Colonization of Piriformospora indica enhances insect herbivore resistance of rice plants through jasmonic acid- and antioxidant-mediated defense mechanisms

References

• Achatz B, Kogel K, Franken P, Waller F. 2010. Piriformospora indica mycorrhization increases grain yield by accelerating early development of barley plants. Plant Signal Behav. 5:1685–1687.
   PubMed Web of Science ®Google Scholar
• Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S. 2010. Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol. 30:161–175.
   PubMed Web of Science ®Google Scholar
• Alscher RG, Erturk N, Heath LS. 2002. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot. 53:1331–1341.
   PubMed Web of Science ®Google Scholar
• Ansari MW, Trivedi DK, Sahoo RK, Gill SS, Tuteja N. 2013. A critical review on fungi mediated plant responses with special emphasis to Piriformospora indica on improved production and protection of crops. Plant Physiol Biochem. 70:403–410.
   PubMed Web of Science ®Google Scholar
• Atia MAM, Abdeldaym EA, Abdelsattar M, Ibrahim DSS, Saleh I, Elwahab MA, Osman GH, Arif IA, Abdelaziz ME. 2020. Piriformospora indica promotes cucumber tolerance against Root-knot nematode by modulating photosynthesis and innate responsive genes. Saudi J Biol Sci. 27:279–287.
   PubMed Web of Science ®Google Scholar
• Bakshi M, Vahabi K, Bhattacharya S, Sherameti I, Varma A, Yeh KW, Baldwin I, Johri AK, Oelmüller R. 2015. WRKY6 restricts Piriformospora indica-stimulated and phosphate-induced root development in Arabidopsis. BMC Plant Biol. 15:305.
   PubMed Web of Science ®Google Scholar
• Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT. 2005. Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia. 146:234–243.
   PubMed Web of Science ®Google Scholar
• Bernaola L, Stout MJ. 2019. Effects of arbuscular mycorrhizal fungi on rice-herbivore interactions are soil-dependent. Sci Rep. 9:14037.
   PubMed Web of Science ®Google Scholar
• Botelho-Júnior S, Siqueira-Júnior CL, Jardim BC, Machado OLT, Neves-Ferreira AGC, Perales J, Jacinto T. 2008. Trypsin inhibitors in passion fruit (Passiflora f. edulis flavicarpa) leaves: accumulation in response to methyl jasmonate, mechanical wounding, and herbivory. J Agric Food Chem. 56:9404–9409.
   PubMed Web of Science ®Google Scholar
• Bütehorn B, Rhody D, Franken P. 2000. Isolation and characterisation of Pitef1 encoding the translation elongation factor EF-1α of the root endophyte Piriformospora indica. Plant Biol. 2:687–692.
   Web of Science ®Google Scholar
• Chang YA, Dai NC, Chen HJ, Tseng CH, Huang ST, Wang SJ. 2019. Regulation of rice sucrose transporter 4 gene expression in response to insect herbivore chewing. J Plant Interact. 14:525–532.
   Web of Science ®Google Scholar
• Chen HJ, Wang SJ, Chen CC, Yeh KW. 2006. New gene construction strategy in T-DNA vector to enhance expression level of sweet potato sporamin and insect resistance in transgenic Brassica oleracea. Plant Sci. 171:367–374.
   PubMed Web of Science ®Google Scholar
• Chen YL, Lee CY, Cheng KT, Chang WH, Huang RN, Nam HG, Chen YR. 2014. Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. Plant Cell. 26:4135–4148.
   PubMed Web of Science ®Google Scholar
• Chu C, Lee TM. 1989. The relationship between ethylene biosynthesis and chilling tolerance in seedlings of rice (Oryza sativa). Bot Bull Acad Sinica (Taiwan. 30:263–273.
   Google Scholar
• Cosme M, Lu J, Erb M, Stout MJ, Franken P, Wurst S. 2016. A fungal endophyte helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling. New Phytol. 211:1065–1076.
   PubMed Web of Science ®Google Scholar
• Daneshkhah R, Cabello S, Rozanska E, Sobczak M, Grundler FM, Wieczorek K, Hofmann J. 2013. Piriformospora indica antagonizes cyst nematode infection and development in Arabidopsis roots. J Exp Bot. 64:3763–3774.
   PubMed Web of Science ®Google Scholar
• Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R. 2005. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell. 17:268–281.
   PubMed Web of Science ®Google Scholar
• Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH. 2006. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci USA. 103:18450–18457.
   PubMed Web of Science ®Google Scholar
• Edilberto D. 2013. Standard evaluation system for rice, 5th ed. Los Banos: International Rice Research Institute. p. 31.
   Google Scholar
• Foster JG, Hess JL. 1980. Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol. 66:482–487.
   PubMed Web of Science ®Google Scholar
• Fukumoto K, Alamgir KM, Yamashita Y, Mori IC, Matsuura H, Galis I. 2013. Response of rice to insect elicitors and the role of OsJAR1 in wound and herbivory-induced JA-Ile accumulation. J Integr Plant Biol. 55:775–784.
   PubMed Web of Science ®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.
   PubMed Web of Science ®Google Scholar
• Guo H, Glaeser SP, Alabid I, Imani J, Haghighi H, Kämpfer P, Kogel KH. 2017. The abundance of endofungal bacterium Rhizobium radiobacter (syn. Agrobacterium tumefaciens) increases in its fungal host Piriformospora indica during the tripartite Sebacinalean symbiosis with higher plants. Front Microbiol. 8:629.
   PubMed Web of Science ®Google Scholar
• Han Y, Lei W, Wen L, Hou M. 2015. Silicon-mediated resistance in a susceptible rice variety to the rice leaf folder, Cnaphalocrocis medinalis Guenée (Lepidoptera: Pyralidae). PLoS ONE. 10:e0120557.
   PubMed Web of Science ®Google Scholar
• Han Y, Li P, Gong S, Yang L, Wen L, Hou M. 2016. Defense responses in rice induced by silicon amendment against infestation by the leaf folder Cnaphalocrocis medinalis. PLoS ONE. 11:e0153918.
   PubMed Web of Science ®Google Scholar
• Heath RL, Packer L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 125:189–198.
   PubMed Web of Science ®Google Scholar
• Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A. 2012. Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol. 196:520–534.
   PubMed Web of Science ®Google Scholar
• Hill DS. 1983. Agricultural insect pests of the tropics and their control. Cambridge, MA, USA: Cambridge University Press.
   Google Scholar
• Hill T, Kafer E. 2001. Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions. Fungal Genet Newsl. 48:20–21.
   Google Scholar
• Hodges DM, Forney CF, Wismer WV. 2001. Antioxidant responses in harvested leaves of two cultivars of spinach differing in senescence rates. J Am Soc Hortic Sci. 126:611–617.
   Web of Science ®Google Scholar
• Hoffmann D, Vierheilig H, Riegler P, Schausberger P. 2009. Arbuscular mycorrhizal symbiosis increases host plant acceptance and population growth rates of the two-spotted spider mite Tetranychus urticae. Oecologia. 158:663–671.
   PubMed Web of Science ®Google Scholar
• Huot B, Yao J, Montgomery BL, He SY. 2014. Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant. 7:1267–1287.
   PubMed Web of Science ®Google Scholar
• Jiang W, Pan R, Wu C, Xu L, Abdelaziz ME, Oelmüller R, Zhang W. 2020. Piriformospora indica enhances freezing tolerance and post-thaw recovery in Arabidopsis by stimulating the expression of CBF genes. Plant Signal Behav. 15:1745472.
   PubMed Web of Science ®Google Scholar
• Jogawat A, Vadassery J, Verma N, Oelmüller R, Dua M, Nevo E, Johri AK. 2016. PiHOG1, a stress regulator MAP kinase from the root endophyte fungus Piriformospora indica, confers salinity stress tolerance in rice plants. Sci Rep. 16(6):36765.
   Google Scholar
• Koiwa H, Bressan RA, Hasegawa PM. 1997. Regulation of protease inhibitors and plant defense. Trends Plant Sci. 2:379–384.
   Web of Science ®Google Scholar
• Lata R, Chowdhury S, Gond SK, Jr WJ. 2018. Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol. 66:268–276.
   PubMed Web of Science ®Google Scholar
• Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, Oelmüller R, Yeh KW. 2011. Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol Plant Microbe Interact. 24:421–431.
   PubMed Web of Science ®Google Scholar
• Li Q, Kuo YW, Lin KH, Huang W, Deng C, Yeh KW, Chen SP. 2021. Piriformospora indica colonization increases the growth, development, and herbivory resistance of sweet potato (Ipomoea batatas L.). Plant Cell Rep. 40:339–350.
   PubMed Web of Science ®Google Scholar
• Li R, Wang M, Wang Y, Schuman MC, Weinhold A, Schäfer M, Jiménez-Alemán GH, Barthel A, Baldwin IT. 2017a. Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco. Proc Natl Acad Sci USA. 114:E7205–E7214.
   PubMed Web of Science ®Google Scholar
• Li Z, Han X, Song X, Zhang Y, Jiang J, Han Q, Liu M, Qiao G, Zhuo R. 2017b. Overexpressing the Sedum alfredii Cu/Zn superoxide dismutase increased resistance to oxidative stress in transgenic Arabidopsis. Front Plant Sci. 8:1010.
   PubMed Web of Science ®Google Scholar
• Liu H, Senthilkumar R, Ma G, Zou Q, Zhu K, Shen X, Tian D, Hua MS, Oelmüller R, Yeh KW. 2019. Piriformospora indica-induced phytohormone changes and root colonization strategies are highly host-specific. Plant Signal Behav. 14:1632688.
   PubMed Web of Science ®Google Scholar
• Liu X, Li J, Xu L, Wang Q, Lou Y. 2018. Expressing OsMPK4 impairs plant growth but enhances the resistance of rice to the striped stem borer Chilo suppressalis. Int J Mol Sci. 19:1182.
   PubMed Web of Science ®Google Scholar
• Lokya V, Swathi M, Mallikarjuna N, Padmasree K. 2020. Response of midgut trypsin- and chymotrypsin-like proteases of Helicoverpa armigera larvae upon feeding with peanut BBI: biochemical and biophysical characterization of PnBBI. Front Plant Sci. 11:266.
   PubMed Web of Science ®Google Scholar
• Lu J, Robert CAM, Riemann M, Cosme M, Mène-Saffrané L, Massana J, Stout MJ, Lou Y, Gershenzon J, Erb M. 2015. Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol. 167:1100–1116.
   PubMed Web of Science ®Google Scholar
• Lyons R, Manners JM, Kazan K. 2013. Jasmonate biosynthesis and signaling in monocots: a comparative overview. Plant Cell Rep. 32:815–827.
   PubMed Web of Science ®Google Scholar
• Maruta T, Inoue T, Noshi M, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S. 2012. Cytosolic ascorbate peroxidase 1 protects organelles against oxidative stress by wounding- and jasmonate-induced H2O2 in Arabidopsis plants. Biochim Biophys Acta. 20:1901–1907.
   Google Scholar
• Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22:867–880.
   Web of Science ®Google Scholar
• Orozco-Cardenas M, Ryan CA. 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA. 96:6553–6557.
   PubMed Web of Science ®Google Scholar
• Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell. 13:179–191.
   PubMed Web of Science ®Google Scholar
• Padmavathi Ch, Katti G, Padmakumari AP, Voleti SR, Subba Rao LV. 2013. The effect of leaffolder Cnaphalocrocis medinalis (Guenee) [Lepidoptera: Pyralidae] injury on the plant physiology and yield loss in rice. J Appl Entomol. 137:249-256.
   Web of Science ®Google Scholar
• Pan Z, Camara B, Gardner HW, Backhaus RA. 1998. Aspirin inhibition and acetylation of the plant cytochrome P450, allene oxide synthase, resembles that of animal prostaglandin endoperoxide H synthase. J Biol Chem. 273:18139–18145.
   PubMed Web of Science ®Google Scholar
• Paoletti F, Aldinucci D, Mocali A, Caparrini A. 1986. A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem. 154:536–541.
   PubMed Web of Science ®Google Scholar
• Real-Santillán RO, Del-Val E, Cruz-Ortega R, Contreras-Cornejo HÁ, González-Esquivel CE, Larsen J. 2019. Increased maize growth and P uptake promoted by arbuscular mycorrhizal fungi coincide with higher foliar herbivory and larval biomass of the Fall Armyworm Spodoptera frugiperda. Mycorrhiza. 29:615–622.
   PubMed Web of Science ®Google Scholar
• Riemann M, Riemann M, Takano M. 2008. Rice JASMONATE RESISTANT 1 is involved in phytochrome and jasmonate signaling. Plant Cell Environ. 31:783–792.
   PubMed Web of Science ®Google Scholar
• Rizzo E, Sherman T, Manosalva P, Gomez SK. 2020. Assessment of local and systemic changes in plant gene expression and aphid responses during potato interactions with arbuscular mycorrhizal fungi and potato aphids. Plants (Basel). 9:82.
   PubMedGoogle Scholar
• Saddique MAB, Ali Z, Khan AS, Rana IA, Shamsi IH. 2018. Inoculation with the endophyte Piriformospora indica significantly affects mechanisms involved in osmotic stress in rice. Rice. 11:34.
   PubMed Web of Science ®Google Scholar
• Schmelz EA, Alborn HT, Tumlinson JH. 2003. Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Plant Physiol. 117:403–412.
   Google Scholar
• Schoenherr AP, Rizzo E, Jackson N, Manosalva P, Gomez SK. 2019. Mycorrhiza-induced resistance in potato involves priming of defense responses against cabbage looper (Noctuidae: Lepidoptera). Environ Entomol. 48:370–381.
   PubMed Web of Science ®Google Scholar
• Senthilkumar R, Cheng CP, Yeh KW. 2010. Genetically pyramiding protease-inhibitor genes for dual broad-spectrum resistance against insect and phytopathogens in transgenic tobacco. Plant Biotechnol J. 8:65–75.
   PubMed Web of Science ®Google Scholar
• Shamsi TN, Parveen R, Fatima S. 2016. Characterization, biomedical and agricultural applications of protease inhibitors: A review. Int J Biol Macromol. 91:1120–1133.
   PubMed Web of Science ®Google Scholar
• Sherameti I, Tripathi S, Varma A, Oelmüller 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.
   PubMed Web of Science ®Google Scholar
• Shimizu T, Miyamoto K, Miyamoto K, Minami E, Nishizawa Y, Iino M, Nojiri H, Yamane H, Okada K. 2013. OsJAR1 contributes mainly to biosynthesis of the stress-induced jasmonoyl-isoleucine involved in defense responses in rice. Biosci Biotechnol Biochem. 77:1556–1564.
   PubMed Web of Science ®Google Scholar
• Shulaev V, Oliver DJ. 2006. Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol. 141:367–372.
   PubMed Web of Science ®Google Scholar
• Singh PK, Nag A, Arya P, Kapoor R, Singh A, Jaswal R, Sharma TR. 2018. Prospects of understanding the molecular biology of disease resistance in rice. Int J of Mol Sci. 19:1141.
   PubMed Web of Science ®Google Scholar
• Song YY, Ye M, Li CY, Wang RL, Wei XC, Luo SM, Zeng RS. 2013. Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol. 9:1036–1044.
   Google Scholar
• Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B. 2010. Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol. 167:1009–1017.
   PubMed Web of Science ®Google Scholar
• Suza WP, Staswick PE. 2008. The role of JAR1 in Jasmonoyl-L: -isoleucine production during Arabidopsis wound response. Planta. 227:1221–1232.
   PubMed Web of Science ®Google Scholar
• Tsai HJ, Shao KH, Chan MT, Cheng CP, Yeh KW, Oelmüller R, Wang SJ. 2020. Piriformospora indica symbiosis improves water stress tolerance of rice through regulating stomata behavior and ROS scavenging systems. Plant Signal. Behav. 15:1722447.
   PubMed Web of Science ®Google Scholar
• Upadhyay RK, Mattoo AK. 2018. Genome-wide identification of tomato (Solanum lycopersicum L.) lipoxygenases coupled with expression profiles during plant development and in response to methyl-jasmonate and wounding. J Plant Physiol. 231:318–328.
   PubMed Web of Science ®Google Scholar
• Varma A, Verma S, Sudha SN, Bütehorn B, Franken P. 1999. Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol. 65:2741–2744.
   PubMed Web of Science ®Google Scholar
• Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn Mycologia B, Franken P. 1998. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia. 90:896–903.
   Web of Science ®Google Scholar
• Vos IA, Verhage A, Schuurink RC, Watt LG, Pieterse CMJ, Van Wees SCM. 2013. Onset of herbivore-induced resistance in systemic tissue primed for jasmonate-dependent defenses is activated by abscisic acid. Front Plant Sci. 4:539.
   PubMed Web of Science ®Google Scholar
• Wakuta S, Suzuki E, Saburi W, Matsuura H, Nabeta K, Imai R, Matsui H. 2011. OsJAR1 and OsJAR2 are jasmonyl-l-isoleucine synthases involved in wound- and pathogen-induced jasmonic acid signalling. Biochem Biophy Res Commun. 409:634–639.
   PubMed Web of Science ®Google Scholar
• Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Wettstein D, et al. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA. 102:13386–13391.
   PubMed Web of Science ®Google Scholar
• Wang Q, Li J, Hu L, Zhang T, Zhang G, Lou Y. 2013. OsMPK3 positively regulates the JA signaling pathway and plant resistance to a chewing herbivore in rice. Plant Cell Rep. 32:1075–1084.
   PubMed Web of Science ®Google Scholar
• Wang SJ, Ho CH, Chen HW. 2011a. Rice develop wavy seminal roots in response to light stimulus. Plant Cell Rep. 30:1747–1758.
   PubMed Web of Science ®Google Scholar
• Wang SJ, Lan YC, Chen SF, Chen YM, Yeh KW. 2002. Wound-response regulation of the sweet potato sporamin gene promoter region. Plant Mol Biol. 48:223–231.
   PubMed Web of Science ®Google Scholar
• Wang X, Hu L, Zhou G, Cheng J, Lou Y. 2011b. Salicylic acid and ethylene signaling pathways are involved in production of rice trypsin proteinase inhibitors induced by the leaf folder Cnaphalocrocis medinalis (Guenée). Chi Sci Bull. 56:2351–2358.
   Google Scholar
• White JF, Kingsley KL, Zhang Q, Verma R, Obi N, Dvinskikh S, Elmore MT, Verma SK, Gond SK, Kowalski KP. 2019. Review: endophytic microbes and their potential applications in crop management. Pest Manag Sci. 75:2558–2565.
   PubMed Web of Science ®Google Scholar
• Yang J, Duan G, Li C, Liu L, Han G, Zhang Y, Wang C. 2019. The crosstalks between jasmonic acid and other plant hormone signaling highlight the involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses. Front Plant Sci. 10:1349.
   PubMed Web of Science ®Google Scholar
• Ye M, Luo SM, Xie JF, Li YF, Xu T, Liu Y, Song YY, Zhu-Salzman K, Zeng RS. 2012. Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. PLoS ONE. 7:e36214.
   PubMed Web of Science ®Google Scholar
• Yeh KW, Lin MI, Tuan SJ, Chen YM, Lin CJ, Kao SS. 1997. Sweet potato (Ipomoea batatas) trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura. Plant Cell Rep. 16:696–699.
   PubMed Web of Science ®Google Scholar
• Ziegler J, Keinänen M, Baldwin IT. 2001. Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuata. Phytochemistry. 58:729–738.
   PubMed Web of Science ®Google Scholar