Skip to main content

Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress

Mycorrhiza volume 23, pages 381–390 (2013)Cite this article

Abstract

The influence of the arbuscular mycorrhizal (AM) fungus, Glomus fasciculatum, on the growth, heat stress responses and the antioxidative activity in cyclamen (Cyclamen persicum Mill.) plants was studied. Cyclamen plants (inoculated or not with the AM fungus) were placed in a commercial potting media at 17–20 °C for 12 weeks in a greenhouse and subsequently subjected to two temperature conditions in a growth chamber. Initially, plants were grown at 20 °C for 4 weeks as a no heat stress (HS−) condition, followed by 30 °C for another 4 weeks as a heat stress (HS+) condition. Different morphological and physiological growth parameters were compared between G. fasciculatum-inoculated and noninoculated plants. The mycorrhizal symbiosis markedly enhanced biomass production and HS + responses in plants compared to that in the controls. A severe rate of leaf browning (80–100 %) was observed in control plants, whereas the mycorrhizal plants showed a minimum rate of leaf browning under HS + conditions. The mycorrhizal plants showed an increase activity of antioxidative enzymes such as superoxide dismutase and ascorbate peroxidase, as well as an increase in ascorbic acid and polyphenol contents. The 2,2-diphenyl-1-picrylhydrazyl radical scavenging activity also showed a greater response in mycorrhizal plants than in the control plants under each temperature condition. The results indicate that in cyclamen plants, AM fungal colonisation alleviated heat stress damage through an increased antioxidative activity and that the mycorrhizal symbiosis strongly enhanced temperature stress tolerance which promoted plant growth and increased the host biomass under heat stress.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Alguacil MM, Hernandez JA, Caravaea F, Portillo B, Roldan A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant 118:562–570

    Article  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Ball GV (1991) Cyclamen (Cyclamen persicum) In: Ball GV (ed.) The Ball redbook, 15th edn. Geo J. Ball, Chicago, pp 475-481

  • Baumann K, Schneider BU, Marschner P, Hüttl RF (2005) Root distribution and nutrient status of mycorrhizal and non-mycorrhizal Pinus sylvestris L. Seedlings growing in a sandy substrate with lignite fragments. Plant Soil 276:347–357

    Article  CAS  Google Scholar 

  • Ben Khaled L, Gomez AM, Ourraqi EM, Oihabi A (2003) Physiological and biochemical responses to salt stress of mycorrhized and/or nodulated clover seedlings (Trifolium alexandrinum L.). Agron 23:571–580

    Article  CAS  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    PubMed  Article  CAS  Google Scholar 

  • Borland A, Elliott S, Patterson S (2006) Are the metabolic components of crassulacean acid metabolism up-regulated in responses to an increase in oxidative bueden? J Exp Bot 57:319–328

    PubMed  Article  CAS  Google Scholar 

  • Bors W, Michel C, Saran M (1994) Flavonoids antioxidants: rate constants for reactions with oxygen radicals. Methods Enzymol 234:420–429

    PubMed  Article  CAS  Google Scholar 

  • Burits M, Bucar F (2000) Antioxidant activity of Nigella sativa essential oil. Phytother Res 14:323–328

    PubMed  Article  CAS  Google Scholar 

  • Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbial Ecol 73:197–214

    CAS  Google Scholar 

  • Elmer WH, McGovern RJ (2004) Efficacy of integrating biologicals with fungicides for the suppression of Fusarium wilt of cyclamen. Crop Prot 23:909–914

    Article  CAS  Google Scholar 

  • Goto T, Shimizu N, Morishita T, Fujii K, Nakano Y, Shima K (2011) Effects of polyethylene pot removal and irrigation method on growth and flowering of garden-type cyclamen. Acta Hortic 886:83–90

    Google Scholar 

  • Grace SC (2005) Phenolics and antioxidants. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Oxford, UK, pp 141-168

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

    Article  Google Scholar 

  • Hajiboland R, Aliasgharzadesh N, Laiegh FS, 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 

  • Hichem H, Mounir D, Naceur EA (2009) Differential responses of two maize (Zea mays L.) varieties to salt stress: changes on polyphenols composition of foliage and oxidative damages. Ind Crops Prod 30:144–151

    Article  CAS  Google Scholar 

  • Horemans N, Foyer CH, Potters G, Asard H (2000) Ascorbate function and associated transport systems in plants. Plant Physiol Biochem 38:531–540

    Article  CAS  Google Scholar 

  • Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès J, Al-Jaburi HJ, Zhao CX, Shao HB, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436

    Article  Google Scholar 

  • Karlsson M, Werner J (2001a) Temperature affects rate of leaf unfolding and flowering in cyclamen. HortScience 36:292–294

    Google Scholar 

  • Karlsson MG, Werner JW (2001b) Temperature after flower initiation affects morphology and flowering of cyclamen. Sci Hortic 91:357–363

    Article  Google Scholar 

  • Latef AAHA, Chaoxing H (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  Google Scholar 

  • Liu A, Wang B, Hamel C (2004) Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature. Mycorrhiza 14:93–101

    PubMed  Article  CAS  Google Scholar 

  • Martin CA, Stutz JC (2004) Interactive effects of temperature and arbuscular mycorrhizal fungi on growth, P uptake and root respiration of Capsicum annum L. Mycorrhiza 14:241–244

    PubMed  Article  Google Scholar 

  • Marxen K, Vanselow KH, Lippemeier S, Hintze R, Ruser A, Hansen UP (2007) Determination of DPPH radical oxidation caused by methanolic extracts of some microalgal species by linear regression analysis of spectrophotometric measurements. Sensors 7:2080–2095

    Article  CAS  Google Scholar 

  • Matsubara Y (2010) High temperature stress tolerance and the changes in antioxidative ability in mycorrhizal strawberry plants. In Abigail N, Sampson (ed) Horticulture in the 21st century. Nova Science, New York, pp 179-192

  • Matsubara Y, Harada T (1996) Effect of constant and diurnally fluctuating temperatures on arbuscular mycorrhizal fungus infection and the growth of infected asparagus (Asparagus officinalis L.) seedlings. J Japan Soc Hortic Sci 65:565–570

    Article  Google Scholar 

  • McDonald S, Prenzler PD, Autolovich M, Robards K (2001) Phenolic content and antioxidant activity of olive oil extracts. Food Chem 73:73–84

    Article  CAS  Google Scholar 

  • Miransari M, Bahrami HA, Rejali F, Malakouti MJ (2008) Using arbuscular mycorrhiza to alleviate the stress of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1206

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    PubMed  Article  CAS  Google Scholar 

  • Mukherjee SP, Choudhouri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Nahiyan ASM, Matsubara Y (2012) Tolerance to fusarium root rot and changes in antioxidative ability in mycorrhizal asparagus plants. Hortscience 47:356–360

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Noctor G (2006) Metabolic signaling in defense and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425

    PubMed  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 55:158–163

    Article  Google Scholar 

  • Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143

    Article  CAS  Google Scholar 

  • Potters G, De Gara L, Asard H, Horemans N (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40:537–548

    Article  CAS  Google Scholar 

  • Prior RL, Cao G (1999) In vivo total antioxidant capacity: comparison of different analytical methods. Free Radical Bio Med 27:1173–1181

    Article  CAS  Google Scholar 

  • Sairam RK, Srivastava GC, Saxena DC (2000) Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes. Biol Plant 43:245–251

    Article  CAS  Google Scholar 

  • Sánchez-Moreno C, Larrauri JA, Saura-Calixto F (1999) Free radical scavenging capacity and inhibition of lipid oxidation of wines, grape juices and related polyphenolic constituents. Food Res Int 32:407–412

    Article  Google Scholar 

  • Shokri S, Maadi B (2009) Effect of arbuscular mycorrhizal fungus on the mineral nutrition and yield of Trifolium alexandrinum plants under salinity stress. J Agron 8:79–83

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Tabata K, Oba K, Suzuki K, Esaka M (2001) Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for L-galactono-1,4-lactone dehydrogenase. Plant J 27:139–148

    PubMed  Article  CAS  Google Scholar 

  • Tanou G, Molassiotis A, Diamantidis G (2009) Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot 65:270–281

    Article  CAS  Google Scholar 

  • Venkateswarlu B, Shanker AK (2009) Climate change and agriculture: adaptation and mitigation strategies. Indian J Agron 54:226–230

    Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Weih M, Karlsson PS (1999) Growth response of altitudinal ecotypes of mountain birch to temperature and fertilisation. Oecologia 119:16–23

    Article  Google Scholar 

  • Wu QS, Xia RX, Zou YN (2006) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163:1101–1110

    PubMed  Article  CAS  Google Scholar 

  • Wu G, Wei ZK, Shao HB (2007) The mutual responses of higher plants to environment: physiological and microbiological aspects. Biointerfaces 59:113–119

    Article  CAS  Google Scholar 

  • Yesson C, Culham A (2006) A phyloclimatic study of cyclamen. BMC Evol Biol 6:72

    PubMed  Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Zhu XC, Song FB, Xu HW (2010b) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331:129–137

    Article  CAS  Google Scholar 

  • Zhu XC, Song FB, Liu SQ, Liu TD (2011) Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 346:189–199

    Article  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. The United Graduate School of Agricultural Science, Gifu University, Gifu, 501-1193, Japan

    Moslama Aktar Maya

  2. Faculty of Applied Biological Sciences, Gifu University, Gifu, 501-1193, Japan

    Yoh-ichi Matsubara

Authors
  1. Moslama Aktar Maya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoh-ichi Matsubara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoh-ichi Matsubara.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Maya, M.A., Matsubara, Yi. Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza 23, 381–390 (2013). https://doi.org/10.1007/s00572-013-0477-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-013-0477-z

Keywords

  • Abiotic stress
  • Mycorrhizal symbiosis
  • Glomus fasciculatum
  • Growth promotion
  • Superoxide dismutase
  • Cyclamen persicum