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Archives of Virology
Published in: Archives of Virology 9/2017

01-09-2017 | Original Article

Genome-wide identification of cucumber green mottle mosaic virus-responsive microRNAs in watermelon

Authors: Yuyan Sun, Xiaowei Niu, Min Fan

Published in: Archives of Virology | Issue 9/2017

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Abstract

Cucumber green mottle mosaic virus (CGMMV) is a damaging pathogen that attacks crop plants belonging to the family Cucurbitaceae. Little is known about the regulatory role of microRNAs (miRNAs) in response to CGMMV infection. To identify CGMMV-responsive miRNAs, two sRNA libraries from mock-inoculated and CGMMV-infected watermelon leaves were constructed and sequenced using Solexa sequencing technology. In total, 471 previously known and 1,809 novel miRNAs were obtained, of which 377 known and 246 novel miRNAs were found to be differentially expressed during CGMMV infection. The target genes for the CGMMV-responsive known miRNAs are active in diverse biological processes, including cell wall modulation, plant hormone signaling, defense-related protein induction, primary and secondary metabolism, regulation of virus replication, and intracellular transport. The expression patterns of some CGMMV-responsive miRNAs and their corresponding targets were confirmed by RT-qPCR. One target gene for miR156a-5p was verified by 5’-RNA-ligase-mediated rapid amplification of cDNA ends (5’-RLM-RACE) analysis. The results of this study provide further insights into the miRNA-mediated regulatory network involved in the response to viral infection in watermelon and other cucurbit crops.
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Literature
1.
Collins JK, Wu GY, Perkins-Veazie P, Spears K, Claypool PL, Baker RA, Clevidence BA (2007) Watermelon consumption increases plasma arginine concentrations in adults. Nutrition 23:261–266CrossRefPubMed
2.
Liu HW, Luo LX, Liang CQ, Jiang N, Liu PF, Li JQ (2015) High-throughput sequencing identifies novel and conserved cucumber (Cucumis sativus L.) microRNAs in response to cucumber green mottle mosaic virus infection. PLoS One 10:e0129002CrossRefPubMedPubMedCentral
3.
Tesoriero LA, Chambers G, Srivastava M, Smith S, Conde B, Tran-Nguyen LTT (2016) First report of cucumber green mottle mosaic virus in Australia. Australas Plant Dis Notes 11:1CrossRef
4.
Tian T, Posis K, Maroon-Lango CJ, Mavrodieva V, Haymes S, Pitman TL, Falk BW (2014) First report of cucumber green mottle mosaic virus on melon in the United States. Plant Dis 98:1163CrossRef
5.
Liu HW, Luo LX, Li JQ, Liu PF, Chen XY, Hao JJ (2014) Pollen and seed transmission of cucumber green mottle mosaic virus in cucumber. Plant Pathol 63:72–77CrossRef
6.
Ainsworth GC (1935) Mosaic disease of the cucumber. Ann Appl Biol 22:55–67CrossRef
7.
Celix A, Luis-Arteaga M, Rodriguez-Cerezo E (1996) First report of cucumber green mottle mosaic tobamovirus infecting greenhouse-grown cucumber in Spain. Plant Dis 80:1303CrossRef
8.
Varveri C, Vassilakos N, Bem F (2002) Characterization and detection of cucumber green mottle mosaic virus in Greece. Phytoparasitica 30(5):93–501CrossRef
9.
Inouye T, Inouye N, Asatani M, Mitsuhata K (1967) Studies on cucumber green mottle mosaic virus in Japan. Ber Ohara Inst Landw Biol 14:49–69
10.
Lee KW, Lee BC, Park HC, Lee YS (1990) Occurrence of cucumber green mottle mosaic virus disease of watermelon in Korea. Korean J Plant Pathol 6:250–255
11.
Qin BX, Cai JH, Liu ZM, Chen YH, Zhu GN, Huang FX (2005) Preliminary identification of a cucumber green mottle mosaic virus infecting pumpkin. Plant Quar 4:198–200 (In Chinese)
12.
Antignus Y, Pearlsman M, Ben-Yoseph R, Cohen S (1990) Occurrence of a variant of cucumber green mottle mosaic virus in Israel. Phytoparasitica 18:50–56CrossRef
13.
Al-Shahwan IM, Abdalla OA (1992) A strain of cucumber green mottle mosaic virus (CGMMV) from bottlegourd in Saudi Arabia. J Phytopathol 134:152–156CrossRef
14.
Ling K, Li R, Zhang W (2014) First report of cucumber green mottle mosaic virus infecting greenhouse cucumber in Canada. Plant Dis 98:701
15.
Wu HJ, Qin BX, Chen HY, Peng B, Cai JH, Gu QS (2011) The rate of seed contamination and transmission of cucumber green mottle mosaic virus in watermelon and melon. Sci Agric Sin 44:1527–1532
16.
Li J, Gu Q (2015) Research progress on transmission modes of cucumber green mottle mosaic virus. China Veg 1:13–18 (in Chinese)
17.
Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217CrossRefPubMed
18.
Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148CrossRefPubMed
19.
20.
Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J (2012) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci USA 109:1790–1795CrossRefPubMedPubMedCentral
21.
Du P, Wu J, Zhang J, Zhao S, Zheng H, Gao G, Wei LP, Li Y (2011) Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors. PLoS Pathog 7:e1002176CrossRefPubMedPubMedCentral
22.
Yin X, Wang J, Cheng H, Wang X, Yu D (2013) Detection and evolutionary analysis of soybean miRNAs responsive to soybean mosaic virus. Planta 237:1213–1225CrossRefPubMed
23.
Feng J, Liu S, Wang M, Lang Q, Jin C (2014) Identification of microRNAs and their targets in tomato infected with cucumber mosaic virus based on deep sequencing. Planta 240:1335–1352CrossRefPubMed
24.
Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967CrossRefPubMed
25.
Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A (2005) Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33:121–124CrossRef
26.
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2011) GenBank. Nucleic Acids Res 39:D32–D37CrossRefPubMed
27.
Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:154–158CrossRef
28.
Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao XF, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Scott Poethig R, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu J (2008) Criteria for annotation of plant microRNAs. Plant Cell 20:3186–3190CrossRefPubMedPubMedCentral
29.
30.
Eldem V, Akcay UC, Ozhuner E, Bakir Y, Uranbey S, Unver T (2012) Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by high-throughput deep sequencing. PLoS One 7:e50298CrossRefPubMedPubMedCentral
31.
Li BS, Qin YR, Duan H, Yin WL, Xia XL (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779CrossRefPubMedPubMedCentral
32.
Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221CrossRefPubMed
33.
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527CrossRefPubMed
34.
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:182–185CrossRef
35.
Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39:519–525CrossRefPubMed
36.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefPubMed
37.
Ramesh SV, Ratnaparkhe MB, Kumawat G, Gupta GK, Husain SM (2014) Plant miRNAome and antiviral resistance: a retrospective view and prospective challenges. Virus Genes 48:1–14CrossRefPubMed
38.
He X, Fang Y, Feng L, Guo H (2008) Characterization of conserved novel microRNAs and their targets, including a TuMV-induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS Lett 582:2445–2452CrossRefPubMed
39.
Yang J, Zheng SL, Zhang HM, Liu XY, Li J, Li JM, Chen JP (2014) Analysis of small RNAs derived from Chinese wheat mosaic virus. Arch Virol 159:3077–3082CrossRefPubMed
40.
Li Y, Deng C, Shang Q, Zhao X, Liu X, Zhou Q (2016) Characterization of siRNAs derived from cucumber green mottle mosaic virus in infected cucumber plants. Arch Virol 161:455–458CrossRefPubMed
41.
42.
Wang XB, Wu QF, Ito T, Cillo F, Li WX, Chen X, Yu J, Ding S (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:484–489CrossRefPubMed
43.
Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219CrossRefPubMedPubMedCentral
44.
Bazzini AA, Hopp HE, Beachy RN, Asurmendi S (2007) Infection and co-accumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc Natl Acad Sci USA 104:12157–12162CrossRefPubMedPubMedCentral
45.
van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defence-related proteins in infected plants. Annu Rev Phytopathol 44:35–162
46.
Lu S, Li Q, Wei H, Chang MJ, Tunlaya AS, Kim H, Liu J, Song J, Sun Y, Yuan L, Yeh T, Peszlen I, Ralph J, Sederoff SR, Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 110:10848–10853CrossRefPubMedPubMedCentral
47.
Rhee Y, Tzfira T, Chen M, Waigmann E, Citovsky V (2001) Cell-to-cell movement of Tobacco mosaic virus: enigmas and explanations. Mol Plant Pathol 1:33–39CrossRef
48.
Kima W, Kima J, Koe J, Kimd J, Hana K (2013) Transcription factor MYB46 is an obligate component of the transcriptional regulatory complex for functional expression of secondary wall-associated cellulose synthases in Arabidopsis thaliana. J Plant Physiol 170:1374–1378CrossRef
49.
Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defences in Arabidopsis. Plant Cell 19:1665–1681CrossRefPubMedPubMedCentral
50.
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 82:2477–2485CrossRefPubMed
51.
Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JD (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18:650–655CrossRefPubMed
52.
McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959CrossRefPubMedPubMedCentral
53.
Siemens J, Keller I, Sarx J, Kunz S, Schuller A, Nagel W, Schmulling T, Parniske M, Ludwig-Muller J (2006) Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol Plant Microbe Interact 19:480–494CrossRefPubMed
54.
55.
Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45CrossRefPubMed
56.
Ray S, Yumak H, Domashevskiy A, Khan MA, Gallie DR, Goss DJ (2006) Tobacco etch virus mRNA preferentially binds wheat germ eukaryotic initiation factor (eIF) 4G rather than eIFiso4G. J Biol Chem 281:35826–35834CrossRefPubMed
57.
Ayme V, Petit-Pierre J, Souche S, Palloix A, Moury B (2007) Molecular dissection of the potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. J Gen Virol 88:1594–1601CrossRefPubMed
58.
Albar L, Bangratz-Reyser M, Hebrard E, Ndjiondjop MN, Jones M, Ghesquiere A (2006) Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant J 47:417–426CrossRefPubMed
59.
Boisnard A, Albar L, Thiéméle D, Rondeau M, Ghesquière A (2007) Evaluation of genes from eIF4E and eIF4G multigenic families as potential candidates for partial resistance QTLs to Rice yellow mottle virus in rice. Theor Appl Genet 116:53–62CrossRefPubMed
60.
61.
Sampietro DA, Fauguel CM, Vattuone MA, Presello DA, Catalán CAN (2013) Phenylpropanoids from maize pericarp: resistance factors to kernel infection and fumonisin accumulation by Fusarium verticillioides. Eur J Plant Pathol 135:105–113CrossRef
62.
Wang J, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749CrossRefPubMed
63.
Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522CrossRefPubMedPubMedCentral
64.
Mao H, Yu L, Li Z, Yan Y, Han R, Ma M (2016) Genome-wide analysis of the SPL family transcription factors and their responses to abiotic stresses in maize. Plant Gene 6:1–12CrossRef
65.
Alizadeh F, Abdullah SNS, Chong P, Selamat AB (2014) Expression analysis of fatty acid biosynthetic pathway genes during interactions of oil palm (Elaeis guineensis Jacq.) with the pathogenic Ganoderma boninense and symbiotic Trichoderma harzianum fungal organisms. Plant Mol Biol Rep 32:70–81CrossRef
66.
Nakaune R, Hamamoto H, Imada J, Akutsu K, Hibi T (2002) A novel ABC transporter gene, PMR5, is involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Mol Genet Genom 267:179–185CrossRef
67.
Wang Y, Chai C, Valliyodan B, Maupin C, Annen B, Nguyen HT (2015) Genome-wide analysis and expression profiling of the PIN auxin transporter gene family in soybean (Glycine max). BMC Genom 16:951CrossRef
68.
Howarth JR, Fourcroy P, Davidian J, Smith FW, Hawkesford MJ (2003) Cloning of two contrasting high-affinity sulfate transporters from tomato induced by low sulfate and infection by the vascular pathogen Verticillium dahliae. Planta 218:58–64CrossRefPubMed
69.
Joko T, Hirata H, Tsuyumu S (2007) A sugar transporter (MfsX) is also required by Dickeya dadantii 3937 for in planta fitness. J Gen Plant Pathol 73:274–280CrossRef
70.
Eybishtz A, Peretz Y, Sade D, Gorovits R, Czosnek H (2010) Tomato yellow leaf curl virus infection of a resistant tomato line with a silenced sucrose transporter gene LeHT1 results in inhibition of growth, enhanced virus spread, and necrosis. Planta 231:537–548CrossRefPubMed
Metadata
Title
Genome-wide identification of cucumber green mottle mosaic virus-responsive microRNAs in watermelon
Authors
Yuyan Sun
Xiaowei Niu
Min Fan
Publication date
01-09-2017
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 9/2017
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-017-3401-6

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