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Reactive Oxygen Species (ROS) Metabolism and Signaling in Plant-Mycorrhizal Association Under Biotic and Abiotic Stress Conditions

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Mycorrhiza - Eco-Physiology, Secondary Metabolites, Nanomaterials

Abstract

A stringent regulation between reactive oxygen species (ROS) generation and scavenging is an essential process that helps a plant to adaptively utilize ROS as a primary defense molecule against biotic and abiotic stress condition. ROS at lower level primarily acts as a signaling molecule regulating plant cellular processes that include plant-microbe interaction. However, ROS generated at higher levels often leads to the inhibition of cellular processes, thus consequently leading a detrimental effect in plant growth and homeostasis. Rhizosphere being the “chemical space” around the roots which proves to be biologically active zone for plant-microbe interactions forms a link responsible for mutual signaling in each of the partners. Moreover plant fitness is said to be enhanced by these symbiotic mycorrhizal associations which are known to alleviate detrimental effects caused by environmental stresses thereby enhancing overall plant growth and development. This present chapter summarizes a precise interlink between biotic-abiotic stressed plants and its mycorrhizal association linking ROS modulation with plant signaling thereby establishing a link between stress tolerance and ROS metabolism. The literature reviewed herein will help to delineate the basic mechanism of ROS signaling, by ascertaining the physiological responses via altering the ROS metabolism, in mycorrhizal-associated stressed plants. This will ultimately help in designing innovative strategies to improve the overall plant productivity under stressful regimes.

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References

  • Abadi VAJM, Sepehri M (2016) Effect of Piriformospora indica and Azotobacter chroococcum on mitigation of zinc deficiency stress in wheat (Triticum aestivum L.) Symbiosis 69:9. doi:10.1007/s13199-015-0361-z

    Article  CAS  Google Scholar 

  • Akum FN, Steinbrenner J, Biedenkopf D, Imani J, Kogel K (2015) The Piriformospora indica effector PIIN_08944 promotes the mutualistic Sebacinalean symbiosis. Front Plant Sci 6:906. doi:10.3389/fpls.2015.00906

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrio E, Marino D, Marmeys A, de Segonzac MD, Damiani I (2013) Hydrogen peroxide-regulated genes in the M. truncatula–Sinorhizobium meliloti symbiosis. New Phytol 198:190–202. doi:10.1111/nph.12120

    Article  CAS  Google Scholar 

  • Anthony RG, Khan S, Costa J, Pais MS, Bogre L (2006) The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J Biol Chem 281:37536–37546

    Article  CAS  PubMed  Google Scholar 

  • Bakshi M, Sherameti I, Johri AK, Varma A, Oelmuller R (2014) Phosphate availability affects root architecture and development, plant performance and is controlled by root-colonizing microbes. J Endocyto Cell Res 25:56–65

    Google Scholar 

  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G et al (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510

    Article  CAS  PubMed  Google Scholar 

  • Barna B, Fodor J, Harrach BD, Pogany M, Kiraly Z (2012) The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol Biochem 59:37–43

    Article  CAS  PubMed  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. doi:10.1093/jxb/ert375

    Article  CAS  PubMed  Google Scholar 

  • Behie SW, Bidochka MJ (2014) Nutrient transfer in plant–fungal symbioses. Trends Plant Sci 19:1360–1385

    Article  Google Scholar 

  • Beneventi MA, da Silva OB, de Sa MEL, Firmino AAP, de Amorim RMS, Albuquerque EVS et al (2013) Transcription profile of soybean–root-knot nematode interaction reveals a key role of phythormones in the resistance reaction. BMC Genomics 10:322. doi:10.1186/1471-2164-14-322

    Article  Google Scholar 

  • Benhiba L, Fouad MO, Essahibi A, Ghoulam C, Qaddoury A (2015) Arbuscular mycorrhizal symbiosis enhanced growth and antioxidant metabolism in date palm subjected to long-term drought. Trees 29:1725–1733

    Article  CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  CAS  PubMed  Google Scholar 

  • Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C et al (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7(5):e1002051. doi:10.1371/journal.ppat.1002051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardenas L, Quinto C (2008) Reactive oxygen species (ROS) as early signals in root hair cells responding to rhizobial nodulation factors. Plant Signal Behav 3:1–3

    Article  Google Scholar 

  • Cruz C, Fegghi Z, Martins-Loucao MA, Varma A (2013) Plant nitrogen use efficiency may be improved through symbiosis with Piriformospora indica, Chap 17. In: Varma A et al (eds) Piriformospora indica. Soil Biology 33. doi:10.1007/978-3-642-33802-1_17, Springer, Berlin, pp 285–293

  • Doty SL (2016) Plant–microbe symbiotic interactions. Plant Mol Biol 90:535. doi:10.1007/s11103-016-0470-y

    Article  CAS  PubMed  Google Scholar 

  • Espinosa F, Garrido I, Ortega A, Casimiro I, Alvarez-Tinaut MC (2014) Redox activities and ros, no and phenylpropanoids production by axenically cultured intact olive seedling roots after interaction with a mycorrhizal or a pathogenic fungus. PLoS One 9(6):e100132. doi:10.1371/journal.pone.0100132

    Article  PubMed  PubMed Central  Google Scholar 

  • Evangelisti E, Rey T, Schornack S (2014) Cross-interference of plant development and plant–microbe interactions. Curr Opin Plant Biol 20:118–126

    Article  CAS  PubMed  Google Scholar 

  • Farrar K, Bryant D, Cope-Selby N (2014) Understanding and engineering beneficial plant–microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J 12:1193–1206

    Article  PubMed  PubMed Central  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 

  • Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill JL, Monfreda C, Polasky S, Rockstrom J, Sheehan J, Siebert S, Tilman D, David P, Zaks M (2011) Solutions for a cultivated planet. Nature 478:337–342

    Article  CAS  PubMed  Google Scholar 

  • Fouad OM, Essahibi A, Benhiba L, Qaddoury A (2014) Effectiveness of arbuscular mycorrhizal fungi in the protection of olive plants against oxidative stress induced by drought. Span J Agric Res 12:763–771

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Gill R, Trivedi DK, Anjum NA, Sharma KK, Ansari MW, Johri AK, Prasad R, Pereira E, Varma A, Tuteja N (2016) Piriformospora indica: potential and significance in plant stress tolerance. Front Microbiol 7:332. doi:10.3389/fmicb.2016.00332

    Article  PubMed  PubMed Central  Google Scholar 

  • Goh C, Vallejos DFV, Nicotra AB, Mathesius U (2013) The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 39:826–839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashem A, Abd-Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D, Wirth S (2016) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23:272–281

    Article  CAS  PubMed  Google Scholar 

  • Jajic I, Sarna T, Strzalka K (2015) Senescence, stress, and reactive oxygen species. Plants 4:393–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jogawat A, Saha S, Bakshi M, Dayaman V, Kumar M, Dua M, Varma A et al (2013) Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal Behav 9:e26891. doi:10.4161/psb.26891

    Article  Google Scholar 

  • Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Tropical Agri 52:103–122

    Google Scholar 

  • Kachroo A, Robin GP (2013) Systemic signaling during plant defense. Curr Opin Plant Biol 16:527–533

    Article  CAS  PubMed  Google Scholar 

  • Kadota Y, Shirasu K, Zipfel C (2015) Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol 56:1472–1480. doi:10.1093/pcp/pcv063

    Article  CAS  PubMed  Google Scholar 

  • Kiirika LM, Schmitz U, Colditz F (2014) The alternative Medicago truncatula defense proteome of ROS-defective transgenic roots during early microbial infection. Front Plant Sci 5:341. doi:10.3389/fpls.2014.00341

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790

    Article  CAS  PubMed  Google Scholar 

  • Lahrmann U, Ding Y, Banhara A, Rath M, Hajirezaei MR, Döhlemann S, von Wirén N, Parniske M, Zuccaro A (2013) Host-related metabolic cues affect colonization strategies of a root endophyte. Proc Natl Acad Sci U S A 110:13965–13970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malla R, Prasad R, Kumari R, Giang PH, Pokharel U, Oelmueller R, Varma A (2004) Phosphorus solubilizing symbiotic fungus Piriformospora indica. Endocytobiosis Cell Res 15:579–600

    Google Scholar 

  • Mine A, Sato M, Tsuda K (2014) Toward a systems understanding of plant–microbe interactions. Front Plant Sci 5:423. doi:10.3389/fpls.2014.00423

    Article  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem FV (2011) ROS signaling: the new wave? Trends Plant Sci 16(6):300–309. doi:10.1016/j.tplants.2011.03.007

    Article  CAS  PubMed  Google Scholar 

  • Muthukumar T, Udaiyan K (2010) Growth response and nutrient utilization of Casuarina equisetifolia seedlings inoculated with bioinoculants under tropical nursery conditions. New For 40:101–118

    Article  Google Scholar 

  • Nath M, Bhatt D, Prasad R, Gill SS, Anjum NA, Tuteja N (2016) Reactive oxygen species generation-scavenging and signaling during plant-arbuscular mycorrhizal and Piriformospora indica interaction under stress condition. Front Plant Sci 7:1574. doi:10.3389/fpls.2016.01574

    Article  PubMed  PubMed Central  Google Scholar 

  • Neill SJ, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd EDG, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  PubMed  Google Scholar 

  • Petersen LN, Ingle RA, Knight MR, Denby KJ (2009) OXI1 protein kinase is required for plant immunity against Pseudomonas syringae in Arabidopsis. J Exp Bot 60:3727–3735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Prasad R, Kamal S, Sharma PK, Oelmueller R, Varma A (2013) Root endophyte Piriformospora indica DSM 11827 alters plants morphology, enhances biomass and antioxidant activity of medicinal plant Bacopa monniera. J Basic Microbiol 53:1016–1024

    Article  CAS  PubMed  Google Scholar 

  • Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R (2013) Hydrogen peroxide and nitric oxide: key regulators of the legume Rhizobium and mycorrhizal symbioses. Antioxid Redox Signal 18:2202–2219

    Article  CAS  PubMed  Google Scholar 

  • Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant 35:1039–1050

    Article  CAS  Google Scholar 

  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H et al (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861

    Article  CAS  PubMed  Google Scholar 

  • Sarkar J, Ray A, Chakraborty B, Chakraborty U (2016) Antioxidative changes in Citrus reticulata L. induced by drought stress and its effect on root colonization by arbuscular mycorrhizal fungi. Eur J Biol Res 6:1–13

    Google Scholar 

  • Schouteden N, De Waele D, Panis B, Vos CM (2015) Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6:1280. doi:10.3389/fmicb.2015.01280

    Article  PubMed  PubMed Central  Google Scholar 

  • Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531

    Article  CAS  PubMed  Google Scholar 

  • Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:187. doi:10.3389/fpls.2016.00187

    Article  PubMed  PubMed Central  Google Scholar 

  • Sherameti I, Tripathi S, Varma A, Oelmuller R (2008) The root colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress–related genes in leaves. Mol Plant Microbe Interact 21:799–807

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Song F, Li J, Fan X, Zhang Q, Chang W, Yang F, Geng G (2016) Transcriptome analysis of Glomus mosseae/Medicago sativa mycorrhiza on atrazine stress. Sci Rep 6:20245. doi:10.1038/srep20245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF et al (2013) Temporal–spatial interaction between ROS and ABA controls rapid systemic acclimation in plants. Plant Cell 25:3553–3569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tahat MM, Sijam K (2012) Mycorrhizal fungi and abiotic environmental conditions relationship. Res J Environ Sci 6:125–133

    Article  CAS  Google Scholar 

  • Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trivedi D, Srivastava A, Verma PK, Tuteja N, Gill SS (2016) Piriformospora indica: a friend in need is a friend in deed. Res Rev: J Botanical Sci 5:16–19

    Google Scholar 

  • Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Mazars C, Scheel D et al (2009a) A cell wall extract from Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59:193–206

    Article  CAS  PubMed  Google Scholar 

  • Vadassery J, Tripathi S, Prasad R, Varma A, Oelmüller R (2009b) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol 166:1263–1274

    Article  CAS  PubMed  Google Scholar 

  • Vahabi K, Sherameti I, Bakshi M, Mrozinska A, Ludwig A, Reichelt M et al (2015) The interaction of Arabidopsis with Piriformospora indica shifts from initial transient stress induced by fungus-released chemical mediators to a mutualistic interaction after physical contact of the two symbionts. BMC Plant Biol 15:58. doi:10.1186/s12870-015-0419-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Varma A, Sherameti I, Tripathi S, Prasad R et al (2012) The symbiotic fungus Piriformospora indica: review. In: Hock B (ed) Fungal associations, the mycota IX, 2nd edn. Springer, Berlin, pp 231–254

    Google Scholar 

  • Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Butehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–902

    Article  CAS  Google Scholar 

  • Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D et al (2013) Mycorrhiza-induced resistance against the root-knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Biochem 60:45–54. doi:10.1016/j.soilbio.2013.01.013

    Article  CAS  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M et al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Q, Zou Y, Abd-Allah EF (2014) Mycorrhizal association and ROS in plants. In: Ahmad P (ed) Oxidative damage to plants, Chap. 15. Academic Press, San Diego, pp 453–475. doi:10.1016/B978-0-12-799963-0.00015-0

  • Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K et al (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu E, Brosche M (2014) Salicylic acid signaling inhibits apoplastic reactive oxygen species signaling. BMC Plant Biol 14:155. doi:10.1186/1471-2229-14-155

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan J, Tsuichihara N, Etoh T, Iwai S (2007) Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant Cell Environ 30:1320–1325

    Article  CAS  PubMed  Google Scholar 

  • Ye W, Shen CH, Lin Y, Chen PJ, Xu X, Oelmuller R, Yeh KW, Lai Z (2014) Growth promotion-related miRNAs in oncidium orchid roots colonized by the endophytic fungus Piriformospora indica. PLoS One 9(1):e84920. doi:10.1371/journal.pone.0084920

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Sector 125, Noida, 201313, India

    Manoj Nath, Ram Prasad & Narendra Tuteja

  2. Department of Biotechnology, Shree Ramkrishna Institute of Computer Education and Applied Sciences, Affiliated to Veer Narmad South Gujarat University, Surat, Gujarat, 395001, India

    Deepesh Bhatt

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  1. Manoj Nath
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Correspondence to Narendra Tuteja .

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Editors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ajit Varma

  2. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ram Prasad

  3. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Narendra Tuteja

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Nath, M., Bhatt, D., Prasad, R., Tuteja, N. (2017). Reactive Oxygen Species (ROS) Metabolism and Signaling in Plant-Mycorrhizal Association Under Biotic and Abiotic Stress Conditions. In: Varma, A., Prasad, R., Tuteja, N. (eds) Mycorrhiza - Eco-Physiology, Secondary Metabolites, Nanomaterials. Springer, Cham. https://doi.org/10.1007/978-3-319-57849-1_12

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