Cassava torrado-like virus encodes a gene that facilitates the mechanical transmission to Nicotiana benthamiana of Cassava virus X

Jenyfer Jimenez; Ana M. Leiva; Wilmer J. Cuellar

doi:10.17268/sci.agropecu.2023.019

Autores

Jenyfer Jimenez Virology Laboratory, Crops for Nutrition and Health, International Center for Tropical Agriculture, km 17, Recta Cali–Palmira, CP 763537, Palmira
Ana M. Leiva Virology Laboratory, Crops for Nutrition and Health, International Center for Tropical Agriculture, km 17, Recta Cali–Palmira, CP 763537, Palmira.
Wilmer J. Cuellar Virology Laboratory, Crops for Nutrition and Health, International Center for Tropical Agriculture, km 17, Recta Cali–Palmira, CP 763537, Palmira.

DOI:

https://doi.org/10.17268/sci.agropecu.2023.019

Palavras-chave:

Cassava, mechanical transmission, secoviridae, virus interaction, virus movement

Resumo

Cassava-torrado-like virus (CsTLV) is a bipartite single-stranded RNA virus belonging to the family Secoviridae. The virus has been reported in Brazil and Colombia, and is usually found in mixed infections, and in plants affected by Cassava Frogskin Disease (CFSD), an endemic cassava disease in the Americas. Genome analysis of CsTLV identifies a gene in RNA2 implicated in pathogen movement in other torradoviruses. This gene (RNA2-ORF1) and another one no related to virus movement (Maf/Ham1) were amplified by PCR and cloned into constructs under the 35S promoter of cauliflower mosaic virus (CaMV), which then were transfered to agrobacterium binary vectors. When agro-infiltrated in Nicotiana benthamiana plants, only RNA2-ORF1 had a positive effect on the mechanical inoculation of cassava virus X (CsVX), a potexvirus that has a low rate of mechanical infection in N. benthamiana. Efficiency of CsVX mechanical transmission was measured by the number of infected plants, presence of symptoms, and titers of CsVX as measured by ELISA, two weeks after infection. On average, CsVX could infect 2.3 times more plants when these were previously agro-infiltrated with A. tumefaciens binary vector encoding CsTLV RNA2-ORF1. We conclude that the novel secovirid CsTLV associated with leaf spot symptoms in cassava, encodes a gene that could enhance other viral infections in N. benthamiana. Further studies are required to elucidate this effect and its role in mixed infections, often observed in cassava plants affected by CFSD.

Referências

Alvarez, E., Mejia, J. F., Llano, G. A., Loke, J. B., Calari, A., Duduk, B., & Bertaccini, A. (2009). Characterization of a phytoplasma associated with frogskin disease in cassava. Plant Disease, 93(11), 1139-1145.

Brown, N. P., Leroy, C., & Sander, C. (1998). MView: a web-compatible database search or multiple alignment viewer. Bioinformatics (Oxford, England), 14(4), 380-381.

Calvert, L. A., Cuervo, M. I., Ospina, M. D., Fauquet, C. M., & Ramirez, B. C. (1996). Characterization of cassava common mosaic virus and a defective RNA species. Journal of General Virology, 77(3), 525-530.

Calvert, L. A., Cuervo, M., Lozano, I., Villareal, N., & Arroyave, J. (2008). Identification of three strains of a virus associated with cassava plants affected by frogskin disease. Journal of phytopathology, 156(11‐12), 647-653.

Cardozo, L.; Pardo, J. M.; Zacher, M.; Torres, A., & Alvarez, E. (2016). First report of a 16SrIII phytoplasma associated with frogskin disease in cassava (Manihot esculenta) in Paraguay. Plant Dis. 2016, 100, 1492.

Carvajal-Yepes, M., Olaya, C., Lozano, I., Cuervo, M., Castano, M., & Cuellar, W. J. (2014). Unraveling complex viral infections in cassava (Manihot esculenta Crantz) from Colombia. Virus research, 186, 76-86.

Chaparro-Martinez, E. I., & Trujillo-Pinto, G. (2001). First report of frog skin disease in cassava (Manihot esculenta) in Venezuela. Plant Disease, 85(12), 1285-1285.

Collavino, A., Zanini, A. A., Medina, R., Schaller, S., & Di Feo, L. (2021). Cassava common mosaic virus infection affects growth and yield components of cassava plants (Manihot esculenta) in Argentina. Plant Pathology, 71(4), 980-989.

de Oliveira, S. A. S., Ferreira, C. F., Diamantino, M. S. A. S., Santos, T. A., Pereira, J. D. S., & de Oliveira, E. J. (2020). First report of cassava torrado-like virus, cassava polero-like virus and cassava new alphaflexivirus associated with cassava frogskin disease in Brazil. Journal of Plant Pathology, 102(1), 247-247.

Ferriol, I., Vallino, M., Ciuffo, M., Nigg, J. C., Zamora‐Macorra, E. J., Falk, B. W., & Turina, M. (2018). The Torradovirus‐specific RNA2‐ORF1 protein is necessary for plant systemic infection. Molecular plant pathology, 19 (6), 1319-1331.

Harrison, B. D., Lennon, A. M., & Aiton, M. M. (1986). Properties of four previously uncharacterized cassava viruses. Phytopathology, 76, 1075.

James, A. M., Seal, S. E., Bailey, A. M., & Foster, G. D. (2021). Viral inosine triphosphatase: A mysterious enzyme with typical activity, but an atypical function. Molecular Plant Pathology, 22(3), 382-389.

Jimenez, J. (2017). Caracterización del virus Cassava torrado-like virus en yuca (Manihot esculenta Crantz) e identificación de proteínas virales involucradas en la supresión del silenciamiento de ARN. [Tesis]. Universidad Nacional de Colombia – Sede Palmira.

Jimenez, J., Leiva, A. M., Olaya, C., Acosta-Trujillo, D., & Cuellar, W. J. (2021). An optimized nucleic acid isolation protocol for virus diagnostics in cassava (Manihot esculenta Crantz.). MethodsX, 8, 101496.

Kreuze, J. F., Savenkov, E. I., Cuellar, W., Li, X., & Valkonen, J. P. (2005). Viral class 1 RNase III involved in suppression of RNA silencing. Journal of virology, 79(11), 7227-7238.

Kumar, G., & Dasgupta, I. (2021). Variability, functions and interactions of plant virus movement proteins: What do we know so far?. Microorganisms, 9(4), 695.

Legg, J. P., Kumar, P. L., Makeshkumar, T., Tripathi, L., Ferguson, M., Kanju, E., Ntawuruhunga, P., & Cuellar, W. (2015). Cassava virus diseases: biology, epidemiology, and management. Advances in virus research, 91, 85-142.

Leiva, A. M., Jimenez, J., Sandoval, H., Perez, S., & Cuellar, W. J. (2022). Complete genome sequence of a novel secovirid infecting cassava in the Americas. Archives of virology, 167(2), 665-668.

Lennon, A. M., Aiton, M. M. & Harrison, B. D. (1987). Purification and properties of cassava green mottle, a previously undescribed virus from the Solomon Islands. Annals of applied biology, 110(3), 545-555.

Lozano, I., Leiva, A. M., Jimenez, J., Fernandez, E., Carvajal-Yepes, M., Cuervo, M., & Cuellar, W. J. (2017). Resolution of cassava-infecting alphaflexiviruses: Molecular and biological characterization of a novel group of potexviruses lacking the TGB3 gene. Virus Research, 241, 53-61.

Mbanzibwa, D. R., Tian, Y., Mukasa, S. B., & Valkonen, J. P. (2009). Cassava brown streak virus (Potyviridae) encodes a putative Maf/HAM1 pyrophosphatase implicated in reduction of mutations and a P1 proteinase that suppresses RNA silencing but contains no HC-Pro. Journal of Virology, 83(13), 6934-6940.

Morozov, S. Y., & Solovyev, A. G. (2020). Small hydrophobic viral proteins involved in intercellular movement of diverse plant virus genomes. AIMS microbiology, 6(3), 305.

Nolt, B. L., Pineda L, B., & Velasco, A. C. (1992). Surveys of cassava plantations in Colombia for virus and virus‐like diseases. Plant pathology, 41(3), 348-354.

Noskov, V. N., Staak, K., Shcherbakova, P. V., Kozmin, S. G., Negishi, K., Ono, B. C., Hayatsu, H. & Pavlov, Y. I. (1996). HAM1, the gene controlling 6‐N‐hydroxylaminopurine sensitivity and mutagenesis in the yeast Saccharomyces cerevisiae. Yeast, 12(1), 17-29.

Pardo, J. M., Alvarez, E., Becerra Lopez-Lavalle, L. A., Olaya, C., Leiva, A. M., & Cuellar, W. J. (2022). Cassava Frogskin Disease: Current Knowledge on a Re-Emerging Disease in the Americas. Plants, 11(14), 1841.

Pineda, B., Jayasinghe, U., & Lozano, J. C. (1983). La enfermedad “Cuero de Sapo” en yuca (Manihot esculenta Crantz). ASIAVA 4:10-12.

Siriwan, W., Jimenez, J., Hemniam, N., Saokham, K., Lopez-Alvarez, D., et al. (2020). Surveillance and diagnostics of the emergent Sri Lankan cassava mosaic virus (Fam. Geminiviridae) in Southeast Asia. Virus research, 285, 197959.

Solovyev, A., Kalinina, N., & Morozov, S. (2012). Recent advances in research of plant virus movement mediated by triple gene block. Frontiers in plant science, 3, 276.

Tamai, A., & Meshi, T. (2001). Cell-to-cell movement of Potato virus X: the role of p12 and p8 encoded by the second and third open reading frames of the triple gene block. Molecular plant-microbe interactions, 14(10), 1158-1167.

Thomas-Sharma, S., Andrade-Piedra, J., Carvajal, M., Hernandez, J. F., Jeger, M. J., et al. (2017). A risk assessment framework for seed degeneration: Informing an integrated seed health strategy for vegetatively propagated crops. Phytopathology, 107(10), 1123-1135.

Tomlinson, K. R., Pablo-Rodriguez, J. L., Bunawan, H., Nanyiti, S., Green, P., et al. (2019). Cassava brown streak virus Ham1 protein hydrolyses mutagenic nucleotides and is a necrosis determinant. Molecular Plant Pathology, 20(8), 1080-1092.

Valli, A. A., García, R., Ribaya, M., Martínez, F. J., Gómez, D. G., et al. (2022). Maf/ham1-like pyrophosphatases of non-canonical nucleotides are host-specific partners of viral RNA-dependent RNA polymerases. PLoS pathogens, 18(2), e1010332.

van der Vlugt, R. A., Verbeek, M., Dullemans, A. M., Wintermantel, W. M., Cuellar, W. J., Fox, A., & Thompson, J. R. (2015). Torradoviruses. Annual Review of Phytopathology, 53, 485–512.

Venturini, M. T., Araújo, T. D. S., Abreu, E. F. M., Andrade, E. C. D., Santos, V. D. S., Silva, M. R. D., & Oliveira, E. J. D. (2016). Crop losses in Brazilian cassava varieties induced by the Cassava common mosaic virus. Scientia Agricola, 73, 520-524.

Verbeek, M., Dullemans, A. M., Van den Heuvel, J. F. J. M., Maris, P. C., & Van der Vlugt, R. A. A. (2007). Identification and characterisation of tomato torrado virus, a new plant picorna-like virus from tomato. Archives of Virology, 152(5), 881–890.

Verchot-Lubicz, J. (2005). A new cell-to-cell transport model for potexviruses. Molecular plant-microbe interactions, 18(4), 283-290.

Walter, B., Ladeveze, I., Etienne, L., & Fuchs, M. (1989). Some properties of a previously undescribed virus from cassava: Cassava american latent virus. Annals of applied biology, 115 (2), 279-289.

Wu, C. H., Lee, S. C., & Wang, C. W. (2011). Viral protein targeting to the cortical endoplasmic reticulum is required for cell–cell spreading in plants. Journal of Cell Biology, 193(3), 521-535.