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 N. tabacum 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-22transgenic 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.
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: tetteycarlos17@gmail.com; YAN Zhi-yong, E-mail: yzy_1990@163.com; Correspondence LI Xiang-dong, Tel: +86-538-8242523, Fax: +86-538-8226399, E-mail: xdongli@sdau.edu.cn; TIAN Yan-ping, E-mail: yanping.tian@sdau.edu.cn
* These authors contributed equally to this study.
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.