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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

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Abstract

Mechanisms of arbuscular mycorrhiza (AM)-induced lower oxidative burst of host plants under drought stress (DS) are not elucidated. A noninvasive microtest technology (NMT) was used to investigate the effects of Funneliformis mosseae on net fluxes of root hydrogen peroxide (H2O2) and calcium ions (Ca2+) in 5-month-old Poncirus trifoliata, in combination with catalase (CAT) and superoxide dismutase (SOD) activities as well as tissue superoxide radical (O2 •−) and H2O2 concentrations under DS and well-watered (WW) conditions. A 2-month DS (55 % maximum water holding capacity of growth substrates) significantly inhibited AM fungal root colonization, while AM symbiosis significantly increased plant biomass production, irrespective of water status. F. mosseae inoculation generally increased SOD and CAT activity but decreased O2 •− and H2O2 concentrations in leaves and roots under WW and DS. Compared with non-AM seedlings, roots of AM seedlings had significantly higher net H2O2 effluxes and net Ca2+ influxes, especially in the meristem zone, but lower net H2O2 efflux in the elongation zone. Net Ca2+ influxes into roots were significantly positively correlated with root net H2O2 effluxes but negatively with root H2O2 concentrations. Results from this study suggest that AM-induced lower oxidative burst is related with higher antioxidant enzyme activities, root net H2O2 effluxes, and Ca2+ influxes under WW and DS.

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References

  • Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169:704–709

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Jamsheed S, Hameed A, Rasool S, Sharma I, Azooz MM, Hasanuzzaman M (2014) Oxidative damage and antioxidants in plants. In: Ahmad P (ed) Oxidative damage to plants. Elsevier Inc., New York, pp 345–367

    Chapter  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 

  • Allen MF (2011) Linking water and nutrients through the vadose zone: a fungal interface between the soil and plant systems. J Arid Land 3:155–163

    Article  Google Scholar 

  • Anjum SA, Farooq M, Xiee XY, Liu XJ, Ijaz MF (2012) Antioxidant defense system and proline accumulation enables hot pepper to perform better under drought. Sci Hortic 140:66–73

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM (2009) Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol Plant Microbe Interact 22:1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Bagheri V, Shamshiri MH, Shirani H, Roosta H (2012) Nutrient uptake and distribution in mycorrhizal pistachio seedlings under drought stress. J Agric Sci Technol 14:1591–1604

    Google Scholar 

  • Bajji M, Lutts S, Kinet JM (2001) Water deficit effects on solute contribution to osmotic adjustment as a function of leaf ageing in three durum wheat (Triticum durum Desf.) cultivars performing differently in arid conditions. Plant Sci 160:669–681

    Article  CAS  PubMed  Google Scholar 

  • Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, Ruiz-Lonazo JM (2012) Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot 109:1009–1017

    Article  PubMed Central  PubMed  Google Scholar 

  • Bienert GP, Møller ALB, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192

    Article  CAS  PubMed  Google Scholar 

  • Bompadre MJ, Silvani VA, Bidondo LF, Ríos de Molina MC, Colombo RP, Pardo AG, Godeas AM (2014) Arbuscular mycorrhizal fungi alleviate oxidative stress in pomegranate plants growing under different irrigation conditions. Botany 92:187–193

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fidelibus MW, Martin CA, Stutz JC (2001) Geographic isolates of Glomus increase root growth and whole-plant transpiration of Citrus seedlings grown with high phosphorus. Mycorrhiza 10:231–236

    Article  Google Scholar 

  • Gao HB, Zhang SJ, Shen YB (2012) Regurgitant from Orgyia ericae Germar induces calcium influx and accumulation of hydrogen peroxide in Ammopiptanthus mongolicus (Maxim. ex Kom.) Cheng f. cells. Acta Ecol Sin 32:6520–6526 (in Chinese with English abstract)

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goldblith SA, Proctor BE (1950) Photometric determination of catalase activity. J Biol Chem 187:705–709

    CAS  PubMed  Google Scholar 

  • Hu X, Jiang M, Zhang J, Zhang A, Lin F, Tan M (2007) Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize (Zea mays) plants. New Phytol 173:27–38

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2003) Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defense in leaves of maize seedlings. Plant Cell Environ 26:929–939

    Article  CAS  PubMed  Google Scholar 

  • Kong XQ, Luo Z, Dong HZ, Egrinya Eneji A, Li WJ (2012) Effects of non-uniform root zone salinity on water use, Na+ recirculation, and Na+ and H+ flux in cotton. J Exp Bot 63:2105–2116

    Article  CAS  PubMed Central  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 160:421–428

    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 137:1319–1330

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee YJ (2004) Subcellular distribution of P and Ca in arbuscular mycorrhizal plant: an X-ray microanalytical study. Agric Chem Biotechnol 47:189–193

    CAS  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 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Gianinazzi-Pearson V, Arnould C, Wipf D, Zhao B, van Tuinen D (2013) Fungal genes related to calcium homeostasis and signalling are upregulated in symbiotic arbuscular mycorrhiza interactions. Fungal Biol 117:22–31

    Article  CAS  PubMed  Google Scholar 

  • Lu YJ, Li NY, Sun J, Hou PC, Jing XS, Zhu HP, Deng SR, Han YS, Huang XX, Ma XJ, Zhao N, Zhang YH, Shen X, Chen SL (2013) Exogenous hydrogen peroxide, nitric oxide and calcium mediate root ion fluxes in two non-secretor mangrove species subjected to NaCl stress. Tree Physiol 33:81–95

    Article  PubMed  Google Scholar 

  • Maiquetía M, Cáceres A, Herrera A (2009) Mycorrhization and phosphorus nutrition affect water relations and CAM induction by drought in seedlings of Clusia minor. Ann Bot 103:525–532

    Article  PubMed Central  PubMed  Google Scholar 

  • Marten H, Hyun T, Gomi K, Seo S, Hedrich R, Roelfsema MRG (2008) Silencing of NtMPK4 impairs CO2-induced stomatal closure, activation of anion channels and cytosolic Ca2+ signals in Nicotiana tabacum guard cells. Plant J 55:698–708

    Article  CAS  PubMed  Google Scholar 

  • Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673–681

    Article  CAS  PubMed Central  PubMed  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 

  • Ortas I, Ustuner O (2014) Determination of different growth media and various mycorrhizae species on citrus growth and nutrient uptake. Sci Hortic 166:84–90

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pedroso FKJV, Prudent DA, Bueno ACR, Machado EC, Ribeiro RV (2014) Drought tolerance in citrus trees is enhanced by rootstock-dependent changes in root growth and carbohydrate availability. Environ Exp Bot 101:26–35

    Article  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  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 55:158–161

    Article  Google Scholar 

  • Porterfield DM (2007) Measuring metabolism and biophysical flux in the tissue, cellular and sub-cellular domains: recent developments in self-referencing amperometry for physiological sensing. Biosens Bioelectron 22:1186–1196

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Riley R, Corradi N (2013) Searching for clues of sexual reproduction in the genomes of arbuscular mycorrhizal fungi. Fungal Ecol 6:44–49

    Article  Google Scholar 

  • Roldán A, Diaz-Wivancos P, Harnández JA, Carrasco L, Caravaca F (2008) Superoxide dismutase and total peroxidase activities in relation to drought recovery performance of mycorrhizal shrub seedlings grown in an amended semiarid soil. J Plant Physiol 165:715–722

    Article  PubMed  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 208:319–325

    Article  CAS  Google Scholar 

  • Santos CM, Verissimo V, de Lins Wanderley Filho HC, Ferreira VM, da Silva Cavalcante PG, Rolim EV, Endres L (2013) Seasonal variations of photosynthesis, gas exchange, quantum efficiency of photosystem II and biochemical responses of Jatropha curcas L. grown in semi-humid and semi-arid areas subject to water stress. Indust Crop Prod 41:203–213

    Article  Google Scholar 

  • Sekmen AH, Ozgur R, Uzilday B, Turkan I (2014) Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environ Exp Bot 99:141–149

    Article  CAS  Google Scholar 

  • Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrient and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Sun J, Wang MJ, Ding MQ, Deng SR, Liu MQ, Lu CF, Zhou XY, Shen X, Zheng XJ, Zhang ZK, Song J, Hu ZM, Xu Y, Chen SL (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958

    Article  CAS  PubMed  Google Scholar 

  • Tang TH, Chang CT, Wang HJ, Erickson JD, Reichard RA, Martin AG, Shannon EK, Martin AL, Huang YW, Aronstam RS (2013) Oxidative stress disruption of receptor-mediated calcium signaling mechanisms. J Biomed Sci 20:48. doi:10.1186/1423-0127-20-48

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian YH, Lei YB, Zheng YL, Cai ZQ (2013) Synergistic effect of colonization with arbuscular mycorrhizal fungi improves growth and drought tolerance of Plukenetia volubilis seedlings. Acta Physiol Plant 35:687–696

    Article  CAS  Google Scholar 

  • Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei Dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young PW, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci 110:20117–20122

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Twig G, Jung SK, Messerli MA, Smith PJS, Shirihai OS (2001) Real-time detection of reactive oxygen intermediates from single microglial cells. Biol Bull 201:261–262

    Article  CAS  PubMed  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Wang AG, Luo GH (1990) Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. Plant Physiol Commun 26:55–57 (in Chinese with English abstract)

    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

    Article  CAS  PubMed  Google Scholar 

  • Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87

    Article  CAS  Google Scholar 

  • Xiao JX, Yang H, Zhang SL (2012) Effects of arbuscular mycorrhizal fungus on net ion fluxes in the roots of trifoliate orange (Poncirus trifoliata) and mineral nutrition in seedlings under zinc contamination. Acta Ecol Sin 32:2127–2134 (in Chinese with English abstract)

    Article  CAS  Google Scholar 

  • Xu H, Cooke JEK, Zwiazek JJ (2013) Phylogenetic analysis of fungal aquaporins provides insight into their possible role in water transport of mycorrhizal associations. Botany 91:495–504

    Article  CAS  Google Scholar 

  • Zhu XC, Song FB, Liu SQ (2011) Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content and activity of antioxidant system. J Food Agric Environ 9:583–587

    Google Scholar 

  • Zou YN, Wu QS, Huang YM, Ni QD, He XH (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:e80568. doi:10.1371/journal.pone.0080568

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (31101513) and the Excellent Young Teacher Research Support Program of Yangtze University (cyq201326). We thank anonymous reviewers for their valuable comments on the manuscript.

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Authors and Affiliations

  1. College of Horticulture and Gardening/Institute of Root Biology, Yangtze University, 88 Jingmi Road, Jingzhou, Hubei, 434025, People’s Republic of China

    Ying-Ning Zou, Yong-Ming Huang & Qiang-Sheng Wu

  2. Department of Environmental Sciences, University of Sydney, Eveleigh, NSW, 2015, Australia

    Xin-Hua He

  3. School of Plant Biology, University of Western Australia, Crawley, WA, 6009, Australia

    Xin-Hua He

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Zou, YN., Huang, YM., Wu, QS. et al. 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 (2015). https://doi.org/10.1007/s00572-014-0598-z

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