Abstract
Rice tungro disease (RTD) is a devastating disease of rice caused by combined infection with rice tungro bacilliform virus (RTBV) and rice tungro spherical virus (RTSV), with one of the main symptoms being stunting. To dissect the molecular events responsible for RTD-induced stunting, the expression patterns of 23 cell-wall-related genes were examined in different rice lines with the same titers of RTSV but different titers of RTBV and in lines where only RTBV was present. Genes encoding cellulose synthases, expansins, glycosyl hydrolases, exostosins, and xyloglucan galactosyl transferase showed downregulation, whereas those encoding defensin or defensin-like proteins showed upregulation with increasing titers of RTBV. RTSV titers did not affect the expression levels of these genes. A similar relationship was seen for the reduction in the cellulose and pectin content and the accumulation of lignin. In silico analysis of promoters of the genes indicated a possible link to transcription factors reported earlier to respond to viral titers in rice. These results suggest a common network in which the genes related to the cell wall components are affected during infection with diverse viruses in rice.
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References
Nagadhara D, Ramesh S, Pasalu IC et al (2003) Transgenic indica rice resistant to sap-sucking insects. Plant Biotechnol J 1:231–240. https://doi.org/10.1046/j.1467-7652.2003.00022.x
Hibino H, Roechan M, Sudarisman S (1978) Association of two types of virus particles with penyakit habang (tungro disease) of rice in Indonesia. Phytopathology 68:1412–1416. https://doi.org/10.1094/Phyto-68-1412
Jones MC, Gough K, Dasgupta I et al (1991) Rice tungro disease is caused by an RNA and a DNA virus. J Gen Virol 72:757–761. https://doi.org/10.1099/0022-1317-72-4-757
Hay JM, Jones MC, Blakebrough ML et al (1991) An analysis of the sequence of an infectious clone of rice tungro bacilliform virus, a plant pararetrovirus. Nucleic Acids Res 19:2615–2621. https://doi.org/10.1093/nar/19.10.2615
Shen P, Kaniewska M, Smith C, Beachy RN (1993) Nucleotide sequence and genomic organization of rice tungro spherical virus. Virology 193:621–630. https://doi.org/10.1006/viro.1993.1170
Rivera CT, Ou SH (1967) Transmission studies of the two strains of rice tungro virus. Plant Dis Rep 51:877–881
Cabauatan PQ, Hibino H (1985) Transmission of rice tungro bacilliform and spherical viruses by Nephotettix virescens Distant. Philippine Phytopathology (Philippines) v. 21
Dasgupta I, Hull R, Eastop S et al (1991) Rice tungro bacilliform virus DNA independently infects rice after Agrobacterium-mediated transfer. J Gen Virol 72:1215–1221. https://doi.org/10.1099/0022-1317-72-6-1215
Azzam O, Chancellor TCB (2002) The biology, epidemiology, and management of rice tungro disease in Asia. Plant Dis 86:88–100. https://doi.org/10.1094/PDIS.2002.86.2.88
Tyagi H, Rajasubramaniam S, Rajam MV, Dasgupta I (2008) RNA-interference in rice against Rice tungro bacilliform virus results in its decreased accumulation in inoculated rice plants. Transgenic Res 17:897–904. https://doi.org/10.1007/s11248-008-9174-7
Kumar G, Jyothsna M, Valarmathi P et al (2019) Assessment of resistance to rice tungro disease in popular rice varieties in India by introgression of a transgene against Rice tungro bacilliform virus. Arch Virol 164(4):1005–1003
Valarmathi P, Kumar G, Robin S et al (2016) Evaluation of virus resistance and agronomic performance of rice cultivar ASD 16 after transfer of transgene against Rice tungro bacilliform virus by backcross breeding. Virus Genes 52:521–529. https://doi.org/10.1007/s11262-016-1318-x
Shimizu T, Satoh K, Kikuchi S, Omura T (2007) The repression of cell wall- and plastid-related genes and the induction of defense-related genes in rice plants infected with Rice dwarf virus. Mol Plant Microbe Interact 20:247–254. https://doi.org/10.1094/MPMI-20-3-0247
Satoh K, Kondoh H, Sasaya T et al (2010) Selective modification of rice (Oryza sativa) gene expression by rice stripe virus infection. J Gen Virol. https://doi.org/10.1099/vir.0.015990-0
Satoh K, Shimizu T, Kondoh H et al (2011) Relationship between symptoms and gene expression induced by the infection of three strains of Rice dwarf virus. PLoS ONE. https://doi.org/10.1371/journal,pone.0018094
Satoh K, Kondoh H, De Leon TB et al (2013) Gene expression responses to Rice tungro spherical virus in susceptible and resistant near-isogenic rice plants. Virus Res 171:111–120. https://doi.org/10.1016/j.virusres.2012.11.003
Budot BO, Encabo JR, Ambita IDV et al (2014) Suppression of cell wall-related genes associated with stunting of Oryza glaberrima infected with Rice tungro spherical virus. Front Microbiol 5:26
Hibino H (1996) Biology and epidemiology of rice viruses. Annu Rev Phytopathol 32:249–274. https://doi.org/10.1146/annurev.phyto.34.1.249
Falk BW, Tsai JH (1998) Biology and molecular biology of viruses in the genus Tenuivirus. Annu Rev Phytopathol 36:139–163
Wang N, Xing Y, Lou Q et al (2017) Dwarf and short grain 1, encoding a putative U-box protein regulates cell division and elongation in rice. J Plant Physiol 209:84–94
Encabo JR, Cabauatan PQ, Cabunagan RC et al (2009) Suppression of two tungro viruses in rice by separable traits originating from cultivar Utri Merah. Mol Plant-Microbe Interact 22:1268–1281. https://doi.org/10.1094/MPMI-22-10-1268
Cabauatan PQ, Kobayashi N, Ikeda R, Koganezawa H (1993) Oryza glaberrima: an indicator plant for rice tungro spherical virus. Int J Pest Manag 39:273–276. https://doi.org/10.1080/09670879309371804
Somerville C, Bauer S, Brininstool G et al (2004) Toward a systems approach to understanding plant cell walls. Science 80(306):2206–2211
Hu H, Zhang R, Feng S et al (2018) AtCesA6-like members enhance biomass production by distinctively promoting cell growth in Arabidopsis. Plant Biotechnol J 16(5):976–988
Hazen SP, Scott-Craig JS, Walton JD (2002) Cellulose synthase-like genes of rice. Plant Physiol 128:336–340
Ding X, Cao Y, Huang L et al (2008) Activation of the indole-3-acetic acid–amido synthetase GH3-8 suppresses expansin expression and promotes salicylate-and jasmonate-independent basal immunity in rice. Plant Cell 20(1):228–240
Hara Y, Yokoyama R, Osakabe K et al (2014) Function of xyloglucan endotransglucosylase/hydrolases in rice. Ann Bot 114(6):1309–1318
Yoshida S (1976) Routine procedure for growing rice plants in culture solution. Lab Man Physiol Stud Rice 1976:61–66
Sharma S, Kumar G, Dasgupta I (2018) Simultaneous resistance against the two viruses causing rice tungro disease using RNA interference. Virus Res 255:157–164. https://doi.org/10.1016/j.virusres.2018.07.011
Purkayastha A, Mathur S, Verma V et al (2010) Virus-induced gene silencing in rice using a vector derived from a DNA virus. Planta 232:1531–1540. https://doi.org/10.1007/s00425-010-1273-z
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651. https://doi.org/10.1016/j.bbrc.2006.04.140
Bevitori R, Oliveira MB, Grossi-de-Sá MF et al (2014) Selection of optimized candidate reference genes for qRT-PCR normalization in rice (Oryza sativa L.) during Magnaporthe oryzae infection and drought. Genet Mol Res 13:9795–9805. https://doi.org/10.4238/2014.November.27.7
Peng L, Hocart CH, Redmond JW, Williamson RE (2000) Fractionation of carbohydrates in Arabidopsis root cell walls shows that three radial swelling loci are specifically involved in cellulose production. Planta 211:406–414
Li F, Zhang M, Guo K et al (2015) High-level hemicellulosic arabinose predominately affects lignocellulose crystallinity for genetically enhancing both plant lodging resistance and biomass enzymatic digestibility in rice mutants. Plant Biotechnol J 13:514–525
Sluiter A, Hames B, Ruiz R et al (2008) Determination of structural carbohydrates and lignin in biomass. Lab Anal Proced 1617:1–16
Wu Z, Zhang M, Wang L et al (2013) Biomass digestibility is predominantly affected by three factors of wall polymer features distinctive in wheat accessions and rice mutants. Biotechnol Biofuels 6:183
Huang J, Takano T, Akita S (2000) Expression of α-expansin genes in young seedlings of rice (Oryza sativa L.). Planta 211:467–473. https://doi.org/10.1007/s004250000311
Uozu S, Tanaka-Ueguchi M, Kitano H et al (2000) Characterization of XET-related genes of rice. Plant Physiol 122:853–860
Shin J-H, Jeong D-H, Park MC, An G (2005) Characterization and transcriptional expression of the α-expansin gene family in rice. Mol Cells 20(2):210–218
Burton RA, Gibeaut DM, Bacic A et al (2000) Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12:691–705
Tanaka K, Murata K, Yamazaki M et al (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol 133:73–83
Kende H, Bradford K, Brummell D et al (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314
Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6:242
Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321
Dal Santo S, Vannozzi A, Tornielli GB, Fasoli M, Venturini L et al (2013) Genome-wide analysis of the expansin gene superfamily reveals grapevine-specific structural and functional characteristics. PLoS ONE 8(4):e62206. https://doi.org/10.1371/journal.pone.0062206
Goh H-H, Sloan J, Dorca-Fornell C, Fleming A (2012) Inducible repression of multiple expansin genes leads to growth suppression during leaf development. Plant Physiol 159:1759–1770
Choi D, Lee Y, Cho H-T, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398
Nishitani K, Tominaga R (1991) In vitro molecular weight increase in xyloglucans by an apoplastic enzyme preparation from epicotyls of Vigna angularis. Physiol Plant 82:490–497
Nishitani K, Tominaga R (1992) Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem 267:21058–21064
Smith RC, Fry SC (1991) Endotransglycosylation of xyloglucans in plant cell suspension cultures. Biochem J 279:529–535
Schoelz JE, Harries PA, Nelson RS (2011) Intracellular transport of plant viruses: finding the door out of the cell. Mol Plant 4:813–831. https://doi.org/10.1093/mp/ssr070
Otulak-Kozieł K, Kozieł E, Lockhart BEL (2018) Plant cell wall dynamics in compatible and incompatible potato response to infection caused by potato virus Y (PVY(NTN)). Int J Mol Sci 19:862. https://doi.org/10.3390/ijms19030862
Wu J, Jin X, Zhao Y et al (2016) Evolution of the defensin-like gene family in grass genomes. J Genet 95:53–62
Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol 37:165–186
Vance CP, Kirk TK, Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 18:259–288. https://doi.org/10.1146/annurev.py.18.090180.001355
Yin Y, Chen L, Beachy R (1997) Promoter elements required for phloem-specific gene expression from the RTBV promoter in rice. Plant J 12:1179–1188
Dai S, Zhang Z, Chen S, Beachy RN (2004) RF2b, a rice bZIP transcription activator, interacts with RF2a and is involved in symptom development of rice tungro disease. Proc Natl Acad Sci USA 101:687–692
Dai S, Wei X, Alfonso AA et al (2008) Transgenic rice plants that overexpress transcription factors RF2a and RF2b are tolerant to rice tungro virus replication and disease. Proc Natl Acad Sci 105:21012–21016
Acknowledgements
GK acknowledges a research associate fellowship funded by the Council of Scientific and Industrial Research, New Delhi. Funds for this work were made available as the J. C. Bose Fellowship by the Science and Engineering Research Board, Department of Science and Technology, Government of India, to ID. The authors acknowledge a DU-DST FIST infrastructural grant of the Department of Plant Molecular Biology, University of Delhi South Campus
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Kumar, G., Dasgupta, I. The titers of rice tungro bacilliform virus dictate the expression levels of genes related to cell wall dynamics in rice plants affected by tungro disease. Arch Virol 166, 1325–1336 (2021). https://doi.org/10.1007/s00705-021-05006-0
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DOI: https://doi.org/10.1007/s00705-021-05006-0