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Molecular Identification, Incidence, and Distribution of Acidovorax avenae in the Sugarcane-Producing Agroecological Regions of Mexico

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Abstract

Acidovorax avenae causes red stripe disease, which is characterised by red stripe and top rot symptoms in sugarcane (Saccharum spp. hybrids). The incidence of one or both these symptoms in the sugarcane fields was up to 30% in the Chiapas and Veracruz states of Mexico between 2015 and 2016. This study aimed to identify the causative agent of these symptoms and to determine the distribution and incidence of the disease in sugarcane-producing agroecological regions. Eleven bacterial isolates with phenotypic characteristics similar to those of A. avenae were isolated from the symptomatic tissue. Phylogenetic reconstruction based on the 16S rDNA sequence identified these 11 isolates as A. avenae with 99% identity. A. avenae infection was identified in three of the seven agroecological regions of Mexico (Cordoba-Gulf, Papaloapan-Gulf, and Southern region) with incidences ranging between 1 and 55%. The highest incidence of A. avenae infection was in the COLMEX 94-8 variety in the Cordoba-Gulf region (55%), whereas the lowest (1%) incidence was in the CP 72-2086 variety in the Papaloapan-Gulf region. The inoculation of these 11 strains resulted in the development of necrosis and wilting of the youngest leaves, dead of inoculated leave, and stem rot symptoms in the susceptible variety CP 72-2086. This is the first study to report the distribution and incidence of A. avenae in sugarcane plantations of Mexico.

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References

  • Bipen, K., Y. Rakesh, and K. Ratinderbir. 2014. Present status of bacterial top rot disease of sugarcane in Indian Punjab. Plant Disease Research 29: 68–70.

    Google Scholar 

  • Che, F., M. Iwano, N. Tanaka, S. Takayama, E. Minami, N. Shibuya, S. Takayama, E. Minami, N. Shibuya, I. Kadota, and A. Isogai. 1999. Biochemical and morphological features of rice cell death induced by Pseudomonas avenae. Plant and Cell Physiology 40: 1036–1045. https://doi.org/10.1093/oxfordjournals.pcp.a029485.

    Article  CAS  Google Scholar 

  • Chu, N., J.R. Zhou, H.Y. Fu, M.T. Huang, H.L. Zhang, and S.J. Gao. 2020. Global gene responses of resistant and susceptible sugarcane cultivars to Acidovorax avenae subsp. avenae identified using comparative transcriptome analysis. Microorganisms 8: 10. https://doi.org/10.3390/microorganisms8010010.

    Article  CAS  Google Scholar 

  • CONADESUCA. 2018. Comité Nacional para el Desarrollo Sustentable de la Caña de Azúcar (https://www.gob.mx/Conadesuca), México. Accessed 15 Oct 2018.

  • Doyle, J.J., and J.L. Doyle. 1990. Isolation of plant DNA from fresh tissue. Focus 12: 13–15.

    Google Scholar 

  • Fontana, P.D., C.A. Fontana, D. Bassi, E. Puglisi, S.M. Salazar, G.M. Vignolo, and P.S. Coccocelli. 2016. Genome sequence of Acidovorax avenae strain T10_61 associated with sugarcane red stripe in Argentina. Genome Announcements 4: e01669-e1715. https://doi.org/10.1128/genomeA.01669-15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fontana, P.D., A.M. Rago, C.A. Fontana, G.M. Vignolo, P.S. Cocconcelli, and J.A. Mariotti. 2013. Isolation and genetic characterization of Acidovorax avenae from red stripe infected sugarcane in Northwestern Argentina. European Journal of Plant Pathology 137: 525–534. https://doi.org/10.1007/s10658-013-0263-y.

    Article  CAS  Google Scholar 

  • Fontana, P.D., N. Tomasini, C.A. Fontana, V. Di Pauli, P.S. Cocconcelli, G.M. Vignolo, and S.M. Salazar. 2019. MLST reveals a separate and novel clonal group for Acidovorax avenae strains causing red stripe in sugarcane from Argentina. Phytopathology 109: 358–365. https://doi.org/10.1094/PHYTO-08-18-0303-R.

    Article  CAS  PubMed  Google Scholar 

  • Giglioti, E.A., and S. Matsuoka. 2000. False red stripe. In A guide to sugarcane diseases, ed. P. Rott, R.A. Bailey, J.C. Comstock, and B.J. Croft, 27–31. Montpellier: Cirad Publications Service.

    Google Scholar 

  • Giordano, P.R., J.M. Vargas Jr., A.R. Detweiler, N.M. Dykema, and L. Yan. 2010. First report of a bacterial disease on creeping bentgrass (Agrostis stolonifera) caused by Acidovorax spp. in the United States. Plant Disease 94: 922. https://doi.org/10.1094/PDIS-94-7-0922B.

    Article  CAS  PubMed  Google Scholar 

  • Giordano, P.R., A.M. Chaves, N.A. Mitkowski, and J.M. Vargas Jr. 2012. Identification, characterization, and distribution of Acidovorax avenae subsp. avenae associated with creeping bentgrass etiolation and decline. Plant Disease 96: 1736–1742. https://doi.org/10.1094/PDIS-04-12-0377-RE.

    Article  PubMed  Google Scholar 

  • Grisham, M.P., and R.M. Johnson. 2014. Red stripe caused by Acidovorax avenae subsp. avenae in Louisiana sugarcane. Phytopathology 104 (Suppl. 3): 472.

    Google Scholar 

  • Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series, vol. 41, no. 41, 95–98. London: Information Retrieval Ltd., c1979-c2000.

  • Hu, F.P., J.M. Young, C.M. Triggs, D.C. Park, and D.J. Saul. 2001. Relationships within the proteobacteria of plant pathogenic Acidovorax species and subspecies, Burkholderia species, and Herbaspirillum rubrisubalbicans by sequence analysis of 16S rDNA, numerical analysis and determinative tests. Antonie van Leeuwenhoek 80: 201–213. https://doi.org/10.1023/A:1013066912814.

    Article  CAS  PubMed  Google Scholar 

  • Ji, C., J. Ou, D. Xu, and R. Pan. 2014. First report of corn bacterial leaf stripe caused by Acidovorax avenae in Guangdong Province, China. Plant Disease 98: 1424. https://doi.org/10.1094/PDIS-03-14-0334-PDN.

    Article  CAS  PubMed  Google Scholar 

  • Koike, H. 1965. The aluminum-cap method for testing sugarcane varieties against leaf scald disease. Phytopathology 55: 317–319.

    Google Scholar 

  • Kumar, S., G. Stecher, M. Li, C. Knyaz, and K. Tamura. 2018. Mega X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549. https://doi.org/10.1093/molbev/msy096.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, I.M., I.M. Bartoszyk, D.E. Gundersen-Rindal, and R.E. Davis. 1997. Phylogeny and classification of bacteria in the genera Clavibacter and Rathayibacter on the basis of 16S rRNA gene sequence analyses. Applied Environmental Microbiology 63: 2631–2636.

    Article  CAS  Google Scholar 

  • Li, B., L. Wang, M. Ibrahim, M. Ge, Y. Wang, S. Mannan, M. Asif, and G. Sun. 2015. Membrane protein profiling of Acidovorax avenae subsp. avenae under various growth conditions. Archives Microbiology 197: 673–682. https://doi.org/10.1007/s00203-015-1100-9.

    Article  CAS  Google Scholar 

  • Liu, H., W.X. Tian, M. Ibrahim, B. Li, G.Q. Zhang, B. Zhu, and G.L. Xie. 2012. Characterization of pilP, a gene required for twitching motility, pathogenicity, and biofilm formation of Acidovorax avenae subsp. avenae RS-1. European Journal of Plant Pathology 134: 551–560. https://doi.org/10.1007/s10658-012-0038-x.

    Article  CAS  Google Scholar 

  • Martin, J.P., C.A. Wismer, and C.C. Ryan. 1989. Red stripe. In Diseases of sugarcane, ed. C. Ricaud, B.T. Egan, A.G. Gillaspie Jr., and C.G. Hughes, 81–95. Montpellier: Cirad Publications Service.

    Chapter  Google Scholar 

  • Mehnaz, S. 2013. Microbes–friends and foes of sugarcane. Journal of Basic Microbiology 53: 954–971. https://doi.org/10.1002/jobm.201200299.

    Article  PubMed  Google Scholar 

  • Monteil, C.L., R. Cai, H. Liu, M.E. Mechan Llontop, S. Leman, D.J. Studholme, C.E. Morris, and B.A. Vinatzer. 2013. Nonagricultural reservoirs contribute to emergence and evolution of Pseudomonas syringae crop pathogens. New Phytologist 199: 800–811. https://doi.org/10.1111/nph.12316.

    Article  CAS  Google Scholar 

  • Moore, E.R., A.S. Krüger, L. Hauben, S.E. Seal, R. De Baere, R. De Wachter, R. De Wachter, K.N. Timmis, and J. Swings. 1997. 16S rRNA gene sequence analyses and inter-and intrageneric relationships of Xanthomonas species and Stenotrophomonas maltophilia. FEMS Microbiology Letters 15: 145–153. https://doi.org/10.1111/j.1574-6968.1997.tb12563.x.

    Article  Google Scholar 

  • Myung, I.S., J.K. Choi, J.M. Wu, J.Y. Lee, H.L. Yoo, and H.S. Shim. 2012. Bacterial stripe of hog millet caused by Acidovorax avenae subsp. avenae, a new disease in Korea. Plant Disease 96: 1222. https://doi.org/10.1094/PDIS-03-12-0320-PDN.

    Article  CAS  PubMed  Google Scholar 

  • Osada, K.S., L. Fucikovsky, and A. Galindo. 1978. Study of the red stripe disease of sugar-cane. Agrociencia 34: 17–29.

    Google Scholar 

  • Quisehuatl-Tepexicuapan, E., R. Ferrera-Cerrato, H.V. Silva-Rojas, S. Rodriguez-Zaragoza, A. Alarcón, and J.J. Almaraz-Suárez. 2016. Free-living culturable bacteria and protozoa from the rhizoplanes of three floating aquatic plant species. Plant Biosystems 150: 855–865. https://doi.org/10.1080/11263504.2014.989282.

    Article  Google Scholar 

  • Rahesh, Y., K. Bipen, and M.S. Devi. 2014. Pathogenic variability among different isolates of the red stripe/top rot causing pathogen in Punjab state. Environment and Ecology 32: 873–877.

    Google Scholar 

  • Rakesh, Y., and K. Bipen. 2015. Status of Red stripe disease of sugarcane in Punjab, India. Journal of Mycopathological Research 53: 271–274.

    Google Scholar 

  • Ronquist, F., M. Teslenko, P. Van Der Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard, and J.P. Huelsenbeck. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rott, P., and M.J. Davis. 2000. Red stripe (Top rot). In A guide to sugarcane diseases, ed. P. Rott, R.A. Bailey, J.C. Comstock, and B.J. Croft, 60–62. Montpellier: Cirad Publications Service.

    Google Scholar 

  • Schaad, N.W., E. Postnikova, A. Sechler, L.E. Claflin, A.K. Vidaver, J.B. Jones, I. Agarkova, A. Ignatov, E. Dickstein, and B.A. Ramundo. 2008. Reclassification of subspecies of Acidovorax avenae as A. avenae (Manns 1905) emend., A. cattleyae (Pavarino, 1911) comb. nov., A. citrulli Schaad et al., 1978) comb. nov., and proposal of A. oryzae sp. nov. Systtematic and Applied Microbiology 31: 434–446. https://doi.org/10.1016/j.syapm.2008.09.003.

    Article  CAS  Google Scholar 

  • Seijo, T.E., and N.A. Peres. 2011. First report of Acidovorax avenae subsp. avenae causing bacterial leaf stripe of Strelitzia nicolai. Plant Disease 95: 1474. https://doi.org/10.1094/PDIS-03-11-0160.

    Article  CAS  PubMed  Google Scholar 

  • Sentíes-Herrera, H.E., F.C. Gómez-Merino, A. Valdez-Balero, H.V. Silva-Rojas, and L.I. Trejo-Téllez. 2014. The agro-Industrial sugarcane system in Mexico: current status, challenges and opportunities. The Journal of Agriculture Science 6: 26. https://doi.org/10.5539/jas.v6n4p26.

    Article  Google Scholar 

  • Shan, H., W. Li, Y. Huang, X. Wang, R. Zhang, Z. Luo, and J. Yin. 2017. First detection of sugarcane red stripe caused by Acidovorax avenae subsp. avenae in Yuanjiang, Yunnan, China. Tropical Plant Pathology 42: 137–141. https://doi.org/10.1007/s40858-017-0132-x.

    Article  Google Scholar 

  • Silva-Rojas, H.V., A. Rebollar-Alviter, A. Valdez-Balero, J.R. Sánchez-Pale, and M.L. Osnaya-González. 2017. Herbaspirillum rubrisubalbicans causing important emergent diseases in sugarcane in Mexico. Phytopathology 107: 19.

    Google Scholar 

  • Stukenbrock, E.H., and B.A. McDonald. 2008. The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology 46: 75–100. https://doi.org/10.1146/annurev.phyto.010708.154114.

    Article  CAS  PubMed  Google Scholar 

  • Tayeb, L.A., M. Lefevre, V. Passet, L. Diancourt, S. Brisse, and P.A. Grimont. 2008. Comparative phylogenies of Burkholderia, Ralstonia, Comamonas, Brevundimonas and related organisms derived from rpoB, gyrB and rrs gene sequences. Research in Microbiology 159: 169–177. https://doi.org/10.1016/j.resmic.2007.12.005.

    Article  CAS  PubMed  Google Scholar 

  • Xie, G.L., G.Q. Zhang, H. Liu, M.M. Lou, W.X. Tian, B. Li, X.P. Zhou, B. Zhu, and G.L. Jin. 2011. Genome sequence of the rice-pathogenic bacterium Acidovorax avenae subsp. avenae RS-1. Journal of Bacteriology 193: 5013–5014. https://doi.org/10.1128/JB.05594-11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yonzone, R., and M.S. Devi. 2018. Red stripe/top rot disease of sugarcane: a review. International Journal of Current Microbiology and Applied Sciences 7: 1469–1478. https://doi.org/10.20546/ijcmas.2018.701.179.

    Article  Google Scholar 

  • Zhang, R.Y., B. Zou, Y.W. Yan, C.O. Jeon, M. Li, M. Cai, and Z.X. Quan. 2020. Design of targeted primers based on 16S rRNA sequences in meta-transcriptomic datasets and identification of a novel taxonomic group in the Asgard archaea. BMC Microbiology 20: 25. https://doi.org/10.1186/s12866-020-1707-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank the SAGARPA-CONACYT Sectorial Fund for the funding received for this research through the project ‘Diagnosis and comprehensive management of the bacterial syndrome associated with Xanthomonas spp. and of emerging diseases of sugarcane (Saccharum officinarum) in Mexico (Code 2013-02-230876)’ as well as the Biotechnology and Seed Pathology laboratory of the Postgraduate College, Campus Montecillo, (external project PS 15-1063) for partially funding this research.

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Authors and Affiliations

  1. Posgrado en Fitopatología, Colegio de Postgraduados, Campus Montecillo, 56230, Texcoco, Estado de México, Mexico

    Camilo Hernández-Juárez, Carlos De León García de Alba, Guadalupe Valdovinos-Ponce & Sergio Aranda-Ocampo

  2. Producción de Semillas, Colegio de Postgraduados, Campus Montecillo, 56230, Texcoco, Estado de México, Mexico

    Hilda V. Silva-Rojas

  3. Departamento Agrícola, Universidad Autónoma Chapingo, 56230, Texcoco, Estado de México, Mexico

    Evelio Hernández-Juárez

  4. Posgrado en Bioprospección y Sustentabilidad Agrícola en El Trópico, Colegio de Postgraduados, Campus Campeche, 24450, Campeche, Mexico

    Mónica Osnaya-González

  5. Facultad de Química, Universidad Autónoma de Querétaro, 76010, Querétaro, Mexico

    Gerardo M. Nava-Morales

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  1. Camilo Hernández-Juárez
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  2. Hilda V. Silva-Rojas
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  3. Carlos De León García de Alba
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  8. Sergio Aranda-Ocampo
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Contributions

CHJ conducted the experiments, collected the data, and wrote a Doctorate dissertation based on this investigation. SAO conceptualised, designed, and conducted the investigation, as well as reviewed and edited the original manuscript draft. HVSR conceptualised and conducted the investigation, provided inputs for phylogenetic analysis, and partially sponsored the project. EHJ performed statistical analyses. MOG, GVP, GNM, and CDLGA conducted the investigation and edited the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Sergio Aranda-Ocampo.

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Hernández-Juárez, C., Silva-Rojas, H.V., De León García de Alba, C. et al. Molecular Identification, Incidence, and Distribution of Acidovorax avenae in the Sugarcane-Producing Agroecological Regions of Mexico. Sugar Tech 23, 891–899 (2021). https://doi.org/10.1007/s12355-021-00964-w

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