Skip to main content
SpringerLink
Log in

Arbuscular Mycorrhiza and Reactive Oxygen Species

  • Chapter
  • First Online:
Arbuscular Mycorrhizas and Stress Tolerance of Plants

Abstract

The accrual of reactive oxygen species (ROS) is a common biochemical response to all abiotic and biotic stresses in plants. ROS are extremely lethal to biological cells causing oxidative damage to DNA, lipids and proteins. Plants have developed many strategies to overcome oxidative stress to restore the redox homeostasis. One of the strategies is to establish symbiotic association in roots with arbuscular mycorrhizal (AM) fungi to improve host resistance to stress. Initial stages of AM fungus colonization trigger intracellular ROS burst in host plant; however, this effect is transient and is overcome by enhanced activities of antioxidant enzymes and molecules such as carotenoid. Accumulation of ROS in cortical cells has also been related to arbuscule digestion. Improvement of stress resistance has usually been associated with AM-induced escalation in P acquisition and plant growth. Nevertheless, non-nutritional effects of AM on host plants have attracted increasing attention. Under stress conditions, AM plants show reduced lipid peroxidation and lower levels of hydrogen peroxide and superoxide. The formation of AM reinforces the antioxidant defence system of the plant for the prevention of oxidative damage. AM symbiosis is capable of increasing activities of enzymes involved directly in removal of ROS such as superoxide dismutase, catalase (CAT) and ascorbate (ASH)- or thiol-dependent peroxidases (POX) and indirectly by generation of two redox molecules ascorbate and glutathione such as glutathione reductase (GR), dehydroascorbate reductase and monodehydroascorbate reductase. AM helps in augmenting the concentrations of non-enzymatic antioxidants such as α-tocopherol, proline, carotenoids, glutathione and ascorbic acid. This review summarizes current knowledge on the effects of AM symbiosis on the accumulation of ROS and correspondingly on the antioxidant defence system. New perspectives and challenges in molecular studies on oxidative stress alleviation by AM symbiosis are proposed.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abbá S, Khouja HR, Martino E et al (2009) SOD1-targeted gene disruption in the ericoid mycorrhizal fungus Oidiodendron maius reduces conidiation and the capacity for mycorrhization. Mol Plant-Microbe Interact 22(11):1412–1421

    Article  PubMed  CAS  Google Scholar 

  • Abdel Latef AAH, Chaoxing H (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  CAS  Google Scholar 

  • 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(4):1217–1225

    Article  CAS  Google Scholar 

  • Abo-Doma A, Edrees S, Abdel-Aziz SH (2011) The effect of mycorrhiza growth and expression of some genes in barley. Egypt J Genet Cytol 40:301–313

    Google Scholar 

  • Alguacil MM, Herna ́ndez JA, Caravaca F et al (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant 118(4):562–570

    Article  CAS  Google Scholar 

  • Allen MF (2006) Water dynamics of mycorrhiza in arid soils. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, London, pp 74–97

    Chapter  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(1):802–810

    Article  CAS  Google Scholar 

  • Apel Laloi K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Arines J, Quintela M, Vilarino A et al (1994) Protein patterns and superoxide dismutase activity in non-mycorrhizal and arbuscular mycorrhizal Pisum sativum L. plants. Plant Soil 166(1):37–45

    Article  CAS  Google Scholar 

  • Aroca R, Bago A, Sutka M et al (2009) Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and non-stressed mycelium. Mol Plant-Microbe Interact 22(9):1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216

    Article  CAS  Google Scholar 

  • Azcón-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved. Mycorrhiza 6:457–464. doi:10.1007/s005720050147

    Article  Google Scholar 

  • Azcón-Aguilar C, Jaizme-Vega MC, Calvet C (2002) The contribution of arbuscular mycorrhizal fungi for bioremediation. In: Gianinazzi S, Schuepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture, From genes to bioproducts. Birkhauser Verlag, Berlin, pp 187–197

    Chapter  Google Scholar 

  • Azcón R, Pera ́lvarez MC, Biró B et al (2009) Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multi-contaminated soil amended with treated lignocellulosic agrowaste. Appl Soil Ecol 41(2):168–177

    Article  Google Scholar 

  • Babiychuk E, Kushnir S, Belles-Boix E et al (1995) Arabidopsis thaliana NADPH oxidoreductase homologs confer tolerance of yeasts toward the thiol-oxidizing drug diamide. J Biol Chem 270(3):26224–26231

    Article  CAS  PubMed  Google Scholar 

  • Bárzana G, Aroca R, Ruiz-Lozano JM (2015) Localized and non-localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 38:1613–1627

    Article  PubMed  CAS  Google Scholar 

  • Benabdellah K, Azcón-Aguilar C, Valderas A et al (2009a) GintPDX1 encodes a protein involved in vitamin B6 biosynthesis that is up-regulated by oxidative stress in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 184(3):682–693

    Article  CAS  PubMed  Google Scholar 

  • Benabdellah K, Merlos MA, Azcón-Aguilar C et al (2009b) GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genet Biol 46(1):94–103

    Article  CAS  PubMed  Google Scholar 

  • Bienert GP, Møller ALB, Kristiansen KA et al (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282(2):1183–1192

    Article  CAS  PubMed  Google Scholar 

  • Blee KA, Anderson AJ (2000) Defense responses in plants to arbuscular mycorrhizal fungi. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. American Phytopathological Society Press, St. Paul, pp 27–44

    Google Scholar 

  • Blilou I, Bueno P, Ocampo JA et al (2000) Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal fungus Glomus mosseae. Mycol Res 104(6):722–725

    Article  CAS  Google Scholar 

  • Bonfante-Fasolo P (1984) Anatomy and morphology of VA mycorrhizae. In: Powell CL, Bagyaraj DJ (eds) VA mycorrhiza. CRC Press, Boca Raton, pp 35–46

    Google Scholar 

  • Bouvier F, Backhaus RA, Camara B (1998) Induction and control of chromoplast-specific carotenoid genes by oxidative stress. J Biol Chem 273:30651–30659

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Fluhr R (2000) The role of calcium and activated oxygen as signals for controlling cross-tolerance. Trends Plant Sci 5(6):241–246

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Van Camp W, Van Montagu M et al (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218. doi:10.1080/07352689409701914

    Article  CAS  Google Scholar 

  • Brehelin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12(6):260–266

    Article  CAS  PubMed  Google Scholar 

  • Briviba K, Klotz LO, Sies H (1997) Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. Biol Chem 378(11):1259–1265

    CAS  PubMed  Google Scholar 

  • Cheeseman JM (2007) Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress 1(1):4–15

    Google Scholar 

  • Choi YE, Kwom KW, Lee JC et al (2007) Expression of the rice cytoplasmic cysteine synthase gene in tobacco reduces ozone-induced damage. Plant Biotechnol Rep 1(2):93–100

    Article  Google Scholar 

  • Collins A (2001) Carotenoids and genomic stability. Mutat Res 475(1–2):1–28

    Google Scholar 

  • Corradi N, Buffner B, Croll D et al (2009) High-level molecular diversity of copper-zinc superoxide dismutase genes among and within species of arbuscular mycorrhizal fungi. Appl Environ Microbiol 75(7):1970–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong CJ, Zhou Y, Zhao B (2004) Effect of flavonoids on AM fungi and mycorrhizal plant. Mycosystema 23(2):294–300

    CAS  Google Scholar 

  • Doubková P, Vlasáková E, Sudová R (2013) Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil. Plant Soil 370(1):149–161

    Article  CAS  Google Scholar 

  • Dumas-Gaudot E, Gollotte A, Cordier C et al (2000) Modulation of host defence systems. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 173–200

    Chapter  Google Scholar 

  • Evelin H, Kapoor R (2014) Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza 24(3):197–208

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22(3):203–217

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23(1):71–86

    Article  CAS  PubMed  Google Scholar 

  • Feierabend J, Engel S (1986) Photoinactivation of catalase in vitro and in leaves. Arch Biochem Biophys 251(2):567–576

    Article  CAS  PubMed  Google Scholar 

  • Fester T, Hause T (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15(5):373–379

    Article  CAS  PubMed  Google Scholar 

  • Fester T, Hause B, Schmidt D et al (2002) Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol 43(3):256–265

    Article  CAS  PubMed  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422(6930):442–446

    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(1):21–25

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17(7):1866–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155(1):2–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112

    Article  CAS  PubMed  Google Scholar 

  • Fridovich I (1997) Superoxide anion radical superoxide dismutases and related matters. J Biol Chem 272(30):18515–18517

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Sanchez M, Palma JM, Ocampo JA et al (2014) Arbuscular mycorrhizal fungi alleviate oxidative stress induced by ADOR and enhance antioxidant responses of tomato plants. J Plant Physiol 171(6):421–428

    Article  CAS  PubMed  Google Scholar 

  • Garg N, Baher N (2013) Role of arbuscular mycorrhizal symbiosis in proline biosynthesis and metabolism of Cicer arietinum (L.) (Chickpea) genotypes under salt stress. J Plant Growth Regul 32(4):767–778

    Article  CAS  Google Scholar 

  • Garg N, Bhandari P (2012) Influence of cadmium stress and arbuscular mycorrhizal fungi on nodule senescence in Cajanus cajan (L.) Millsp. Int J Phytoremediation 14(1):62–74

    Article  PubMed  Google Scholar 

  • Garg N, Chandel S (2015) Role of arbuscular mycorrhiza in arresting reactive oxygen species (ROS) and strengthening antioxidant defense in Cajanus cajan (L.) Millsp. nodules under salinity (NaCl) and cadmium (Cd) stress. Plant Growth Regul 75(2):521–534

    Article  CAS  Google Scholar 

  • Garg N, Manchanda G (2009a) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. J Agron Crop Sci 195(2):110–123

    Article  CAS  Google Scholar 

  • Garg N, Manchanda G (2009b) ROS generation in plants: boon or bane? Plant Biosyst 143:8–96

    Article  Google Scholar 

  • Garmendia I, Goicoechea N, Aguirreolea J (2004) Antioxidant metabolism in asymptomatic leaves of Verticillium-infected pepper associated with an arbuscular mycorrhizal fungus. J Phytopathol 152(11–12):593–599

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930

    Article  CAS  PubMed  Google Scholar 

  • González-Guerrero M, Cano C, Azcón-Aguilar C et al (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335

    Article  PubMed  CAS  Google Scholar 

  • González-Guerrero M, Oger E, Benabdellah K et al (2010) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr Genet 56(3):265–274

    Article  PubMed  CAS  Google Scholar 

  • Hajiboland R, Aliasgharzadeh N, Laiegh SF et al (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331(1):313–327

    Article  CAS  Google Scholar 

  • Hans J, Hause B, Strack D et al (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-D-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol 134(2):614–624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harada E, Choi YE, Tsuchisaka A et al (2001) Transgenic tobacco plants expressing a rice cysteine synthase gene are tolerant to toxic levels of cadmium. J Plant Physiol 158:655–661

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21(2):79–102

    Article  CAS  Google Scholar 

  • Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Hause B, Fester T (2005) Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221(2):184–196

    Article  CAS  PubMed  Google Scholar 

  • Hause B, Maier W, Miersch O et al (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130(3):1213–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He ZQ, He CX, Zhang ZB et al (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloid Surf B 59(2):128–133

    Article  CAS  Google Scholar 

  • Hetrick BA, Wilson GW, Figge DA (1994) The influence of mycorrhizal symbiosis and fertilizer amendments on establishment of vegetation in heavy metal mine spoil. Environ Pollut 86:171–179. doi:10.1016/0269-7491(94)90188-0

    Article  CAS  PubMed  Google Scholar 

  • Hollander-Czytko H, Grabowski J, Sandorf I et al (2005) Tocopherol content and activities of tyrosine aminotransferase and cystine lyase in Arabidopsis under stress conditions. J Plant Physiol 162(7):767–770

    Article  PubMed  CAS  Google Scholar 

  • Huang LL, Yang C, Zhao Y et al (2008) Antioxidant defenses of mycorrhizal fungus infection against SO2-induced oxidative stress in Avena nuda seedlings. Bull Environ Contam Toxicol 81:440–444

    Article  CAS  PubMed  Google Scholar 

  • Huang YM, Srivastava AK, Zou YN et al (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  PubMed Central  Google Scholar 

  • Jiang QY, Zhuo F, Long SH et al (2016) Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd added soils? Sci Rep 6:21805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126(3):1055–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Dames JF, Gupta A et al (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 

  • Kwak JM, Mori IC, Pei ZM et al (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22(11):2623–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7(3):323–328

    Article  CAS  PubMed  Google Scholar 

  • Lambais MR, Ríos-Ruiz WF, Andrade RM (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol 160(2):421–428

    Article  CAS  Google Scholar 

  • Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137(4):1319–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larson A (1998) The antioxidants of higher plants. Phytochemistry 27:969–978

    Article  Google Scholar 

  • Lázaro JJ, Jiménez A, Camejo D et al (2013) Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front Plant Sci 4:460

    Article  PubMed  PubMed Central  Google Scholar 

  • Li T, Liu RJ, He XH et al (2012) Enhancement of superoxide dismutase and catalase activities and salt tolerance of euhalophyte Suaeda salsa L. by mycorrhizal fungus Glomus mosseae. Pedosphere 22(2):217–224

    Article  CAS  Google Scholar 

  • Li T, Hu YJ, Hao ZP et al (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197(2):617–630

    Article  CAS  PubMed  Google Scholar 

  • Linderman RG (2000) Effects of mycorrhizas on plant tolerances to diseases. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 345–365

    Chapter  Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2 −, H2O2, and ·OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136(2):3114–3123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu A, Chen S, Wang M et al (2016) Arbuscular mycorrhizal fungus alleviates chilling stress by boosting redox poise and antioxidant potential of tomato seedlings. J Plant Growth Regul 35(1):109–120

    Article  CAS  Google Scholar 

  • Loreto F, Pinelli P, Manes F et al (2004) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of mono-terpenes emitted by Quercus ilex leaves. Tree Physiol 24:361–367

    Article  CAS  PubMed  Google Scholar 

  • Manoharan PT, Shanmugaiah V, Balasubramanian N et al (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata L. grown under different water stress conditions. Eur J Soil Biol 46:151–156

    Article  Google Scholar 

  • Marulanda A, Porcel R, Barea JM et al (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought-tolerant or drought-sensitive Glomus species. Microb Ecol 54:543–552. doi:10.1007/s00248-007-9237-y

    Article  CAS  PubMed  Google Scholar 

  • Matamoros MA, Dalton DA, Ramos J et al (2003) Biochemistry and molecular biology of antioxidants in the rhizobia–legume symbiosis. Plant Physiol 133(2):499–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165(13):1390–1403

    Article  CAS  PubMed  Google Scholar 

  • Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Adv 29(6):645–653

    Article  CAS  PubMed  Google Scholar 

  • Ni QD, Zou YN, Wu QS et al (2013) Increased tolerance of citrus (Citrus tangerina) seedlings to soil water deficit after mycorrhizal inoculation: changes in antioxidant enzyme defense system. Not Bot Horti Agrobot 41(2):524–529

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35(2):454–484

    Article  CAS  PubMed  Google Scholar 

  • Ordoñez NM, Marondedze C, Thomas L et al (2014) Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots. FEBS Lett 588(6):1008–1015

    Article  PubMed  CAS  Google Scholar 

  • Palma JM, Longa MA, Arines J et al (1993) Superoxide dismutase in vesicular arbuscular mycorrhizal red clover plants. Physiol Plant 87(1):77–83

    Article  CAS  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nat Rev Microbiol 6:763–775

    Article  CAS  PubMed  Google Scholar 

  • Pauly N, Pucciariello C, Mandon K et al (2006) Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. J Exp Bot 57(8):1769–1776

    Article  CAS  PubMed  Google Scholar 

  • Peñuelas J, Munné-Bosch S (2005) Isoprenoids: an evolutionary pool for photo-protection. Trends Plant Sci 10(4):166–169

    Article  PubMed  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(403):1743–1750

    Article  CAS  PubMed  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. doi:10.1046/j.1469-8137.2003.00658.x

    Article  CAS  Google Scholar 

  • Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology – a charging concept. Plant Physiol Biochem 48(5):292–300

    Article  CAS  PubMed  Google Scholar 

  • Puppo A, Groten K, Bastian F et al (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165(3):683–701

    Article  CAS  PubMed  Google Scholar 

  • Quan LJ, Zhang B, Shi WW et al (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50(1):2–18

    Article  CAS  PubMed  Google Scholar 

  • Rao ASVC, Reddy AR (2008) Glutathione reductase: a putative redox regulatory system in plant cells. In: Khan NA, Singh S, Umar S (eds) Sulfur assimilation and abiotic stresses in plants. Springer, Dordrecht, pp 111–147

    Chapter  Google Scholar 

  • Reddy AR, Raghavendra AS (2006) Photooxidative stress. In: Madhava Rao KV, Raghavendra AS, Reddy KJ (eds) Physiology and molecular biology of stress tolerance in plants. Springer, Dordrecht, pp 157–186

    Chapter  Google Scholar 

  • Rouhier N, Jacquot JP (2008) Getting sick may help plants overcome abiotic stress. New Phytol 180(4):738–741

    Article  CAS  PubMed  Google Scholar 

  • Ruis H, Koller F (1997) Biochemistry, molecular biology, and cell biology of yeast and fungal catalases. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 309–342

    Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress, new perspectives for molecular studies. Mycorrhiza 13:309–317. doi:10.1007/s00572-003-0237-6

    Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM et al (2001a) Cloning of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorrhizal symbiosis and by drought stress. J Exp Bot 52(364):2241–2242

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM et al (2001b) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151(2):493–502. doi:10.1046/j.0028-646x.2001.00196.x

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Azcón C et al (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63(11):4033–4044

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Sánchez M, Aroca R, Mun ̃oz Y et al (2010) The Arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167(11):862–869

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Sánchez M, Armada E, Munoz Y et al (2011) Azospirillum and arbuscular mycorrhizal colonization enhanced rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 168(10):1031–1037

    Article  PubMed  CAS  Google Scholar 

  • Salzer P, Corbiere H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza forming fungus Glomus intraradices. Planta 208(3):319–325

    Article  CAS  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53(372):1351–1365. doi:10.1093/jexbot/53.372.1351

    PubMed  Google Scholar 

  • Serbinonva EA, Packer L (1994) Antioxidant properties of tocopherol and tocotrienol. Methods Enzymol 234:354–367

    Article  Google Scholar 

  • Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J Plant Physiol 164(9):1144–1151

    Article  CAS  PubMed  Google Scholar 

  • Sharma P, Jha AB, Dubey RS (2010) Oxidative stress and antioxidative defense system in plants growing under abiotic stresses. In: Pessarakli M (ed) Handbook of plant and crop stress, 3rd edn. Taylor and Francis, Boca Raton, pp 89–138

    Google Scholar 

  • Sharma P, Jha AB, Dubey RS et al (2012) Reactive oxygen species, oxidative damage and antioxidative defense mechanism in plants under stressful conditions. J Bot. doi:10.1155/2012/217037

    Google Scholar 

  • Shim IS, Momose Y, Yamamoto A (2003) Inhibition of catalase activity by oxidative stress and its relationship to salicylic acid accumulation in plants. Plant Growth Regul 39(3):285–292

    Article  CAS  Google Scholar 

  • Singh A (2007) Molecular basis of plant–symbiotic fungi interaction: an overview. Sci World J 5(5):115–131

    Google Scholar 

  • Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6(2):175–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Song F, Song G, Airong Dong A et al (2011) Regulatory mechanisms of host plant defense responses to arbuscular mycorrhiza. Acta Ecol Sin 31:322–327

    Article  Google Scholar 

  • Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol 172(1):22–34

    Article  CAS  PubMed  Google Scholar 

  • Subramanian KS, Virgine Tenshia JS, Jayalakshmi K et al (2011) Antioxidant enzyme activities in arbuscular mycorrhizal (Glomus intraradices) fungus inoculated and non-inoculated maize plants under zinc deficiency. Indian J Microbiol 51(1):37–43

    Article  PubMed  PubMed Central  Google Scholar 

  • Takemoto D, Tanaka A, Scott B (2007) NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44:1065–1076

    Article  CAS  PubMed  Google Scholar 

  • Tan SY, Jiang QY, Zhuo F et al (2015) Effect of inoculation with Glomus versiforme on cadmium accumulation, antioxidant activities and phytochelatins of Solanum photeinocarpum. PLoS One 10(7):e0132347. doi:10.1371/journal.pone.0132347

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thomas CE, McLean R, Parker RA et al (1992) Ascorbate and phenolic antioxidant interactions in prevention of liposomal oxidation. Lipids 27(7):543–550

    Article  CAS  PubMed  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P et al (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193(3):755–769

    Article  CAS  PubMed  Google Scholar 

  • Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rend Lincei 19(4):325–346

    Article  Google Scholar 

  • Wang S, Wan C, Wang Y et al (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistance plants of the Alxa Desert, China. J Arid Environ 56:525–539

    Article  Google Scholar 

  • Watanabe K, Suzuki K, Kitamura S (2006) Characterization of a GDP-D-mannose 3″, 5″-epimerase from rice. Phytochemistry 67(4):338–346

    Article  CAS  PubMed  Google Scholar 

  • Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163(4):417–425

    Article  CAS  PubMed  Google Scholar 

  • Wu QS, Zou YN (2009) Mycorrhiza has a direct effect on reactive oxygen metabolism of drought-stressed citrus. Plant Soil Environ 55:436–442

    CAS  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. doi:10.1016/j.jplph.2005.09.001

    Article  CAS  PubMed  Google Scholar 

  • Wu QS, Zou YN, Abd-Allah EF (2014) Mycorrhizal association and ROS in plants. In: Ahmad P (ed) Oxidative damage to plants. Elsevier Inc., Amsterdam, pp 453–475. doi:http://dx.doi.org/10.1016/B978-0-12-799963-0.00015-0

  • Yang Y, Han X, Liang Y et al (2015) The combined effects of Arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS One 10(12):e0145726. doi:10.1371/journal.pone.0145726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang RQ, Zhu HH, Zhao HQ et al (2013) Arbuscular mycorrhizal fungal inoculation increases phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signaling pathways. J Plant Physiol 170(1):74–79

    Article  CAS  PubMed  Google Scholar 

  • Zou YN, Wu QS, Huang YM et al (2013) Mycorrhizal-mediated lower proline accumulation in Poncirus trifoliata under water deficit derives from the integration of inhibition of proline synthesis with increase of proline degradation. PLoS One 8(11):e80568. doi:10.1371/journal.pone.0080568

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zou YN, Huang YM, Wu QS et al (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(2):143–152

    Article  CAS  PubMed  Google Scholar 

  • Zyracka E, Zadrag R, Koziol S et al (2005) Yeast as a biosensor for antioxidants: simple growth tests employing a Saccharomyces cerevisiae mutant defective in superoxide dismutase. Acta Biochim Pol 52(3):679–684

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, University of Delhi, Delhi, 110007, India

    Rupam Kapoor & Neeraja Singh

Authors
  1. Rupam Kapoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neeraja Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rupam Kapoor .

Editor information

Editors and Affiliations

  1. College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei, China

    Qiang-Sheng Wu

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Cite this chapter

Kapoor, R., Singh, N. (2017). Arbuscular Mycorrhiza and Reactive Oxygen Species. In: Wu, QS. (eds) Arbuscular Mycorrhizas and Stress Tolerance of Plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-4115-0_10

Download citation

Publish with us

Policies and ethics

Search

Navigation