46
Views
0
CrossRef citations to date
0
Altmetric
Review Article

Apple stem grooving capillovirus: pliant pathogen and its potential as a tool in functional genomics and effective disease management

, , , , , , , , , , , , & ORCID Icon show all
Pages 261-295 | Received 31 Jan 2024, Accepted 21 May 2024, Published online: 05 Jun 2024

References

  • Alas T, Baloglu S, Caglar BK, Gunes A. 2019. Detection and characterization of citrus tatter leaf virus (CTLV) and citrus yellow vein clearing virus (CYVCV) in citrus trees from Cyprus. Saudi J Biol Sci. 26(5):995–998. doi: 10.1016/j.sjbs.2019.02.001.
  • Aldaoud R, Dawson WO, Jones GE. 1989. Rapid, random evolution of the genetic structure of replicating tobacco mosaic virus populations. Intervirology. 30(4):227–233. doi: 10.1159/000150096.
  • Anderson JP, Daifuku R, Loeb LA. 2004. Viral error catastrophe by mutagenic nucleosides. Annu Rev Microbiol. 58(1):183–205. doi: 10.1146/annurev.micro.58.030603.123649.
  • Andika IB, Wei S, Cao C, Salaipeth L, Kondo H, Sun L. 2017. Phytopathogenic fungus hosts a plant virus: a naturally occurring cross-kingdom viral infection. Proc Natl Acad Sci USA. 114(46):12267–12272. doi: 10.1073/pnas.1714916114.
  • Atabekova AK, Solovieva AD, Chergintsev DA, Solovyev AG, Morozov SY. 2023. Role of plant virus movement proteins in suppression of Host RNAi defense. Int J Mol Sci. 24(10):9049. doi: 10.3390/ijms24109049.
  • Atreya CD, Pirone TP. 1993. Mutational analysis of the helper component-proteinase gene of a potyvirus: effects of amino acid substitutions, deletions, and gene replacement on virulence and aphid transmissibility. Proc Natl Acad Sci USA. 90(24):11919–11923. doi: 10.1073/pnas.90.24.11919.
  • Babaei G, Massah A, Koohi Habibi M. 2021. Efficient translation of Eggplant mottled dwarf nucleorhabdovirus N and X genes requires both 5′ and 3′ UTRs. Virol J. 18(1):129. doi: 10.1186/s12985-021-01601-4.
  • Baranovskaya I, Sergeeva M, Fadeev A, Kadirova R, Ivanova A, Ramsay E, Vasin A. 2019. Changes in RNA secondary structure affect NS1 protein expression during early stage influenza virus infection. Virol J. 16(1):162. doi: 10.1186/s12985-019-1271-0.
  • Bazzini A, Hopp H, Beachy R, Asurmendi S. 2007. Infection and coaccumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc Natl Acad Sci USA. 104(29):12157–12162. doi: 10.1073/pnas.0705114104.
  • Bhardwaj P, Awasthi P, Prakash O, Sood A, Zaidi A, Hallan V. 2017. Molecular evidence of natural occurrence of Apple stem grooving virus on bamboos. Trees. 31(1):367–375. doi: 10.1007/s00468-016-1375-8.
  • Bhardwaj P, Hallan V. 2019a. Molecular evidence of Apple stem grooving virus infecting Ficus palmata. Trees. 33(1):1–9. doi: 10.1007/s00468-018-1752-6.
  • Bhardwaj P, Hallan V. 2019b. Occurrence of Apple stem grooving virus on Rubus ellipticus, a perennial weed in India. Eur J Plant Pathol. 153(1):311–319. doi: 10.1007/s10658-018-1535-3.
  • Bhardwaj P, Ram R, Zaidi A, Hallan V. 2016. Apple stem grooving virus naturally infects Himalayan wild cherry (Prunuscerasoides D. Don). Forest Pathology. 46(2):116–121. doi: 10.1111/efp.12226.
  • Bhardwaj P, Ram R, Zaidi AA, Hallan V. 2014. Characterization of Apple stem grooving virus infecting Actinidia deliciosa (Kiwi) in India. Sci Hortic. 176:105–111. doi: 10.1016/j.scienta.2014.06.038.
  • Bhardwaj P, Ram R, Zaidi AA, Hallan V. 2015. Natural occurrence of Apple stem grooving virus on Bauhinia variegata. Trees. 29(5):1415–1422. doi: 10.1007/s00468-015-1219-y.
  • Bhardwaj P, Singh RM, Hallan V. 2023. Molecular evidence of Apple Stem Grooving Virus infecting Pear in India. Indian Phytopathol. 76(2):615–623. doi: 10.1007/s42360-023-00628-7.
  • Brakta A, Thakur P, Handa A. 2013. First report of apple top working disease caused by viruses (apple stem grooving virus, apple chlorotic leaf spot virus, and apple stem pitting virus) in apple in India. Plant Dis. 97(7):1001–1001. doi: 10.1094/PDIS-11-12-1082-PDN.
  • Brierley I, Pennell S, Gilbert RJ. 2007. Viral RNA pseudoknots: versatile motifs in gene expression and replication. Nat Rev Microbiol. 5(8):598–610. doi: 10.1038/nrmicro1704.
  • Bujarski JJ. 2013. Genetic recombination in plant-infecting messenger-sense RNA viruses: overview and research perspectives. Front Plant Sci. 4:68. doi: 10.3389/fpls.2013.00068.
  • Byszewska M, Śmietański M, Purta E, Bujnicki JM. 2014. RNA methyltransferases involved in 5′ cap biosynthesis. RNA Biol. 11(12):1597–1607. doi: 10.1080/15476286.2015.1004955.
  • Caparco AA, González-Gamboa I, Hays SS, Pokorski JK, Steinmetz NF. 2023. Delivery of Nematicides Using TMGMV-Derived Spherical Nanoparticles. Nano Lett. 23(12):5785–5793. doi: 10.1021/acs.nanolett.3c01684.
  • Carpenter CD, Oh J-W, Zhang C, Simon AE. 1995. Involvement of a stem-loop structure in the location of junction sites in viral RNA recombination. J Mol Biol. 245(5):608–622. doi: 10.1006/jmbi.1994.0050.
  • Castillo-González C, Liu X, Huang C, Zhao C, Ma Z, Hu T, Sun F, Zhou Y, Zhou X, Wang X-J, et al. 2015. Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense. Elife. 4:e06671. doi: 10.7554/eLife.06671.
  • Cejnar P, Ohnoutková L, Ripl J, Vlčko T, Kundu JK. 2018. Two mutations in the truncated Rep gene RBR domain delayed the Wheat dwarf virus infection in transgenic barley plants. J. Integrat. Agricult. 17(11):2492–2500. doi: 10.1016/S2095-3119(18)62000-3.
  • Chang Y-C, Lin T-C. 2020. Temperature effects on fruit development and quality performance of nagami kumquat (Fortunella margarita [Lour.] Swingle). Hort J. 89(4):351–358. doi: 10.2503/hortj.UTD-120.
  • Chariou PL, Dogan AB, Welsh AG, Saidel GM, Baskaran H, Steinmetz NF. 2019. Soil mobility of synthetic and virus-based model nanopesticides. Nat Nanotechnol. 14(7):712–718. doi: 10.1038/s41565-019-0453-7.
  • Chen J, Tang H-H, Li L, Qin S-J, Wang G-P, Hong N. 2017. Effects of virus infection on plant growth, root development and phytohormone levels in in vitro-cultured pear plants. Plant Cell Tiss Organ Cult. 131(2):359–368. doi: 10.1007/s11240-017-1289-1.
  • Chen S, Ye T, Hao L, Chen H, Wang S, Fan Z, Guo L, Zhou T. 2014. Infection of apple by apple stem grooving virus leads to extensive alterations in gene expression patterns but no disease symptoms. PLoS One. 9(4):e95239. doi: 10.1371/journal.pone.0095239.
  • Cho I-S, Kim D-H, Kim H-R, Chung B-N, Cho J-D, Choi G-S. 2010. Occurrence of pome fruit viruses on pear trees (Pyrus pyrifolia) in Korea. Res. Plant Dis. 16(3):326–330. doi: 10.5423/RPD.2010.16.3.326.
  • Chung BN, Kwon S-J, Yoon J-Y, Cho I-S. 2022. First report of Cnidium officinale as a natural host plant of apple stem grooving virus in South Korea. Plant Dis. 106(1):338. doi: 10.1094/PDIS-04-21-0781-PDN.
  • Clover G, Pearson M, Elliott D, Tang Z, Smales T, Alexander B. 2003. Characterization of a strain of Apple stem grooving virus in Actinidia chinensis from China. Plant Pathol. 52(3):371–378. doi: 10.1046/j.1365-3059.2003.00857.x.
  • Csorba T, Kontra L, Burgyán J. 2015. Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology. 479-480:85–103. doi: 10.1016/j.virol.2015.02.028.
  • Dai X, Hakizimana O, Zhang X, Kaushik AC, Zhang J. 2020. Orchestrated efforts on host network hijacking: processes governing virus replication. Virulence. 11(1):183–198. doi: 10.1080/21505594.2020.1726594.
  • Dasgupta R, Garcia BH, Goodman RM. 2001. Systemic spread of an RNA insect virus in plants expressing plant viral movement protein genes. Proc Natl Acad Sci USA. 98(9):4910–4915. doi: 10.1073/pnas.081288198.
  • Deb B, Uddin A, Chakraborty S. 2020. Codon usage pattern and its influencing factors in different genomes of hepadnaviruses. Arch Virol. 165(3):557–570. doi: 10.1007/s00705-020-04533-6.
  • DEN Boon JA, Ahlquist P. 2010. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol. 64(1):241–256. doi: 10.1146/annurev.micro.112408.134012.
  • Dhir S, Walia Y, Zaidi A, Hallan V. 2015. A simplified strategy for studying the etiology of viral diseases: apple stem grooving virus as a case study. J Virol Methods. 213:106–110. doi: 10.1016/j.jviromet.2014.11.017.
  • Diamos AG, Rosenthal SH, Mason HS. 2016. 5′ and 3′ untranslated regions strongly enhance performance of geminiviral replicons in Nicotiana benthamiana leaves. Front Plant Sci. 7:200. doi: 10.3389/fpls.2016.00200.
  • Diaz-Lara A, Mollov D, Golino D, Al Rwahnih M. 2020. Complete genome sequence of rose virus A, the first carlavirus identified in rose. Arch Virol. 165(1):241–244. doi: 10.1007/s00705-019-04460-1.
  • Dolja VV, Krupovic M, Koonin EV. 2020. Deep roots and splendid boughs of the ­global plant virome. Annu Rev Phytopathol. 58(1):23–53. doi: 10.1146/annurev-phyto-030320-041346.
  • Drazeta L, Lang A, Hall AJ, Volz RK, Jameson PE. 2004. Causes and effects of changes in xylem functionality in apple fruit. Ann Bot. 93(3):275–282. doi: 10.1093/aob/mch040.
  • Elena SF, Fraile A, García-Arenal F. 2014. Evolution and emergence of plant viruses. Adv Virus Res. 88:161–191. doi: 10.1016/B978-0-12-800098-4.00003-9.
  • Erickson AK, Jesudhasan PR, Mayer MJ, Narbad A, Winter SE, Pfeiffer JK. 2018. Bacteria facilitate enteric virus co-infection of mammalian cells and promote genetic recombination. Cell Host Microbe. 23(1):77–88. e5. doi: 10.1016/j.chom.2017.11.007.
  • Fetters AM, Cantalupo PG, Wei N, Robles MTS, Stanley A, Stephens JD, Pipas JM, Ashman T-L. 2022. The pollen virome of wild plants and its association with variation in floral traits and land use. Nat Commun. 13(1):523. doi: 10.1038/s41467-022-28143-9.
  • Fleischmann WR.Jr, 1996. Viral genetics. Medical microbiology. Chapter 43, 4th edition. Galveston: Galveston (TX) University of Texas Medical Branch. https://www.ncbi.nlm.nih.gov/books/NBK8439/
  • Gao R, Xu Y, Candresse T, He Z, Li S, Ma Y, Lu M. 2017. Further insight into genetic variation and haplotype diversity of Cherry virus A from China. PLoS One. 12(10):e0186273. doi: 10.1371/journal.pone.0186273.
  • Geng G, Yu C, Li X, Yuan X. 2019. Variable 3’polyadenylation of Wheat yellow mosaic virus and its novel effects on translation and replication. Virol J. 16(1):23. doi: 10.1186/s12985-019-1130-z.
  • González R, Butković A, Elena SF. 2019. Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus. Virus Evol. 5(2):vez024. doi: 10.1093/ve/vez024.
  • Gregori J, Cortese MF, Piñana M, Campos C, Garcia-Cehic D, Andrés C, Abril JF, Codina MG, Rando A, Esperalba J, et al. 2021. Host-dependent editing of SARS-CoV-2 in COVID-19 patients. Emerg Microbes Infect. 10(1):1777–1789. doi: 10.1080/22221751.2021.1969868.
  • Han J-Y, Park C-H, Seo E-Y, Kim J-K, Hammond J, Lim H-S. 2016. Occurrence of Apple stem grooving virus in commercial apple seedlings and analysis of its coat protein sequence. Korean J. Agricult. Sci. 43(1):21–27. doi: 10.7744/kjoas.20160003.
  • He R, Li Y, Bernards MA, Wang A. 2023. Manipulation of the cellular membrane-cytoskeleton network for RNA virus replication and movement in plants. Viruses. 15(3):744. doi: 10.3390/v15030744.
  • He Y, Chen Y, Wang Z, Wang L, Wang G, Hong N, Xu W. 2016. First Report of Apple stem grooving virus Infecting Rosa chinensis in China. Plant Dis. 100(6):1252–1252. doi: 10.1094/PDIS-12-15-1468-PDN.
  • He Y, Yang Z, Hong N, Wang G, Ning G, Xu W. 2015. Deep sequencing reveals a novel closterovirus associated with wild rose leaf rosette disease. Mol Plant Pathol. 16(5):449–458. doi: 10.1111/mpp.12202.
  • Hilf ME. 2008. An immunocapture RT-PCR procedure using Apple stem grooving virus antibodies facilitates analysis of Citrus tatter leaf virus from the original Meyer lemon host. Plant Dis. 92(5):746–750. doi: 10.1094/PDIS-92-5-0746.
  • Hirata H, Lu X, Yamaji Y, Kagiwada S, Ugaki M, Namba S. 2003. A single silent substitution in the genome of Apple stem grooving virus causes symptom attenuation. J Gen Virol. 84(Pt 9):2579–2583. doi: 10.1099/vir.0.19179-0.
  • Hirata H, Yamaji Y, Komatsu K, Kagiwada S, Oshima K, Okano Y, Takahashi S, Ugaki M, Namba S. 2010. Pseudo-polyprotein translated from the full-length ORF1 of capillovirus is important for pathogenicity, but a truncated ORF1 protein without variable and CP regions is sufficient for replication. Virus Res. 152(1–2):1–9. doi: 10.1016/j.virusres.2010.03.016.
  • Hu G-J, Dong Y-F, Zhang Z-P, Fan X-D, Fang R, Li Z-N. 2018. Effect of pre-culture on virus elimination from in vitro apple by thermotherapy coupled with shoot tip culture. J. Integrat. Agricult. 17(9):2015–2023. doi: 10.1016/S2095-3119(18)61913-6.
  • Hu G-J, Wang G-P, Wang L-P, Hong N. 2017. The incidence and molecular characteristics of apple stem grooving virus from pear in China. Australasian Plant Pathol. 46(4):305–311. doi: 10.1007/s13313-017-0492-1.
  • Hull R. 2009. Comparative plant virology (5th Edition). Academic press, Amsterdam: Elsevier.
  • Hull R. 2014. Replication of plant viruses. Plant Virol. 341–421. doi: 10.1016/B978-0-12-384871-0.00007-8.
  • Igori D, Lim S, Cho I, Kim H, Lee S, Moon JS. 2020. First report of malus domestica Virus A infecting an apple tree in South Korea. Plant Dis. 104(9):2530–2530. doi: 10.1094/PDIS-01-20-0073-PDN.
  • Igarashi A, Yamagata K, Sugai T, Takahashi Y, Sugawara E, Tamura A, Yaegashi H, Yamagishi N, Takahashi T, Isogai M, et al. 2009. Apple latent spherical virus vectors for reliable and effective virus-induced gene silencing among a broad range of plants including tobacco, tomato, Arabidopsis thaliana, cucurbits, and legumes. Virology. 386(2):407–416. doi: 10.1016/j.virol.2009.01.039.
  • Isogai M, Shimoda R, Nishimura H, Yaegashi H. 2022. Pollen grains infected with apple stem grooving virus serve as a vector for horizontal transmission of the virus. J Gen Plant Pathol. 88(1):81–87. doi: 10.1007/s10327-021-01039-0.
  • Izuishi Y, Isaka N, Li H, Nakanishi K, Kageyama J, Ishikawa K, Shimada T, Masuta C, Yoshikawa N, Kusano H, et al. 2020. Apple latent spherical virus (ALSV)-induced gene silencing in a medicinal plant, Lithospermum erythrorhizon. Sci Rep. 10(1):13555. doi: 10.1038/s41598-020-70469-1.
  • Jia A, Yan C, Yin H, Sun R, Xia F, Gao L, Zhang Y, Li Y. 2021. Small RNA and transcriptome sequencing of a symptomatic peony plant reveals mixed infections with novel viruses. Plant Dis. 105(12):3816–3828. doi: 10.1094/PDIS-01-21-0007-RE.
  • Jo Y, Choi H, Kim S-M, Kim S-L, Lee BC, Cho WK. 2016. Integrated analyses using RNA-Seq data reveal viral genomes, single nucleotide variations, the phylogenetic relationship, and recombination for Apple stem grooving virus. BMC Genomics. 17(1):579. doi: 10.1186/s12864-016-2994-6.
  • Jones RA. 2018. Plant and insect viruses in managed and natural environments: novel and neglected transmission pathways. Adv Virus Res. 101:149–187. doi: 10.1016/bs.aivir.2018.02.006.
  • Kanegae Y, Kumakura N, Shirasu K. 2016. 関 東 部 会 講 演 要 旨. Jpn. J. Phytopathol. 82:25.
  • Kasschau KD, Cronin S, Carrington JC. 1997. Genome amplification and long-distance movement functions associated with the central domain of tobacco etch potyvirus helper component–proteinase. Virology. 228(2):251–262. doi: 10.1006/viro.1996.8368.
  • Kim J, Lal A, Kil E-J, Kwak H-R, Yoon H-S, Choi H-S, Kim M, Ali M, Lee S. 2021. Adaptation and codon-usage preference of apple and pear-infecting apple stem grooving viruses. Microorganisms. 9(6):1111. doi: 10.3390/microorganisms9061111.
  • Kim N-Y, Lee H-J, Kim N-K, Oh J, Lee S-H, Kim H, Moon JS, Jeong R-D. 2019. Survey of major viruses in commercial nursery trees of major pear cultivars in Korea. Res. Plant Dis. 25:43–47.
  • Kim N-Y, Oh J, Lee S-H, Kim H, Moon JS, Jeong R-D. 2018. Rapid and specific detection of apple stem grooving virus by reverse transcription-recombinase polymerase amplification. Plant Pathol J. 34(6):575–579. doi: 10.5423/PPJ.NT.06.2018.0108.
  • Klöcker N, Weissenboeck FP, VAN Dülmen M, Špaček P, Hüwel S, Rentmeister A. 2022. Photocaged 5′ cap analogues for optical control of mRNA translation in cells. Nat Chem. 14(8):905–913. doi: 10.1038/s41557-022-00972-7.
  • Komatsu K, Hirata H, Fukagawa T, Yamaji Y, Okano Y, Ishikawa K, Adachi T, Maejima K, Hashimoto M, Namba S. 2012. Infection of capilloviruses requires subgenomic RNAs whose transcription is controlled by promoter-like sequences conserved among flexiviruses. Virus Res. 167(1):8–15. doi: 10.1016/j.virusres.2012.02.019.
  • Kumar S, Singh RM, Ram R, Badyal J, Hallan V, Zaidi A, Varma A. 2012. Determination of major viral and sub viral pathogens incidence in apple orchards in Himachal Pradesh. Indian J Virol. 23(1):75–79. doi: 10.1007/s13337-011-0056-x.
  • Kuzmitskaya P, Urbanovich OY. 2016. Distribution and genetic diversity of three apple viruses in Belarus. Vestn VOGiS. 20(5):673–682. doi: 10.18699/VJ16.187.
  • Lai Y, Wu X, Lv L, Weng J, Han K, Chen Z, Chen J, Yan F, Zheng H. 2021. Gynura japonica: a new host of apple stem grooving virus and chrysanthemum virus B in China. Plant Dis. 105(11):3770. doi: 10.1094/PDIS-11-20-2512-PDN.
  • Lakatos L, Csorba T, Pantaleo V, Chapman EJ, Carrington JC, Liu YP, Dolja VV, Calvino LF, López-moya JJ, Burgyán J. 2006. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. Embo J. 25(12):2768–2780. doi: 10.1038/sj.emboj.7601164.
  • Lemma B, Xing F, Li S, Zhang Z. 2016. First Report of Apple stem grooving virus, Apple stem pitting virus, and Apple chlorotic leaf spot virus in Apple Trees From Chencha, Ethiopia. Plant Dis. 100(12):2540. doi: 10.1094/PDIS-05-16-0678-PDN.
  • Li L, Wen L, Wang G, Lyu Y, Yang Z, Yang X, Li Q, Hong N. 2022. Seed transmission of three viruses in two pear rootstock species Pyrus betulifolia and P. calleryana. Viruses. 14(3):599. doi: 10.3390/v14030599.
  • Li T, Jiang Z, Zhang L, Tan D, Wei Y, Yuan H, Li T, Wang A. 2016. Apple (Malus domestica) Md ERF 2 negatively affects ethylene biosynthesis during fruit ripening by suppressing Md ACS 1 transcription. Plant J. 88(5):735–748. doi: 10.1111/tpj.13289.
  • Li Z-N, Jelkmann W, Sun P-P, Zhang L. 2020. Construction of full-length infectious cDNA clones of Apple stem grooving virus using Gibson Assembly method. Virus Res. 276:197790. doi: 10.1016/j.virusres.2019.197790.
  • Liebenberg A, Moury B, Sabath N, Hell R, Kappis A, Jarausch W, Wetzel T. 2012. Molecular evolution of the genomic RNA of Apple stem grooving capillovirus. J Mol Evol. 75(3-4):92–101. doi: 10.1007/s00239-012-9518-z.
  • Lin CY, Chang L, Lin YH, Cheng HJ, Wu ML, Hung TH. 2018. Biological and molecular characterization of citrus tatter leaf virus in Taiwan. Plant Pathol. 67(4):995–1008. doi: 10.1111/ppa.12806.
  • Lister R. 1970. Apple stem grooving virus. CMI AAB descriptions of plant viruses. 31. Kew, UK: Commonwealth Mycological Institute.
  • Liu J, Zhang X, Yang Y, Hong N, Wang G, Wang A, Wang L. 2016. Characterization of virus-derived small interfering RNAs in Apple stem grooving virus-infected in vitro-cultured Pyrus pyrifolia shoot tips in response to high temperature treatment. Virol J. 13(1):166. doi: 10.1186/s12985-016-0625-0.
  • Liu J, Zhang X, Zhang F, Hong N, Wang G, Wang A, Wang L. 2015. Identification and characterization of microRNAs from in vitro-grown pear shoots infected with Apple stem grooving virus in response to high temperature using small RNA sequencing. BMC Genomics. 16(1):945. doi: 10.1186/s12864-015-2126-8.
  • Lovisolo O, Accotto GP, Masenga V, Colariccio A. 2003. An isolate of Apple stem grooving virus associated with Cleopatra mandarin fruit intumescence. Fitopatol Bras. 28(1):54–58. doi: 10.1590/S0100-41582003000100008.
  • Ma X, Hong N, Moffett P, Zhou Y, Wang G. 2019. Functional analysis of apple stem pitting virus coat protein variants. Virol J. 16(1):20. doi: 10.1186/s12985-019-1126-8.
  • Macho AP, Lozano-duran R. 2019. Molecular dialogues between viruses and receptor-like kinases in plants. Mol Plant Pathol. 20(9):1191–1195. doi: 10.1111/mpp.12812.
  • Maeda K, Kikuchi T, Kasajima I, Li C, Yamagishi N, Yamashita H, Yoshikawa N. 2020. Virus-induced flowering by apple latent spherical virus vector: effective use to accelerate breeding of grapevine. Viruses. 12(1):70. doi: 10.3390/v12010070.
  • Magome H, Yoshikawa N, Takahashi T, Ito T, Miyakawa T. 1997. Molecular variability of the genomes of capilloviruses from apple, Japanese pear, European pear, and citrus trees. Phytopathology. 87(4):389–396. doi: 10.1094/PHYTO.1997.87.4.389.
  • Magome H, Yoshikawa N, Takahashi T. 1999. Single-strand conformation polymorphism analysis of apple stem grooving capillovirus sequence variants. Phytopathology. 89(2):136–140. doi: 10.1094/PHYTO.1999.89.2.136.
  • Mahmood MA, Naqvi RZ, Rahman SU, Amin I, Mansoor S. 2023. Plant virus-derived vectors for plant genome engineering. Viruses. 15(2):531. doi: 10.3390/v15020531.
  • Malpica JM, Sacristán S, Fraile A, García-Arenal F. 2006. Association and host selectivity in multi-host pathogens. PLoS One. 1(1):e41. doi: 10.1371/journal.pone.0000041.
  • Marais A, Faure C, Theil S, Candresse T. 2018. Molecular characterization of a novel species of capillovirus from Japanese apricot (Prunus mume). Viruses. 10(4):144. doi: 10.3390/v10040144.
  • Martelli GP, Adams MJ, Kreuze JF, Dolja VV. 2007. Family Flexiviridae: a case study in virion and genome plasticity. Annu Rev Phytopathol. 45(1):73–100. doi: 10.1146/annurev.phyto.45.062806.094401.
  • Martínez-Turiño S, Calvo M, Bedoya LC, Zhao M, García JA. 2021. Virus host jumping can be boosted by adaptation to a bridge plant species. Microorganisms. 9(4):805. doi: 10.3390/microorganisms9040805.
  • Medina-Puche L, Tan H, Dogra V, Wu M, Rosas-Diaz T, Wang L, Ding X, Zhang D, Fu X, Kim C, et al. 2020. A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell. 182(5):1109–1124. e25. doi: 10.1016/j.cell.2020.07.020.
  • Méndez-lópez E, Donaire L, Gosálvez B, Díaz-vivancos P, Sánchez-pina MA, Tilsner J, Aranda MA. 2023. Tomato SlGSTU38 interacts with the PepMV coat protein and promotes viral infection. New Phytol. 238(1):332–348. doi: 10.1111/nph.18728.
  • Menzel W, Jelkmann W, Maiss E. 2002. Detection of four apple viruses by multiplex RT-PCR assays with coamplification of plant mRNA as internal control. J Virol Methods. 99(1-2):81–92. doi: 10.1016/s0166-0934(01)00381-0.
  • Miao R, Ye Z, MacFarlane S, Li Y, Mao Q, Tian Y, Deng Z, Sun Z, Yang J, Li J, et al. 2022. The P3N-PIPO protein encoded by wheat yellow mosaic virus is a pathogenicity determinant and promotes its pathogenicity through interaction with NbRLK6 in nicotiana benthamiana. Viruses,. 14(10):2171. doi: 10.3390/v14102171.
  • Mittler E, Dieterle ME, Kleinfelter LM, Slough MM, Chandran K, Jangra RK. 2019. Hantavirus entry: perspectives and recent advances. Adv Virus Res. 104:185–224. doi: 10.1016/bs.aivir.2019.07.002.
  • Mohammadlou M, Koolivand D, Hajizadeh M. 2022. Detection, phylogenetic and population genetic analysis of Apple stem grooving virus based on coat protein gene. J Appl Res Plant Protect. 11:67–78.
  • Moreno-Pérez MG, García-Luque I, Fraile A, García-Arenal F. 2016. Mutations that determine resistance breaking in a plant RNA virus have pleiotropic effects on its fitness that depend on the host environment and on the type, single or mixed, of infection. J Virol. 90(20):9128–9137. doi: 10.1128/JVI.00737-16.
  • Nabi SU, Baranwal VK, Yadav MK, Rao GP. 2020. Association of Apple necrotic mosaic virus (ApNMV) with mosaic disease in commercially grown cultivars of apple (Malus domestica Borkh) in India. 3 Biotech. 10(3):122. doi: 10.1007/s13205-020-2117-6.
  • Nagy PD, Pogany J, Xu K. 2016. Cell-free and cell-based approaches to explore the roles of host membranes and lipids in the formation of viral replication compartment induced by tombusviruses. Viruses. 8(3):68. doi: 10.3390/v8030068.
  • Nagy PD. 2011. The roles of host factors in tombusvirus RNA recombination. Adv Virus Res. 81:63–84. doi: 10.1016/B978-0-12-385885-6.00008-0.
  • Nakazono-Nagaoka E, Fujikawa T, Uechi N, Iwanami T. 2015. Vein enation symptom in Yuzu is caused by Citrus vein enation virus. Jpn J Phytopathol. 81(4):341–345. doi: 10.3186/jjphytopath.81.341.
  • Nickel O, Fajardo T, Candresse T. 2020. First report on detection of three bunya-like viruses in apples in Brazil. Plant Disease. 104(11):3088–3088. doi: 10.1094/PDIS-02-20-0283-PDN.
  • Nickel O, Fajardo TV, Jelkmann W, Kuhn GB. 2001. Sequence analysis of the capsid protein gene of an isolate of Apple stem grooving virus, and its survey in Southern Brazil. Fitopatol Bras. 26(3):655–659. doi: 10.1590/S0100-41582001000300014.
  • Nickel O, Targon ML, Fajardo TV, Machado MA, Trivilin AP. 2004. Polyclonal antibodies to the coat protein of Apple stem grooving virus expressed in Escherichia coli: production and use in immunodiagnosis. Fitopatol Bras. 29(5):558–562. doi: 10.1590/S0100-41582004000500017.
  • Ohira K, Namba S, Rozanov M, Kusumi T, Tsuchizaki T. 1995. Complete sequence of an infectious full-length cDNA clone of citrus tatter leaf capillovirus: comparative sequence analysis of capillovirus genomes. J Gen Virol. 76 (Pt 9):2305–2309. doi: 10.1099/0022-1317-76-9-2305.
  • Olsthoorn RC, Mertens S, Brederode FT, Bol JF. 1999. A conformational switch at the 3′ end of a plant virus RNA regulates viral replication. Embo J. 18(17):4856–4864. doi: 10.1093/emboj/18.17.4856.
  • Pagán I, Montes N, Milgroom MG, García-Arenal F. 2014. Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host. PLoS Pathog. 10(7):e1004293. doi: 10.1371/journal.ppat.1004293.
  • Pagán I. 2022. Transmission through seeds: the unknown life of plant viruses. PLoS Pathog. 18(8):e1010707. doi: 10.1371/journal.ppat.1010707.
  • Pallas V, García JA. 2011. How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol. 92(12):2691–2705. doi: 10.1099/vir.0.034603-0.
  • Peng C-W, Peremyslov VV, Snijder EJ, Dolja VV. 2002. A replication-competent chimera of plant and animal viruses. Virology. 294(1):75–84. doi: 10.1006/viro.2001.1306.
  • Ramanathan A, Robb GB, Chan S-H. 2016. mRNA capping: biological functions and applications. Nucleic Acids Res. 44(16):7511–7526. doi: 10.1093/nar/gkw551.
  • Rampersad S, Tennant P. 2018. Replication and expression strategies of viruses. Viruses. 55–82. doi: 10.1016/B978-0-12-811257-1.00003-6.
  • Rani A, Suman R, Chandel V, Srivastava A, Noorani MS, Rishi N, Dhir S. 2021. Biological and molecular characterization of two isolates of apple stem grooving virus revealed distinct properties and indicates virus emergence driven by recombination. J Phytopathol. 169(11-12):740–751. doi: 10.1111/jph.13046.
  • Ranji A, Boris-Lawrie K. 2010. RNA helicases: emerging roles in viral replication and the host innate response. RNA Biol. 7(6):775–787. doi: 10.4161/rna.7.6.14249.
  • Ruark-Seward CL, Bonville B, Kennedy G, Rasmussen DA. 2020. Evolutionary dynamics of Tomato spotted wilt virus within and between alternate plant hosts and thrips. Sci Rep. 10(1):15797. doi: 10.1038/s41598-020-72691-3.
  • Rubio L, Galipienso L, Ferriol I. 2020. Detection of plant viruses and disease management: relevance of genetic diversity and evolution. Front Plant Sci. 11:1092. doi: 10.3389/fpls.2020.01092.
  • Salánki K, Kiss L, Gellért Á, Balázs E. 2011. Identification a coat protein region of cucumber mosaic virus (CMV) essential for long-distance movement in cucumber. Arch Virol. 156(12):2279–2283. doi: 10.1007/s00705-011-1104-y.
  • Sanjuán R, Domingo-Calap P. 2021. Genetic diversity and evolution of viral populations. Encycl Virol. 53–61. doi: 10.1016/B978-0-12-809633-8.20958-8.
  • Schneider WL, Roossinck MJ. 2001. Genetic diversity in RNA virus quasispecies is controlled by host-virus interactions. J Virol. 75(14):6566–6571. doi: 10.1128/JVI.75.14.6566-6571.2001.
  • Schönegger D, Moubset O, Margaria P, Menzel W, Winter S, Roumagnac P, Marais A, Candresse T. 2023. Benchmarking of virome metagenomic analysis approaches using a large, 60+ members, viral synthetic community. J Virol. 97(11):e01300-23. doi: 10.1128/jvi.01300-23.
  • Senshu H, Yamaji Y, Minato N, Shiraishi T, Maejima K, Hashimoto M, Miura C, Neriya Y, Namba S. 2011. A dual strategy for the suppression of host antiviral silencing: two distinct suppressors for viral replication and viral movement encoded by potato virus M. J Virol. 85(19):10269–10278. doi: 10.1128/JVI.05273-11.
  • Sharma N, Handa A, Gupta BK. 2018. Serological evidence of mixed infection of major apple viruses in wet and dry temperate zone of himachal Pradesh. Plant Disease Res. 33:202–207.
  • Shi X, Zhang Z, Zhang C, Zhou X, Zhang D, Liu Y. 2021. The molecular mechanism of efficient transmission of plant viruses in variable virus–vector–plant interactions. Hortic Plant J. 7(6):501–508. doi: 10.1016/j.hpj.2021.04.006.
  • Shim H, Min Y, Hong S, Kwon M, Kim D, Kim H, Choi Y, Lee S, Yang J. 2004. Nucleotide sequences of a Korean isolate of apple stem grooving virus associated with black necrotic leaf spot disease on pear (Pyrus pyrifolia). Mol Cells (Spring Sci Bus Med BV). 18(2):192–199.
  • Shim HK, Hwang KH, Shim CK. 2006. The pear black necrotic leaf spot disease virus transmitted by talaromycesflavus displays pathogenicity similar to apple stem grooving virus strains. Plant Pathol J. 22:255–259.
  • Shim SY, Jung YC, Le VP, Son DW, Ryoo E, Shim JO, Lim I, Kim W. 2010. Genetic variation of G4P [6] rotaviruses: evidence for novel strains circulating between the hospital and community. J Med Virol. 82(4):700–706. doi: 10.1002/jmv.21698.
  • Shimura H, Pantaleo V, Ishihara T, Myojo N, Inaba J-I, Sueda K, Burgyán J, Masuta C. 2011. A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog. 7(5):e1002021. doi: 10.1371/journal.ppat.1002021.
  • Shokri S, Shujaei K, Gibbs AJ, Hajizadeh M. 2023. Evolution and biogeography of apple stem grooving virus. Virol J. 20(1):105. doi: 10.1186/s12985-023-02075-2.
  • Silva J, Melo F, Elena S, Candresse T, Sabanadzovic S, Tzanetakis I, Blouin A, Villamor D, Mollov D, Constable F, et al. 2022. Virus classification based on in-depth sequence analyses and development of demarcation criteria using the Betaflexiviridae as a case study. J Gen Virol. 103(11). doi: 10.1099/jgv.0.001806.
  • Singh S, Dhyani D, Nag A, Sharma R. 2017. Morphological and molecular characterization revealed high species level diversity among cultivated, introduced and wild roses (Rosa sp.) of western Himalayan region. Genet Resour Crop Evol. 64(3):515–530. doi: 10.1007/s10722-016-0377-0.
  • Song Y, Zheng Y, Li L, Wang G, Hong N. 2010. Prokaryotic expression of cp genes from Apple stem grooving virus and production of antisera against recombinant coat proteins. J Fruit Sci. 27:752–756.
  • Souza EB, Nickel O, Fajardo TV, Silva JM, Barros DR. 2017. Biological and molecular characterization of two Brazilian isolates of Apple stem grooving virus. Trop Plant Pathol. 42(5):391–396. doi: 10.1007/s40858-017-0163-3.
  • Suman R, Rishi N, Dhir S, Hallan V, Chandel V. 2023. Molecular characterization and variability analyses of apple stem pitting virus and apple stem grooving virus isolates infecting apple in Kashmir, India. Indian Phytopathol. 76(1):233–241. doi: 10.1007/s42360-022-00586-6.
  • Tan S-H, Osman F, Bodaghi S, Dang T, Greer G, Huang A, Hammado S, Abu-Hajar S, Campos R, Vidalakis G. 2019. Full genome characterization of 12 citrus tatter leaf virus isolates for the development of a detection assay. PLoS One. 14(10):e0223958. doi: 10.1371/journal.pone.0223958.
  • Tatineni S, Afunian MR, Gowda S, Hilf ME, BAR-Joseph M, Dawson WO. 2009. Characterization of the 5′-and 3′-terminal subgenomic RNAs produced by a capillovirus: evidence for a CP subgenomic RNA. Virology. 385(2):521–528. doi: 10.1016/j.virol.2008.12.024.
  • Tatineni S, Afunian MR, Hilf ME, Gowda S, Dawson WO, Garnsey SM. 2009. Molecular characterization of Citrus tatter leaf virus historically associated with Meyer lemon trees: complete genome sequence and development of biologically active in vitro transcripts. Phytopathology. 99(4):423–431. doi: 10.1094/PHYTO-99-4-0423.
  • Tatineni S, Alexander J, Kovacs F. 2024. The HC-Pro cistron of Triticum mosaic virus is dispensable for systemic infection in wheat but is required for symptom phenotype and efficient genome amplification. Virus Res. 339:199277. doi: 10.1016/j.virusres.2023.199277.
  • Tatineni S, Robertson CJ, Garnsey SM, Dawson WO. 2011. A plant virus evolved by acquiring multiple nonconserved genes to extend its host range. Proc Natl Acad Sci USA. 108(42):17366–17371. doi: 10.1073/pnas.1113227108.
  • Tatineni S, Qu F, Li R, Morris TJ, French R. 2012. Triticum mosaic poacevirus enlists P1 rather than HC-Pro to suppress RNA silencing-mediated host defense. Virology. 433(1):104–115. doi: 10.1016/j.virol.2012.07.016.
  • Terauchi H, Magome H, Yoshikawa N, Takahashi T, Inouy N. 1997. Construction of an infectious cDNA clone of the apple stem grooving capillovirus (isolate Li-23) genome containing a cauliflower mosaic virus 35S RNA promoter. Ann Phytopathol Soc Jpn. 63:432–436.
  • Udovychenko К. 2015. Assesment of genetic ralationship of some Ukrainian isolates OD apple viruses. Sci Suppl Ukraine. 8(57):1–8.
  • Umer M, Liu J, You H, Xu C, Dong K, Luo N, Kong L, Li X, Hong N, Wang G, et al. 2019. Genomic, morphological and biological traits of the viruses infecting major fruit trees. Viruses. 11(6):515. doi: 10.3390/v11060515.
  • Uranga M, Aragonés V, García A, Mirabel S, Gianoglio S, Presa S, Granell A, Pasin F, Daròs J-A. 2024. RNA virus-mediated gene editing for tomato trait breeding. Horticult Res. 11(1):uhad279. doi: 10.1093/hr/uhad279.
  • Uranga M, Daròs JA. 2023. Tools and targets: the dual role of plant viruses in CRISPR–Cas genome editing. Plant Genome. 16(2):e20220. doi: 10.1002/tpg2.20220.
  • Visser M, Maree HJ, D Jasper GR, Burger JT. 2014. High through-put sequencing reveals small RNAs involved in ASGV infection. BMC Genomics. 15(1):568. doi: 10.1186/1471-2164-15-568.
  • Vogler H, Kwon M-O, Dang V, Sambade A, Fasler M, Ashby J, Heinlein M. 2008. Tobacco mosaic virus movement protein enhances the spread of RNA silencing. PLoS Pathog. 4(4):e1000038. doi: 10.1371/journal.ppat.1000038.
  • Wang H, Cui X, Cai X, An T. 2022. Recombination in positive-strand RNA viruses. Front Microbiol. 13:870759. doi: 10.3389/fmicb.2022.870759.
  • Wang Y, Zhao C-L, Li J-Y, Liang Y-J, Yang R-Q, Liu J-Y, Ma Z, Wu L. 2018. Evaluation of biochemical components and antioxidant capacity of different kiwifruit (Actinidia spp.) genotypes grown in China. Biotechnol Biotechnol Equip. 32(3):558–565. doi: 10.1080/13102818.2018.1443400.
  • Wu C-Y, Nagy PD. 2020. Role reversal of functional identity in host factors: dissecting features affecting pro-viral versus antiviral functions of cellular DEAD-box helicases in tombusvirus replication. PLoS Pathog. 16(10):e1008990. doi: 10.1371/journal.ppat.1008990.
  • Xing F, Robe BL, Zhang Z, Wang H, Li S. 2018. Genomic analysis, sequence diversity, and occurrence of apple necrotic mosaic virus, a novel ilarvirus associated with mosaic disease of apple trees in China. Plant Dis. 102(9):1841–1847. doi: 10.1094/PDIS-10-17-1580-RE.
  • Xuan Z-Y, Zhang S, Ping L, Yang F-Y, Chen H-M, Liu K-H, Yan Z, Li Z-A, Zhou C-Y, Cao M-J. 2022. Apple stem grooving virus is associated with leaf yellow mottle mosaic disease on Citrus grandis cv. Huangjinmiyou in China. J Integrat Agricult. 21(7):2031–2041. doi: 10.1016/S2095-3119(21)63823-6.
  • Yamagishi N, Sasaki S, Yamagata K, Komori S, Nagase M, Wada M, Yamamoto T, Yoshikawa N. 2011. Promotion of flowering and reduction of a generation time in apple seedlings by ectopical expression of the Arabidopsis thaliana FT gene using the Apple latent spherical virus vector. Plant Mol Biol. 75(1-2):193–204. doi: 10.1007/s11103-010-9718-0.
  • Yang F, Wang G, Xu W, Hong N. 2017. A rapid silica spin column-based method of RNA extraction from fruit trees for RT-PCR detection of viruses. J Virol Methods. 247:61–67. doi: 10.1016/j.jviromet.2017.05.020.
  • Yoshikawa N, Sasaki E, Kato M, Takahashi T. 1992. The nucleotide sequence of apple stem grooving capillovirus genome. Virology. 191(1):98–105. doi: 10.1016/0042-6822(92)90170-t.
  • Zeng T, Liao P, Zheng C, Gao H, Ye X, Zhou C, Zhou Y. 2023. The interaction between the lemon ribosomal protein ClRPS9-2 and citrus yellow vein clearing virus coat protein affects viral infection and gene silencing suppressor activity. Mol Plant Pathol. 24(9):1047–1062. doi: 10.1111/mpp.13347.
  • Zhang Jinzhu ZC, Junyuan H, Chongling D, Baoshan C, Muqing Z. 2021. Investigation and the genetic diversity analysis of the pathogenic virus causing citrus tatter leaf disease and citrus leaf spot disease in Guangxi. Chinese J Trop Crops. 42:1414–1423.
  • Zhao L, Hao X, Liu P, Wu Y. 2012. Complete sequence of an Apple stem grooving virus (ASGV) isolate from China. Virus Genes. 45(3):596–599. doi: 10.1007/s11262-012-0799-5.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.