014) Mycorrhizal-induced calmodulin mediated changes in antioxidant enzymes and growth response of drought-stressed trifoliate orange. Front Microbiol 5:682. doi:10.3389/fmicb.2014.00682

    Article  PubMed Central  PubMed  Google Scholar 

  • Iseri OD, Korpe DA, Sahin FI, Haberal M (2013) Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress. Acta Physiol Plant 35:1905–1913

    Article  CAS  Google Scholar 

  • Kopriva S, Mugford SG, Baraniecka P, Lee BR, Matthewman CA, Koprivova A (2012) Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis. Front Plant Sci 3:1–9

    Article  Google Scholar 

  • Kumar A, Dames JF, Gupta A, Sharma S, Gilbert JA, Ahmad P (2014) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Crit Rev Biotechnol. doi:10.3109/07388551.2014.899964

    PubMed  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic-acid in spinach (Spinacia oleracea) chloroplasts—the effect of hydrogen-peroxide and of Paraquat. Biochem J 210:899–903

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lázaro JJ, Jiménez A, Camejo D, Iglesias-Baena I, Martí Mdel C, Lázaro-Payo A, Barranco-Medina S, Sevilla F (2013) Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front Plant Sci 4:460

    Article  PubMed Central  PubMed  Google Scholar 

  • Lecourieux D, Ranjeva R, Pugin Alain (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269

    Article  CAS  PubMed  Google Scholar 

  • Li SW, Xue LG (2010) The interaction between H2O2 and NO, Ca2+, cGMP, and MAPKs during adventitious rooting in mung bean seedlings. In Vitro Cell Dev Biol Plant 46:142–148

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma YH, Ma FW, Zhang JK, Li MJ, Wang YH, Liang D (2008) Effects of high temperature on activities and gene expression of enzymes involved in ascorbate-glutathione cycle in apple leaves. Plant Sci 175:761–766

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Ntatsi G, Savvas D, Ntatsi G, Klaring HP, Schwarz D (2014) Growth, yield, and metabolic responses of temperature-stressed tomato to grafting onto rootstocks differing in cold tolerance. J Am Soc Hortic Sci 139:230–243

    CAS  Google Scholar 

  • Ordoñez NM, Marondedze C, Thomas L, Pasqualini S, Shabala L, Shabala S, Gehring C (2014) Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots. FEBS Lett 588:1008–1015

    Article  PubMed  Google Scholar 

  • Pandey SK, Nookaraju A, Upadhyaya CP, Gururani MA, Venkatesh J, Kim DH, Park SW (2011) An update on biotechnological approaches for improving abiotic stress tolerance in tomato. Crop Sci 51:2303–2324

    Article  CAS  Google Scholar 

  • Popov VN, Antipina OV, Pchelkin VP, Tsydendambaev VD (2012) Changes in the content and composition of lipid fatty acids in tobacco leaves and roots at low-temperature hardening. Russ J Plant Physiol 59:177–1782

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • Porter WM (1979) The “Most Probable Number” method for enumerating infective propagules of vesicular arbuscular mycorrhizal fungi in soil. Aust J Soil Res 17:515–519

    Article  Google Scholar 

  • Rao MV, Ormrod DP (1995) Impact of UVB and O3 on the oxygen-free radical scavenging system in Arabidopsis thaliana genotypes differing in flavonoid biosynthesis. Photochem Photobiol 62:719–726

    Article  CAS  Google Scholar 

  • Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12:30–43

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shigeoka S, Maruta T (2014) Cellular redox regulation, signaling, and stress response in plants. Biosci Biotechnol Biochem 78:1457–1470

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  PubMed  Google Scholar 

  • Talaat NB, Shawky BT (2014) Modulation of the ROS-scavenging system in salt-stressed wheat plants inoculated with arbuscular mycorrhizal fungi. J Plant Nutr Soil Sci 177:199–207

    Article  CAS  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants. Plant Signal Behav 2:79–85

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang LY, Li D, Deng YS, Lv W, Meng QW (2013) Antisense-mediated depletion of tomato GDP-l-galactose phosphorylase increases susceptibility to chilling stress. J Plant Physiol 170:303–314

    Article  CAS  PubMed  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, VanMontagu M, Inze D, VanCamp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 99:4097–4102

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu JQ, Sun Y, Zhang Y, Ding J, Xia XJ, Xiao CL, Shi K, Zhou YH (2009) Selective trans-cinnamic acid uptake impairs [Ca2+]cyt homeostasis and growth in Cucumis sativus L. J Chem Ecol 35:1471–1477

    Article  CAS  PubMed  Google Scholar 

  • Zhang GX, Liu YF, Ni Y, Meng ZJ, Lu T, Li TL (2014) Exogenous calcium alleviates low night temperature stress on the photosynthetic apparatus of tomato leaves. PLoS One 9:e97322

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou J, Wang J, Shi K, Xia XJ, Zhou YH, Yu JQ (2012a) Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol Biochem 60:141–149

    Article  CAS  PubMed  Google Scholar 

  • Zhou ZZ, Ma HM, Liang KN, Huang GH, Pinyopusarerk K (2012b) Improved tolerance of teak (Tectona grandis L.f.) seedlings to low-temperature stress by the combined effect of arbuscular mycorrhiza and paclobutrazol. J Plant Growth Regul 31:427–435

    Article  CAS  Google Scholar 

  • Zhu XC, Song FB, Xu HW (2010) Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza 20:325–332

    Article  CAS  PubMed  Google Scholar 

  • Zou YN, Huang YM, Wu QS, He XH (2015) Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2 effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza 25:143–152

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by National Natural Science Foundation of China (31471867, 31101536), Science Development Plan Project of Shandong Province (2012GNC011111), and Outstanding Young Teacher Project in Henan Province (2011GGJS-075, 2012GGJS-078).

Author information

Authors and Affiliations

  1. College of Forestry, Henan University of Science and Technology, No.70, Tianjin Road, Luoyang, 471003, Henan, People’s Republic of China

    Airong Liu, Shuangchen Chen, Mengmeng Wang, Rui Chang, Xiaomin Lin & Golam Jalal Ahammed

  2. Department of Plant Science, Agricultural and Animal Husbandry College of Tibet University, Xueyuan Road, Linzhi, 860000, People’s Republic of China

    Shuangchen Chen & Zhonghong Wang

  3. Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, Guangdong, People’s Republic of China

    Dilin Liu

  4. Laboratory of Plant Physiology, Wageningen University, Wageningen, 6700 AR, The Netherlands

    Bing Bai

Authors
  1. Airong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuangchen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mengmeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dilin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rui Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhonghong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaomin Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bing Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Golam Jalal Ahammed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shuangchen Chen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, A., Chen, S., Wang, M. et al. Arbuscular Mycorrhizal Fungus Alleviates Chilling Stress by Boosting Redox Poise and Antioxidant Potential of Tomato Seedlings. J Plant Growth Regul 35, 109–120 (2016). https://doi.org/10.1007/s00344-015-9511-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-015-9511-z

Keywords

Search

Navigation