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Journal of Integrative Agriculture  2022, Vol. 21 Issue (9): 2641-2651    DOI: 10.1016/j.jia.2022.07.020
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Tomato mottle mosaic virus: characterization, resistance gene effectiveness, and quintuplex RT-PCR detection system
Carlos Kwesi TETTEY*, YAN Zhi-yong*, MA Hua-yu, ZHAO Mei-sheng, GENG Chao, TIAN Yan-ping, LI Xiang-dong
Shandong Provincial Key Laboratory of Agricultural Microbiology, College of Plant Protection, Shandong Agricultural University, Tai’an 271018, P.R.China
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本研究中,我们首先测定了中国山东省潍坊市番茄果实采集到的ToMMV山东分离物(ToMMV-SD)的症状特点和基因组特性。ToMMV-SD在番茄叶片上引起严重的花叶、斑驳和坏死,在果实上引起黄斑和坏死斑。ToMMV-SD全长基因组包括6399个核苷酸(登录号:NW373515),在基因组水平上与美国分离物SC13-051一致率最高,为99.5%。构建的ToMMV-SD侵染性克隆在本氏烟(Nicotiana benthamiana)叶片引起明显的花叶和坏死。ToMMV-SD可侵染一些含有抗性基因Tm-22的商业化番茄品种和含有抗性基因L的辣椒品种。茄子(Solanum melongena)和大白菜(Brassica pekinensis)表现斑驳症状,中烟100(N. tabacum cv. Zhongyan 100)表现为无症侵染。ToMMV-SD不能侵染小白菜(Brassica rapa ssp. chinensis)、萝卜(Raphanus sativus)、原种28-2豇豆(Vigna unguiculata cv. Yuanzhong 28-2)、含有N基因的珊西烟(N. tabacum cv. Xanthi NN)和Tm-22转基因本氏烟。建立的五重RT-PCR系统能够将ToMMV与番茄花叶病毒、番茄褐色皱果病毒、烟草花叶病毒和番茄斑萎病毒区分,检测下限达到0.02 pg。这些结果对ToMMV的快速诊断和防控具有积极作用


Tomato mottle mosaic virus (ToMMV), an economically important species of the genus Tobamovirus, causes significant loss in yield and quality of tomato fruits.  Here, we identified the Shandong isolate of ToMMV (ToMMV-SD) collected from symptomatic tomato fruits in Weifang, Shandong Province of China.  ToMMV-SD caused symptoms such as severe mosaic, mottling, and necrosis of tomato leaves, yellow spot and necrotic lesions on tomato fruits.  The obtained full genome of ToMMV-SD was 6 399 nucleotides (accession number MW373515) and had the highest identity of 99.5% with that of isolate SC13-051 from the United States of America at the genomic level.  The infectious clone of ToMMV-SD was constructed and induced clear mosaic and necrotic symptoms onto Nicotiana benthamiana leaves.  Several commercial tomato cultivars, harboring Tm-22 resistance gene, and pepper cultivars, containing L resistance gene, were susceptible to ToMMV-SD.  Plants of Solanum melongena (eggplant) and Brassica pekinensis (napa cabbage) showed mottling symptoms, while Ntabacum cv. Zhongyan 100 displayed latent infection.  ToMMV-SD did not infect plants of N. tabacum cv. Xanthi NN, Brassica rapa ssp. chinensis (bok choy), Raphanus sativus (radish), Vigna unguiculata cv. Yuanzhong 28-2 (cowpea), or Tm-22 transgenic N. benthamiana.  A quintuplex RT-PCR system differentiated ToMMV from tomato mosaic virus, tomato brown rugose fruit virus, tobacco mosaic virus, and tomato spotted wilt virus, with the threshold amount of 0.02 pg.  These results highlight the threat posed by ToMMV to tomato and pepper cultivation and offer an efficient detection system for the simultaneous detection of four tobamoviruses and tomato spotted wilt virus infecting tomato plants in the field. 

Keywords:  host range        multiplex RT-PCR        resistance genes       symptom        Tobamovirus        tomato mottle mosaic virus  
Received: 16 September 2021   Accepted: 26 October 2021
Fund: This study was supported by the grants from the National Natural Science Foundation of China (32072387), and the ‘Taishan Scholar’ Construction Project, China (TS201712023).
About author:  Carlos Kwesi TETTEY, E-mail:; YAN Zhi-yong, E-mail:; Correspondence LI Xiang-dong, Tel: +86-538-8242523, Fax: +86-538-8226399, E-mail:; TIAN Yan-ping, E-mail: * These authors contributed equally to this study.

Cite this article: 

Carlos Kwesi TETTEY, YAN Zhi-yong, MA Hua-yu, ZHAO Mei-sheng, GENG Chao, TIAN Yan-ping, LI Xiang-dong . 2022. Tomato mottle mosaic virus: characterization, resistance gene effectiveness, and quintuplex RT-PCR detection system. Journal of Integrative Agriculture, 21(9): 2641-2651.

Ambrós S, Martínez F, Ivars P, Hernández C, de la Iglesia F, Elena S F. 2017. Molecular and biological characterization of an isolate of Tomato mottle mosaic virus (ToMMV) infecting tomato and other experimental hosts in eastern Spain. European Journal of Plant Pathology, 149, 261–268. 
Chai A L, Chen L D, Li B J, Xie X W, Shi Y X. 2018. First report of a mixed infection of tomato mottle mosaic virus and tobacco mild green mosaic virus on eggplants in China. Plant Disease, 102, 2668.
Che H Y, Luo D Q, Cao X R. 2018. First report of tomato mottle mosaic virus in tomato crops in China. Plant Disease, 102, 2051. 
Fidan H, Sarikaya P, Yildiz K, Topkaya B, Erkis G, Calis O. 2021. Robust molecular detection of the new tomato brown rugose fruit virus in infected tomato and pepper plants from Turkey. Journal of Integrative Agriculture, 20, 2170–2179. 
Hak H, Spiegelman Z. 2021. The Tomato brown rugose fruit virus movement protein overcomes Tm-22 resistance in tomato while attenuating viral transport. Molecular Plant–Microbe Interactions, 50, 529–534.
Hall T A. 1999. Bioedit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/ NT. Nucleic Acids Symposium Series, 41, 95–98. 
Hall T J. 1980. Resistance at the Tm-2 locus in the tomato to tomato mosaic virus. Euphytica, 29, 189–197. 
Jacobi V, Bachand G D, Hamelin R C, Castello J D. 1998. Development of a multiplex immunocapture RT-PCR assay for detection and differentiation of tomato and tobacco mosaic tobamoviruses. Journal of Virological Methods, 74, 167–178. 
Kobayashi M, Yamamoto-Katou A, Katou S, Hirai K, Meshi T, Ohashi Y, Mitsuhara I. 2011. Identification of an amino acid residue required for differential recognition of a viral movement protein by the Tomato mosaic virus resistance gene Tm-22. Journal of Plant Physiology, 168, 1142–1145.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. 
Kumar S, Udaya Shankar A C, Nayaka S C, Lund O S, Prakash H S. 2011. Detection of Tobacco mosaic virus and Tomato mosaic virus in pepper and tomato by multiplex RT-PCR. Letters in Applied Microbiology, 53, 359–363.
Lanfermeijer F C, Dijkhuis J, Sturre M J G, De Haan P, Hille J. 2003. Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-22 from Lycopersicon esculentum. Plant Molecular Biology, 52, 1037–1049.
Lee J D, Han J H, Yoon J B. 2012. A set of allele-specific markers linked to L locus resistant to tobamovirus in Capsicum spp. Korean Journal of Horticultural Science and Technology, 30, 286–293.
Li R, Gao S, Fei Z, Ling K S. 2013. Complete genome sequence of a new Tobamovirus naturally infecting tomatoes in Mexico. Genome Announcements, 1, 4–5. 
Li Y, Tan G, Xiao L, Zhou W, Lan P, Chen X, Liu Y, Li R, Li F. 2021. A multiyear survey and identification of pepper- and tomato-infecting viruses in Yunnan Province, China. Frontiers in Microbiology, 12, 623875.
Li Y, Zhou W P, Lu S Q, Chen D R, Dai J H, Guo Q Y, Liu Y, Li F, Tan G L. 2020. Occurrence and biological characteristics of Tomato mottle mosaic virus on Solanaceae crops in China. Scientia Agricultura Sinica, 53, 539–550. (in Chinese) 
Li Y Y, Wang C L, Xiang D, Li R H, Liu Y, Li F. 2014. First report of tomato mottle mosaic virus infection of pepper in China. Plant Disease, 98, 1447–1447. 
Li Y Y, Wang Y, Hu J, Xiao L,Tan G L, Lan P X, Liu Y, Li F. 2017. The complete genome sequence, occurrence and host range of Tomato mottle mosaic virus Chinese isolate. Virology Journal, 14, 15. 
Liu Y, Li F, Li Y Y, Zhang S B, Gao X W, Xie Y, Yan F, Zhang A S, Dai L Y, Cheng Z B, Ding M, Niu Y B, Wang S J, Che H Y, Jiang T, Shi X B, He Z F, Wu Y F, Zhang D Y, Qing L, et al. 2019. Identification, distribution and occurrence of viruses in the main vegetables of China. Scientia Agricultura Sinica, 52, 239–261. (in Chinese)
Lovelock D A, Kinoti W M, Bottcher C, Wildman O, Dall D, Rodoni B C, Constable F E. 2020. Tomato mottle mosaic virus intercepted by Australian biosecurity in Capsicum annuum seed. Australasian Plant Disease Notes, 15, 8.
Luria N, Smith E, Reingold V, Bekelman I, Lapidot M, Levin I, Elad N, Tam Y, Sela N, Abu-Ras A, Ezra N, Haberman A, Yitzhak L, Lachman O, Dombrovsky A. 2017. A new Israeli Tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PLoS ONE, 12, e0170429. 
Nagai A, Duarte L M L, Chaves A L R, Peres L E P, dos Santos D Y A C. 2019. Tomato mottle mosaic virus in Brazil and its relationship with Tm-22 gene. European Journal of Plant Pathology, 155, 353–359. 
Salem N, Mansour A, Ciuffo M, Falk B W, Turina M. 2016. A new tobamovirus infecting tomato crops in Jordan. Archives of Virology, 161, 503–506. 
Sui X, Zheng Y, Li R, Padmanabhan C, Tian T, Deborah G H, Keinath A P, Fei Z, Wu Z, Ling K S. 2017. Molecular and biological characterization of tomato mottle mosaic virus and development of RT-PCR detection. Plant Disease, 101, 704–711. 
Tomita R. Sekine K T, Mizumoto H, Sakamoto M, Murai J, Kiba A, Hikichi Y, Suzuki K, Kobayashi K. 2011. Genetic basis for the hierarchical interaction between Tobamovirus spp. and L resistance gene alleles from different pepper species. Molecular Plant–Microbe Interactions, 24, 108–117.
Turina M, Geraats B P J, Ciuffo M. 2016. First report of Tomato mottle mosaic virus in tomato crops in Israel. New Disease Reports, 33, 1–1. 
Webster C G, Rosskopf E N, Lucas L, Mellinger H C, Adkins S. 2014. First report of tomato mottle mosaic virus infecting tomato in the United States. Plant Health Progress, 15, 151–152. 
Yan Z, Ma H, Wang L, Tettey C, Zhao M, Geng C, Tian Y, Li X. 2021a. Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm-22 resistance gene. Molecular Plant Pathology, 22, 1347–1357.
Yan Z, Zhao M, Ma H, Liu L, Yang G, Geng C, Tian Y, Li X. 2021b. Biological and molecular characterization of tomato brown rugose fruit virus and development of quadruplex RT-PCR detection. Journal of Integrative Agriculture, 20, 1871–1879. 
Zhang Y, Lubberstedt T, Xu M. 2013. The genetic and molecular basis of plant resistance to pathogens. Journal of Genetics and Genomics, 40, 23–35. 

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