Abstract
Plants have evolved according to their environmental conditions and continuously interact with different biological entities. These interactions induce many positive and negative effects on plant metabolism. Many viruses also associate with various plant species and alter their metabolism. Further, virus–plant interaction also alters the expression of many plant hormones. To overcome the biotic stress imposed by the virus’s infestation, plants produce different kinds of secondary metabolites that play a significant role in plant defense against the viral infection. In this review, we briefly highlight the mechanism of virus infection, their influence on the plant secondary metabolites and phytohormone biosynthesis in response to the virus–plant interactions.
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References
Abdala G, Milrad S, Vigliocco A, Lorenzo E, Pharis R, Wanner G (1999) Hyperauxinity in diseased leaves affected by Mal de Rio Cuarto Virus (MRCV). Biocell 23(1):13–18
Agarwal N, Srivastava R, Verma A, Rai KM, Singh B, Verma PC (2020) Unravelling cotton nonexpressor of pathogenesis-related 1(NPR1)-like genes family: evolutionary analysis and putative role in fiber development and defense pathway. Plants 9(8):999
Alazem M, Lin NS (2015) Roles of plant hormones in the regulation of host–virus interactions. Mol Plant Pathol 16(5):529–540. https://doi.org/10.1111/mpp.12204
Alazem M, Lin NS (2017) Antiviral roles of abscisic acid in plants. Front Plant Sci 8:1760. https://doi.org/10.3389/fpls.2017.01760
Alazem M, Lin KY, Lin NS (2014) The abscisic acid pathway has multifaceted effects on the accumulation of Bamboo mosaic virus. Mol Plant Microbe Interact 27(2):177–189. https://doi.org/10.1094/MPMI-08-13-0216-R
Alazem M, He MH, Moffett P, Lin NS (2017) Abscisic acid induces resistance against Bamboo mosaic virus through argonaute2 and 3. Plant Physiol 174(1):339–355. https://doi.org/10.1104/pp.16.00015
Alazem M, Tseng K-C, Chang W-C, Seo J-K, Kim K-H (2018) Elements involved in the Rsv3-mediated extreme resistance against an avirulent strain of soybean mosaic virus. Viruses 10(11):581
Alazem M, Kim KH, Lin NS (2019) Effects of abscisic acid and salicylic acid on gene expression in the antiviral RNA silencing pathway in Arabidopsis. Int J Mol Sci. https://doi.org/10.3390/ijms20102538
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63(10):3523–3543. https://doi.org/10.1093/jxb/ers100
Baebler Š, Witek K, Petek M, Stare K, Tušek-Žnidarič M, Pompe-Novak M, Renaut J, Szajko K, Strzelczyk-Żyta D, Marczewski W, Morgiewicz K, Gruden K, Hennig J (2014) Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato. J Exp Bot 65(4):1095–1109. https://doi.org/10.1093/jxb/ert447
Balázs E, Sziráki I, Király Z (1977) The rôle of cytokinins in the systemic acquired resistance of tobacco hypersensitive to tobacco mosaic virus. Physiol Plant Pathol 11(1):29-IN23. https://doi.org/10.1016/S0048-4059(77)80003-9
Baliji S, Lacatus G, Sunter G (2010) The interaction between geminivirus pathogenicity proteins and adenosine kinase leads to increased expression of primary cytokinin-responsive genes. Virology 402(2):238–247. https://doi.org/10.1016/j.virol.2010.03.023
Ben-Tal Y, Marco S (1980) Qualitative changes in cucumber gibberellins following cucumber mosaic virus infection. Physiol Plant Pathol 16(3):327–336. https://doi.org/10.1016/S0048-4059(80)80004-X
Bi H, Fan W, Zhang P (2017) C4 protein of sweet potato leaf curl virus regulates brassinosteroid signaling pathway through interaction with AtBIN2 and affects male fertility in Arabidopsis. Front Plant Sci 8:1689–1689. https://doi.org/10.3389/fpls.2017.01689
Blanco-Ulate B, Hopfer H, Figueroa-Balderas R, Ye Z, Rivero RM, Albacete A, Pérez-Alfocea F, Koyama R, Anderson MM, Smith RJ, Ebeler SE, Cantu D (2017) Red blotch disease alters grape berry development and metabolism by interfering with the transcriptional and hormonal regulation of ripening. J Exp Bot 68(5):1225–1238. https://doi.org/10.1093/jxb/erw506
Calil IP, Fontes EPB (2017) Plant immunity against viruses: antiviral immune receptors in focus. Ann Bot 119(5):711–723. https://doi.org/10.1093/aob/mcw200
Callaway A, Liu W, Andrianov V, Stenzler L, Zhao J, Wettlaufer S, Jayakumar P, Howell SH (1996) Characterization of cauliflower mosaic virus (CaMV) resistance in virus-resistant ecotypes of Arabidopsis. Mol Plant Microbe Interact 9(9):810–818. https://doi.org/10.1094/mpmi-9-0810
Casteel CL, De Alwis M, Bak A, Dong H, Whitham SA, Jander G (2015) Disruption of ethylene responses by turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector. Plant Physiol 169(1):209–218. https://doi.org/10.1104/pp.15.00332
Chaudhry Z, Yoshioka T, Satoh S, Hase S, Ehara Y (1998) Stimulated ethylene production in tobacco (Nicotiana tabacum L. cv. Ky 57) leaves infected systemically with cucumber mosaic virus yellow strain. Plant Sci 131(2):123–130. https://doi.org/10.1016/S0168-9452(97)00257-4
Chen S, Yu N, Yang S, Zhong B, Lan H (2018) Identification of Telosma mosaic virus infection in Passiflora edulis and its impact on phytochemical contents. Virol J 15(1):168. https://doi.org/10.1186/s12985-018-1084-6
Chinestra SC, Facchinetti C, Curvetto NR, Marinangeli PA (2010) Detection and frequency of lily viruses in Argentina. Plant Dis 94(10):1188–1194. https://doi.org/10.1094/pdis-07-09-0419
Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, Hwang I (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev Cell 19(2):284–295. https://doi.org/10.1016/j.devcel.2010.07.011
Chong J, Baltz R, Schmitt C, Beffa R, Fritig B, Saindrenan P (2002) Downregulation of a pathogen-responsive tobacco UDP-Glc:phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. Plant Cell 14(5):1093–1107. https://doi.org/10.1105/tpc.010436
Clarke SF, McKenzie MJ, Burritt DJ, Guy PL, Jameson PE (1999) Influence of white clover mosaic potexvirus infection on the endogenous cytokinin content of bean. Plant Physiol 120(2):547–552. https://doi.org/10.1104/pp.120.2.547
Clarke SF, Burritt DJ, Jameson PE, Guy PL (2000a) Effects of plant hormones on white clover mosaic potexvirus double stranded RNA. Plant Pathol 49(4):428–434
Clarke SF, Guy PL, Jameson PE, Schmierer D, Burritt DJ (2000b) Influence of white clover mosaic potexvirus infection on the endogenous levels of jasmonic acid and related compounds in Phaseolus vulgaris L. seedlings. J Plant Physiol 156(4):433–437. https://doi.org/10.1016/S0176-1617(00)80155-8
Clarke SF, Guy PL, Burritt DJ, Jameson PE (2002) Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. Physiol Plant 114(2):157–164. https://doi.org/10.1034/j.1399-3054.2002.1140201.x
Collum TD, Culver JN (2016) The impact of phytohormones on virus infection and disease. Curr Opin Virol 17:25–31. https://doi.org/10.1016/j.coviro.2015.11.003
Costet L, Fritig B, Kauffmann S (2002) Scopoletin expression in elicitor-treated and tobacco mosaic virus-infected tobacco plants. Physiol Plant 115(2):228–235. https://doi.org/10.1034/j.1399-3054.2002.1150208.x
Culver JN, Padmanabhan MS (2007) Virus-induced disease: altering host physiology one interaction at a time. Annu Rev Phytopathol 45(1):221–243. https://doi.org/10.1146/annurev.phyto.45.062806.094422
de Haro LA, Arellano SM, Novák O, Feil R, Dumón AD, Mattio MF, Tarkowská D, Llauger G, Strnad M, Lunn JE, Pearce S, Figueroa CM, del Vas M (2019) Mal de Río Cuarto virus infection causes hormone imbalance and sugar accumulation in wheat leaves. BMC Plant Biol 19(1):112. https://doi.org/10.1186/s12870-019-1709-y
Dehkordi AN, Rubio M, Babaeian N, Albacete A, Martínez-Gómez P (2018) Phytohormone signaling of the resistance to Plum pox virus (PPV, sharka disease) induced by almond (Prunus dulcis (Miller) Webb) grafting to peach (P. persica L. Batsch). Viruses 10(5):238. https://doi.org/10.3390/v10050238
Dempsey DA, Pathirana MS, Wobbe KK, Klessig DF (1997) Identification of an Arabidopsis locus required for resistance to turnip crinkle virus. Plant J 11(2):301–311. https://doi.org/10.1046/j.1365-313x.1997.11020301.x
Deng XG, Zhu T, Peng XJ, Xi DH, Guo H, Yin Y, Zhang DW, Lin HH (2016) Role of brassinosteroid signaling in modulating Tobacco mosaic virus resistance in Nicotiana benthamiana. Sci Rep 6:20579. https://doi.org/10.1038/srep20579
Deng XG, Zhu T, Zou LJ, Han XY, Zhou X, Xi DH, Zhang DW, Lin HH (2016) Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid-mediated systemic virus resistance in Nicotiana benthamiana. Plant J 85(4):478–493. https://doi.org/10.1111/tpj.13120
Dermastia M, Ravnikar M, Kovač M (1995) Increased cytokinin-9-glucosylation in roots of susceptible Solanum tuberosum cultivar infected by potato virus Y. Mol Plant Microbe Interact 8(2):327–330
Dhondt S, Geoffroy P, Stelmach BA, Legrand M, Heitz T (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J 23(4):431–440. https://doi.org/10.1046/j.1365-313x.2000.00802.x
Diao P, Zhang Q, Sun H, Ma W, Cao A, Yu R, Wang J, Niu Y, Wuriyanghan H (2019) miR403a and SA are involved in NbAGO2 mediated antiviral defenses against TMV infection in Nicotiana benthamiana. Genes (Basel). https://doi.org/10.3390/genes10070526
Diaz-Pendon JA, Li F, Li WX, Ding SW (2007) Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19(6):2053–2063. https://doi.org/10.1105/tpc.106.047449
Dixit G, Srivastava A, Rai KM, Dubey RS, Srivastava R, Verma PC (2020) Distinct defensive activity of phenolics and phenylpropanoid pathway genes in different cotton varieties toward chewing pests. Plant Signal Behav 15(5):1747689. https://doi.org/10.1080/15592324.2020.1747689
Du Z, Chen A, Chen W, Westwood JH, Baulcombe DC, Carr JP (2014) Using a viral vector to reveal the role of MicroRNA159 in disease symptom induction by a severe strain of Cucumber mosaic virus. Plant Physiol 164(3):1378–1388. https://doi.org/10.1104/pp.113.232090
Faccioli G, Rubies-Autonell C, Albertini R (1984) Role of cytokinins in the acquired resistance of Chenopodium amaranticolor towards an infection of Tobacco necrosis virus. Phytopathol Mediterr 23(1):15–22
Fazio Gd (1981) Cytokinin levels in healthy and bean golden mosaic virus (BGMV) infected bean plants (Phaseolus vulgaris). Rev Brasil Botanica 4(2):57–61
Ferdes M (2018) Antimicrobial compounds from plants. In: Budimir A (ed) Fighting Antimicrobial Resistance. IAPC Publishing, Zagreb, Croatia, pp 243-271. https://doi.org/10.5599/obp.15.15
Gális I, Smith JL, Jameson PE (2004) Salicylic acid-, but not cytokinin-induced, resistance to WClMV is associated with increased expression of SA-dependent resistance genes in Phaseolus vulgaris. J Plant Physiol 161(4):459–466. https://doi.org/10.1078/0176-1617-01255
Geri C, Love AJ, Cecchini E, Barrett SJ, Laird J, Covey SN, Milner JJ (2004) Arabidopsis mutants that suppress the phenotype induced by transgene-mediated expression of cauliflower mosaic virus (CaMV) gene VI are less susceptible to CaMV-infection and show reduced ethylene sensitivity. Plant Mol Biol 56(1):111–124. https://doi.org/10.1007/s11103-004-2649-x
Gutzeit HO, Ludwig-M J (2014) Plant natural products: synthesis, biological functions and practical applications. John Wiley & Sons, Weinheim
Hamidun B, Dusik L, Bunawan SN, Amin NM (2014) Rice tungro disease: from identification to disease control. World Appl Sci J 31:1221–1226
He Y, Zhang H, Sun Z, Li J, Hong G, Zhu Q, Zhou X, MacFarlane S, Yan F, Chen J (2017) Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to Rice black streaked dwarf virus infection in rice. New Phytol 214(1):388–399. https://doi.org/10.1111/nph.14376
Hyodo K, Okuno T (2020) Hijacking of host cellular components as proviral factors by plant-infecting viruses. In: Carr JP, Roossinck MJ (eds) Advances in Virus Research, vol 107. Academic Press, Cambridge, pp 37–86. doi:https://doi.org/https://doi.org/10.1016/bs.aivir.2020.04.002
Islam W, Naveed H, Zaynab M, Huang Z, Chen HYH (2019) Plant defense against virus diseases; growth hormones in highlights. Plant Signal Behav 14(6):1596719. https://doi.org/10.1080/15592324.2019.1596719
Jameson PE, Clarke SF (2002) Hormone–virus interactions in plants. Crit Rev Plant Sci 21(3):205–228. https://doi.org/10.1080/0735-260291044241
Jelínek L, Dolečková M, Karabin M, Hudcova T, Kotlikova B, Dostalek P (2012) Influence of growing area, plant age, and virus infection on the contents of hop secondary metabolites. Czech J Food Sci 30(6):541–547
Jin L, Qin Q, Wang Y, Pu Y, Liu L, Wen X, Ji S, Wu J, Wei C, Ding B, Li Y (2016) Rice dwarf virus P2 protein hijacks auxin signaling by directly targeting the rice OsIAA10 protein, enhancing viral infection and disease development. PLoS Pathog 12(9):e1005847. https://doi.org/10.1371/journal.ppat.1005847
Kabera JN, Semana E, Mussa AR, He X (2014) Plant secondary metabolites: biosynthesis, classification, function and pharmacological properties. J Pharm Pharmacol 2:377–392
Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development. https://doi.org/10.1242/dev.149344
Knoester M, Bol JF, van Loon LC, Linthorst HJ (1995) Virus-induced gene expression for enzymes of ethylene biosynthesis in hypersensitively reacting tobacco. Mol Plant Microbe Interact 8(1):177–180. https://doi.org/10.1094/mpmi-8-0177
Kobayashi M, Seo S, Hirai K, Yamamoto-Katou A, Katou S, Seto H, Meshi T, Mitsuhara I, Ohashi Y (2010) Silencing of WIPK and SIPK mitogen-activated protein kinases reduces tobacco mosaic virus accumulation but permits systemic viral movement in tobacco possessing the N resistance gene. Mol Plant Microbe Interact 23(8):1032–1041. https://doi.org/10.1094/mpmi-23-8-1032
Kovač M, Müller A, Jarh DM, Milavec M, Düchting P, Ravnikar M (2009) Multiple hormone analysis indicates involvement of jasmonate signalling in the early defence of potato to potato virus Y NTN. Biol Plant 53(1):195–199
Kriznik M, Petek M, Dobnik D, Ramsak Z, Baebler S, Pollmann S, Kreuze JF, Zel J, Gruden K (2017) Salicylic acid perturbs sRNA-gibberellin regulatory network in immune response of potato to potato virus Y infection. Front Plant Sci 8:2192. https://doi.org/10.3389/fpls.2017.02192
Kuriger W, Agrios G (1977) Cytokinin levels and kinetin–virus interactions in tobacco ringspot virus infected cowpea plants. Phytopathology 67:604–609
Lan H, Lai B, Zhao P, Dong X, Wei W, Ye Y, Wu Z (2020) Cucumber mosaic virus infection modulated the phytochemical contents of Passiflora edulis. Microb Pathog 138:103828. https://doi.org/10.1016/j.micpath.2019.103828
Lancini G, Lorenzetti R (1993) Biosynthesis of secondary metabolites. In: Biotechnology of antibiotics and other bioactive microbial metabolites. Springer US, Boston, pp 95–132. doi:https://doi.org/10.1007/978-1-4757-9522-6_4
León J, Shulaev V, Yalpani N, Lawton MA, Raskin I (1995) Benzoic acid 2-hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic acid biosynthesis. Proc Natl Acad Sci USA 92(22):10413–10417. https://doi.org/10.1073/pnas.92.22.10413
Li J-W, Wang B, Song X-M, Wang R-R, Chen L, Zhang H, Zhang Z-B, Wang Q-C (2013) Potato leafroll virus (PLRV) and potato virus Y (PVY) influence vegetative growth, physiological metabolism, and microtuber production of in vitro-grown shoots of potato Solanum tuberosum L. Plant Cell Tissue Organ Cult PCTOC 114(3):313–324. https://doi.org/10.1007/s11240-013-0327-x
Loebenstein G, Lawson RH, Brunt AA (1995) Virus and virus-like diseases of bulb and flower crops. Wiley, Bet Dagan
Lozano-Durán R, Rosas-Díaz T, Gusmaroli G, Luna AP, Taconnat L, Deng XW, Bejarano ER (2011) Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23(3):1014–1032. https://doi.org/10.1105/tpc.110.080267
Machado JP, Brustolini OJ, Mendes GC, Santos AA, Fontes EP (2015) NIK1, a host factor specialized in antiviral defense or a novel general regulator of plant immunity? BioEssays News Rev Mol Cell Dev Biol 37(11):1236–1242. https://doi.org/10.1002/bies.201500066
Masuta C, Tanaka H, Uehara K, Kuwata S, Koiwai A, Noma M (1995) Broad resistance to plant viruses in transgenic plants conferred by antisense inhibition of a host gene essential in S-adenosylmethionine-dependent transmethylation reactions. Proc Natl Acad Sci USA 92(13):6117–6121. https://doi.org/10.1073/pnas.92.13.6117
Montero R, Pérez-Bueno ML, Barón M, Florez-Sarasa I, Tohge T, Fernie AR, Ouad Hel A, Flexas J, Bota J (2016) Alterations in primary and secondary metabolism in Vitis vinifera “Malvasía de Banyalbufar” upon infection with Grapevine leafroll-associated virus 3. Physiol Plant 157(4):442–452. https://doi.org/10.1111/ppl.12440
Muletarova S, Stoikova D, Ivanov K (1995) Changes in the isoenzyme spectrum of peroxidase in potato and tobacco plants inoculated with potato virus A. Rastenievudni Nauki 32:118–120
Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 33(5):887–898. https://doi.org/10.1046/j.1365-313x.2003.01675.x
Ncube B, Van Staden J (2015) Tilting plant metabolism for improved metabolite biosynthesis and enhanced human benefit. Molecules 20(7):12698–12731. https://doi.org/10.3390/molecules200712698
Nicaise V, Candresse T (2017) Plum pox virus capsid protein suppresses plant pathogen-associated molecular pattern (PAMP)-triggered immunity. Mol Plant Pathol 18(6):878–886. https://doi.org/10.1111/mpp.12447
Ohtsubo N, Mitsuhara I, Koga M, Seo S, Ohashi Y (1999) Ethylene promotes the necrotic lesion formation and basic PR gene expression in TMV-infected tobacco. Plant Cell Physiol 40(8):808–817. https://doi.org/10.1093/oxfordjournals.pcp.a029609
Padmanabhan MS, Kramer SR, Wang X, Culver JN (2008) Tobacco mosaic virus replicase-auxin/indole acetic acid protein interactions: reprogramming the auxin response pathway to enhance virus infection. J Virol 82(5):2477–2485. https://doi.org/10.1128/JVI.01865-07
Pandey V, Srivastava R, Akhtar N, Mishra J, Mishra P, Verma PC (2016) Expression of Withania somnifera steroidal glucosyltransferase gene enhances withanolide content in hairy roots. Plant Mol Biol Rep 34(3):681–689. https://doi.org/10.1007/s11105-015-0955-x
Parizad S, Dizadji A, Habibi MK, Winter S, Kalantari S, Movi S, Lorenzo Tendero C, Alonso GL, Moratalla-Lopez N (2019) The effects of geographical origin and virus infection on the saffron (Crocus sativus L.) quality. Food Chem 295:387–394. https://doi.org/10.1016/j.foodchem.2019.05.116
Pennazio S, Roggero P (1996) Plant hormones and plant virus diseases. The auxins. New Microbiol 19(4):369–378
Pethybridge SJ, Wilson CR, Hay FS, Leggett GW, Sherriff LJ (2002) Effect of viruses on agronomic and brewing characteristics of four hop (Humulus lupulus) cultivars in Australia. Ann Appl Biol 140(1):97–105. https://doi.org/10.1111/j.1744-7348.2002.tb00161.x
Petrovič N, Miersch O, Ravnikar M, Kovač M (1997) Potato virus YNTNalters the distribution and concentration of endogenous jasmonic acid in potato plants grownin vitro. Physiol Mol Plant Pathol 50(4):237–244. https://doi.org/10.1006/pmpp.1997.0079
Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055
Pott DM, Osorio S, Vallarino JG (2019) From central to specialized metabolism: an overview of some secondary compounds derived from the primary metabolism for their role in conferring nutritional and organoleptic characteristics to fruit. Front Plant Sci 10:835. https://doi.org/10.3389/fpls.2019.00835
Rajagopal R (1977) Effect of tobacco mosaic virus infection on the endogenous levels of indoleacetic, phenylacetic and abscisic acids of tobacco leaves in various stages of development. J Plant Physiol 83(5):403–409. https://doi.org/10.1016/S0044-328X(77)80046-9
Rao M, Narasimham B, Reddy G, Murthy V (1977) Effect of mosaic virus infection on the endogenous gibberellin levels of sathgudi leaves (Citrus sinensis Osbeck). Indian J Hortic 34(2):196–198
Ravnikar M, Gogala N, Miersch O, Bruckner C (1990) The correlation between plant growth regulator jasmonic acid and PVM in the potato. Potato Res 33:144
Rezzonico E, Flury N, Meins F Jr, Beffa R (1998) Transcriptional down-regulation by abscisic acid of pathogenesis-related beta-1,3-glucanase genes in tobacco cell cultures. Plant Physiol 117(2):585–592. https://doi.org/10.1104/pp.117.2.585
Rodriguez MC, Conti G, Zavallo D, Manacorda CA, Asurmendi S (2014) TMV-Cg coat protein stabilizes DELLA proteins and in turn negatively modulates salicylic acid-mediated defense pathway during Arabidopsisthaliana viral infection. BMC Plant Biol 14:210. https://doi.org/10.1186/s12870-014-0210-x
Russell SL, Kimmins WC (1971) Growth regulators and the effect of barley yellow dwarf virus on barley Hordeum vulgare L. Ann Bot 35(5):1037–1043. https://doi.org/10.1093/oxfordjournals.aob.a084539
Sakamoto S, Putalun W, Vimolmangkang S, Phoolcharoen W, Shoyama Y, Tanaka H, Morimoto S (2018) Enzyme-linked immunosorbent assay for the quantitative/qualitative analysis of plant secondary metabolites. Journal of Natural Medicines 72(1):32–42. https://doi.org/10.1007/s11418-017-1144-z
Scholthof K-BG (2004) Tobacco mosaic virus: a model system for plant biology. Annu Rev Phytopathol 42:13–34
Sheng J, Lartey R, Ghoshroy S, Citovsky V (1998) An Arabidopsis thaliana mutant with virus-inducible phenotype. Virology 249(1):119–128. https://doi.org/10.1006/viro.1998.9238
Siefert F, Kwiatkowski J, Sarkar S, Grossmann K (1995) Changes in endogenous cyanide and 1-aminocyclopropane-1-carboxylic acid levels during the hypersensitive response of tobacco mosaic virus-infected tobacco leaves. Plant Growth Regul 17(2):109–113. https://doi.org/10.1007/BF00024169
Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM (2002) Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83(2):505–517. https://doi.org/10.2307/2680031
Sridhar R, Mohanty SK, Anjaneyulu A (1978) Physiology of rice tungro virus disease: increased cytokinin activity in tungro-infected rice cultivars. Physiol Plant 43(4):363–366. https://doi.org/10.1111/j.1399-3054.1978.tb01595.x
Srivastava R, Srivastava R, Singh UM (2014) Understanding the patterns of gene expression during climate change. In Climate Change Effect on Crop Productivity; CRC Press, Taylor & Francis Group: Boca Raton, FL, USA, pp 279–328. ISBN 978-1-4822-2920-2
Srivastava R, Rai KM, Srivastava R (2018) Plant biosynthetic engineering through transcription regulation: an insight into molecular mechanisms during environmental stress. In: Varjani SJ, Parameswaran B, Kumar S, Khare SK (eds) Biosynthetic technology and environmental challenges. Springer Singapore, Singapore, pp 51–72. https://doi.org/10.1007/978-981-10-7434-9_4
Sziráki I, Balázs E, Király Z (1980) Rôle of different stresses in inducing systemic acquired resistance to TMV and increasing cytokinin level in tobacco. Physiol Plant Pathol 16(2):277–284. https://doi.org/10.1016/0048-4059(80)90042-9
Tavantzis SM, Smith SH, Witham FH (1979) The influence of kinetin on tobacco ringspot virus infectivity and the effect of virus infection on the cytokinin activity in intact leaves of Nicotiana glutinosa L. Physiol Plant Pathol 14 (2):227–233.https://doi.org/10.1016/0048-4059(79)90010-9
Thivierge K, Nicaise V, Dufresne PJ, Cotton S, Laliberte JF, Le Gall O, Fortin MG (2005) Plant virus RNAs. Coordinated recruitment of conserved host functions by (+) ssRNA viruses during early infection events. Plant Physiol 138(4):1822–1827. https://doi.org/10.1104/pp.105.064105
Thompson G, Martin M, Van Staden J (1983) Relationship between tomato spotted wilt virus infection and cytokinin content of tomato. Phytophylactica 15(2):63–66
Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10(6):385–397. https://doi.org/10.1038/nrm2688
Vitti A, Nuzzaci M, Scopa A, Tataranni G, Remans T, Vangronsveld J, Sofo A (2013) Auxin and cytokinin metabolism and root morphological modifications in Arabidopsis thaliana seedlings infected with Cucumber mosaic virus (CMV) or exposed to cadmium. Int J Mol Sci 14(4):6889–6902. https://doi.org/10.3390/ijms14046889
Wang X, Culver JN (2012) DNA binding specificity of ATAF2, a NAC domain transcription factor targeted for degradation by Tobacco mosaic virus. BMC Plant Biol 12:157. https://doi.org/10.1186/1471-2229-12-157
Wang X, Goregaoker SP, Culver JN (2009) Interaction of the Tobacco mosaic virus replicase protein with a NAC domain transcription factor is associated with the suppression of systemic host defenses. J Virol 83(19):9720–9730. https://doi.org/10.1128/jvi.00941-09
War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6(11):1787–1792. https://doi.org/10.4161/psb.6.11.17685
Whenham RJ (1989) Effect of systemic tobacco mosaic virus infection on endogenous cytokinin concentration in tobacco (Nicotiana tabacum L.) leaves: consequences for the control of resistance and symptom development. Physiol Mol Plant Pathol 35(1):85–95. https://doi.org/10.1016/0885-5765(89)90009-X
Wu Q, Wang X, Ding SW (2010) Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe 8(1):12–15. https://doi.org/10.1016/j.chom.2010.06.009
Wu X, Valli A, García JA, Zhou X, Cheng X (2019) The tug-of-war between plants and viruses: great progress and many remaining questions. Viruses 11(3):203. https://doi.org/10.3390/v11030203
Xie K, Li L, Zhang H, Wang R, Tan X, He Y, Hong G, Li J, Ming F, Yao X, Yan F, Sun Z, Chen J (2018) Abscisic acid negatively modulates plant defence against rice black-streaked dwarf virus infection by suppressing the jasmonate pathway and regulating reactive oxygen species levels in rice. Plant Cell Environ 41(10):2504–2514. https://doi.org/10.1111/pce.13372
Xu P, Chen F, Mannas JP, Feldman T, Sumner LW, Roossinck MJ (2008) Virus infection improves drought tolerance. New Phytol 180(4):911–921. https://doi.org/10.1111/j.1469-8137.2008.02627.x
Zaim M, Lal R, Verma R, Pandey R (2014) Studies on effect of poppy mosaic virus infection on poppy produce and some secondary metabolites. Acta Horticult 1036:151–155
Zaim M, Verma RK, Pandey R, Lal RK (2014) Genotype-dependent response of an RNA Virus Infection on Selected pharmaceutically important alkaloids in Papaver somniferum. J Herbs Spices Med Plants 20(2):124–131. https://doi.org/10.1080/10496475.2013.840817
Zhang H, Zhu Liu XH (1997) Effect Of banana bunchy top virus (BBTV) on endogenous hormones of banana plant . Acta Phytopathol Sin 27:79–83
Zhang DW, Deng XG, Fu FQ, Lin HH (2015) Induction of plant virus defense response by brassinosteroids and brassinosteroid signaling in Arabidopsis thaliana. Planta 241(4):875–885. https://doi.org/10.1007/s00425-014-2218-8
Zhang C, Ding Z, Wu K, Yang L, Li Y, Yang Z, Shi S, Liu X, Zhao S, Yang Z, Wang Y, Zheng L, Wei J, Du Z, Zhang A, Miao H, Li Y, Wu Z, Wu J (2016) Suppression of jasmonic acid-mediated defense by viral-inducible microRNA319 facilitates virus infection in rice. Mol Plant 9(9):1302–1314. https://doi.org/10.1016/j.molp.2016.06.014
Zhang H, Tan X, Li L, He Y, Hong G, Li J, Lin L, Cheng Y, Yan F, Chen J, Sun Z (2019) Suppression of auxin signalling promotes rice susceptibility to rice black streaked dwarf virus infection. Mol Plant Pathol 20(8):1093–1104. https://doi.org/10.1111/mpp.12814
Zhang H, Li L, He Y, Qin Q, Chen C, Wei Z, Tan X, Xie K, Zhang R, Hong G, Li J, Li J, Yan C, Yan F, Li Y, Chen J, Sun Z (2020) Distinct modes of manipulation of rice auxin response factor OsARF17 by different plant RNA viruses for infection. Proc Natl Acad Sci USA 117(16):9112–9121. https://doi.org/10.1073/pnas.1918254117
Zhao S, Hong W, Wu J, Wang Y, Ji S, Zhu S, Wei C, Zhang J, Li Y (2017) A viral protein promotes host SAMS1 activity and ethylene production for the benefit of virus infection. Elife. https://doi.org/10.7554/eLife.27529
Zhu S, Gao F, Cao X, Chen M, Ye G, Wei C, Li Y (2005) The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol 139(4):1935–1945. https://doi.org/10.1104/pp.105.072306
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JM duly acknowledge Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, Uttar Pradesh, India.
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This work was supported by the SERB, New Delhi, Government of India [Project No. GAP-3401]. Institute Manuscript Number is CSIR-NBRI_ MS/2020/06/25.
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JM and RS drafted and wrote the manuscript, and involved in drawing the figures and tables in this review article. PKT reviewed and evaluated the manuscript. PCV reviewed and overall guided the manuscript.
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Mishra, J., Srivastava, R., Trivedi, P.K. et al. Effect of virus infection on the secondary metabolite production and phytohormone biosynthesis in plants. 3 Biotech 10, 547 (2020). https://doi.org/10.1007/s13205-020-02541-6
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DOI: https://doi.org/10.1007/s13205-020-02541-6