Indirect effects of transgenes on resistance to northern leaf blight of maize under chemical and manual management practices of weeds
DOI:
https://doi.org/10.33448/rsd-v11i4.27574Keywords:
Genetically modified maize; Zea mays L.; Northern leaf blight; Ammonium glufosinate.Abstract
The effects of transgenes on plant resistance to non-target diseases caused by foliar fungi are still poorly studied. This study aimed to evaluate the indirect effects of the TC1507 event, isolated and in combination with NK603, on the maize genetic resistance to northern leaf blight, in the presence and absence of chemical control of weeds. Three isogenic hybrids were used as treatments in this study: the non-genetically modified conventional hybrid BG7060 (NGM); the genetically modified hybrid BG7060H (Hx), carrying transgenes cry1F and pat (TC1507 event); and the genetically modified hybrid BG7060HR (Hxrr), carrying transgene cp4epsps (NK603 event) combined with the TC1507 event. To evaluate the resistance of the three isogenic hybrids to that pathogen, three experiments were carried out in Florianópolis, southern Brazil, in complete randomized blocks with three replications in experiment 1 (2012/2013 harvest) and four replications in experiments 2 and 3 (2016/2017 harvest). The control of weeds was done by manual weeding, in experiments 1 and 2, and with the application of the herbicide Finale in a single dose, in experiment 3. The severity of northern leaf blight was evaluated under natural conditions of disease occurrence, in experiment 1, and from inoculation of the pathogen, in experiments 2 and 3. The isogenic hybrid Hxrr showed higher incidence and shorter incubation and latency periods than the Hx and conventional isogenic hybrids in the two management environments of weeds. Pathogen resistance, measured from these three variables, tended to be lower in the genetically modified hybrid Hxrr, which contains two events (TC1507 and NK603), followed by the hybrids Hx and NGM, in increasing order of resistance. The addition of the herbicide for the control of weeds increased the susceptibility of the genetically modified hybrids Hx and Hxrr, as well as the conventional hybrid not submitted to this control, but cultivated close to the hybrids Hx and Hxrr managed with the use of the herbicide.
References
Agapito-Tenfen, S. Z., Vilperte, V., Traavik, T. I., & Nodari, R. O. (2018). Systematic miRNome profiling reveals differential microRNAs in transgenic maize metabolism. Environmental Sciences Europe, 30, 37. https://doi.org/10.1186/s12302-018-0168-7.
Agbios. (2008). Information on GM Approved Products. http://www.agbios.com/dbase.php.
Agroceres. (1996). Guia Agroceres de sanidade, (2a ed.), Agroceres.
Albrecht, L. P., Braccini, A. L., Scapim, C. A., Ávila, M. R., Albrecht, A. J. P., & Ricci, T. T. (2011). Qualidade fisiológica das sementes de soja RR em resposta ao uso de diferentes tratamentos contendo glyphosate em aplicação sequencial. Bioscience Journal, 27 (2), 211-220.
Ali, S. E. B., Draxler, A., Poelzl, D., Agapito-Tenfen, S., Hochegger, R., Haslberger, A. G., & Brandes, C. (2020). Analysis of transcriptomic differences between NK603 maize and near-isogenic varieties using RNA sequencing and RT-qPCR. Environmental Sciences Europe, 32 (1), 1-23.
Argenta, G., Silva, P. R. F. D., & Sangoi, L. (2001). Maize plant arrangement: analysis of the state of the art. Ciência Rural, 31, 1075-1084.
Balieiro Neto, G., Cividanes, T. M. S., Branco, R. B. F., Bueno, M. S., Possenti, R., & Nogueira, J. R. (2013). Danos causados por pragas na estrutura, morfologia e composição de híbridos de milho bt para silagem. Boletim de Indústria Animal, 70 (3), 252260. http://dx.doi.org/10.17523/bia.v70n3p252.
Benevenuto, R. F., Agapito-Tenfen, S. Z., Vilperte, V., Wikmark, O-G., Van Rensburg, P. J., & Nodari, R. O. (2017). Molecular responses of genetically modified maize to abiotic stresses as determined through proteomic and metabolomic analyses. PLoS ONE, 12 (2), e0173069. http://dx.doi.org/10.1371/journal.pone.0173069.
Biogene (2016). Híbridos de Milho: BG7060. DuPont, Pioneer. Retrieved March 5, 2016, from http://www,biogene,com,br/milho/produtos/bg7060 .
Bleicher, J. (1988). Níveis de resistência a Helminthosporium turcicum Pass. em três ciclos de seleção em milho pipoca (Zea mays L.). Piracicaba, São Paulo: ESALQ.
Bowers, E. L., Hellmich, R. L., & Munkvold, G. P. (2013). Vip3Aa and Cry1Ab proteins in maize reduce Fusarium ear rot and fumonisins by deterring kernel injury from multiple Lepidopteran pests. World Mycotoxin Journal, 6 (2), 127-135. http://dx.doi.org/10.3920/WMJ2012.1510.
Campbell, C. L., & Madden, L. V. (1990). Introduction to plant disease epidemiology. John Wiley & Sons.
Carbonari, C. A., Latorre, D. O., Gomes, G. L. G. C., Velini, E. D., Owens, D. K., Pan, Z., & Dayan, F. E. (2016). Resistance to glufosinate is proportional to phosphinothricin acetyltransferase expression and activity in LibertyLink® and WideStrike® cotton. Planta, 1, 1-9. http://dx.doi.org/10.1007/s00425-015-2457-3.
Cheeke, T. E., Darby, H., Rosenstiel, T. N., Bever, J. D., & Cruzan, M. B. (2014). Effect of Bacillus thuringiensis (Bt) maize cultivation history on arbuscular mycorrhizal fungal colonization, spore abundance and diversity, and plant growth. Agriculture Ecosystems Environment., 195, 29–35. http://dx.doi.org/10.1016/j.agee.2014.05.019.
Clements, M. J., Campbell, K. W., Maragos, C. M., Pilcher, C., Headrick, J. M., Pataky, J. K., & White, D.G. (2003). Influence of Cry 1Ab protein and hybrid genotype on fumonisin contamination and Fusarium ear rot of corn. Crop Science., 43 (4), 1283–1293. http://dx.doi.org/10.2135/cropsci2003.1283.
Costa, F. M., Silva, N. C. A., & Ogliari, J. B. (2016). Maize diversity in southern Brazil: indication of a microcenter of Zea mays L. Genetic Resources and Crop Evolution, 64 (4), 681-700. doi.org/10.1007/s10722-016-0391-2.
CTNBio - Comissão Técnica Nacional de Biossegurança. (2020). Liberação comercial. Retrieved July 20, 2020, from http://ctnbio.mctic.gov.br/liberacao-comercial#/liberacao-comercial/consultar-processo.
Del Río, L. A., Pastori, G. M., Palma, J. M., Sandalio, L. M., Sevilla, F., Corpas, F. J., Jimenez, A., Lopez-Huertas, E., & Hernandez, J. A. (1998). The activated oxygen role of peroxisomes in senescence. Plant Physiology, 116, 1195–1200. PMCID: PMC1539175.
De Rossi, R. L., Reis, E. M., & Brustolin, R. (2015). Conidial morphology and pathogenicity of Exserohilum turcicum isolates of corn from Argentina and Brazil. Summa Phytopathologica, 41, 58-63.
EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária. (2006). Sistema brasileiro de classificação de solos. (2a ed.), EMBRAPA-SPI.
Estep, L. K., Sackett, K., & Mundt, C. C. (2014). Influential disease foci in epidemics and underlying mechanisms: a field experiment and simulations. Ecological Applications, 24 (7), 1854-1862. http://dx.doi.org/10.1890/13-1408.1.
Ferreira, K. C. Z., Marino, C. L., & Furtado, E. L. (2017). Seleção de genótipos de eucalipto resistentes à ferrugem (Puccinia psidii) através de parâmetros monocíclicos. Summa Phytopathol., 43 (2), 103-110. http://dx.doi.org/10.1590/0100-5405/2062.
Gatch, E. W., & Munkvold, G. P. (2002). Fungal species composition in maize stalks in relation to European corn borer injury and transgenic insect protection. Plant Disease, 86, 1156-1162. http://dx.doi.org/10.1094/PDIS.2002.86.10.1156.
Gressel, J., Gassmann, A. J., & Owen, M. D. K. (2017). How well will stacked transgenic pest/herbicide resistances delay pests from evolving resistance? Pest Management Science, 73 (1), 22-34. http://dx.doi.org/10.1002/ps.4425.
Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., & Compant, S. (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology Molecular Biology Reviews, 79, 293–320. http://dx.doi.org/10.1128/MMBR.00050-14.
Holderbaum, D. F., Traavik, T. I., Nodari, R. O., & Guerra, M. P. (2019). Comparison of in vitro callus-cultures from transgenic maize AG-5011YG (MON810) and conventional near-isogenic maize AG-5011. Crop Breeding and Applied Biotechnology, 19 (2), 169-175. https://dx.doi.org/10.1590/1984-70332019v19n2a24.
IBGE - Instituto Brasileiro de Geografia e Estatística. (2017). Censo Agropecuário 2017: Indicadores municipais. https://mapasinterativos.ibge.gov.br/agrocompara.
Ibrahim, A., Sorensen, D., Jenkins, H. A., Ejim, L., Capretta, A., & Sumarah, M.W. (2017). Epoxynemanione A, nemanifuranones A-F, and nemanilactones A-C, from Nemania serpens, an endophytic fungus isolated from Riesling grapevines. Phytochemistry, 140, 16–26. http://dx.doi.org/ 10.1016/j.phytochem.2017.04.009.
ICEA - Instituto do Controle do Espaço Aéreo. (2017). Arquivo meteorológico. Subdivisão de Climatologia e Arquivos Meteorológicos. http://pesquisa.icea.gov.br/climatologia/arquivo.php.
ISAAA - International Service for the Acquisition of Agri-biotech Applications. (2019). Global status of commercialized biotech/GM crops in 2018. China Biotechnology, 39 (8), 1-6.
ISAAA. Global Status of Commercialized Biotech/GM Crops in 2019: Biotech Crops Drive Socio-Economic Development and Sustainable Environment in the New Frontier. ISAAA Brief No. 55, 2020.
Kaiser, U., Kluth, C., & Märländer, B. (2010). Variety-specific Epidemiology of Cercospora beticola Sacc. and Consequences for Threshold-based Timing of Fungicide Application in Sugar Beet. Journal of Phytopathology, 158 (4), 296–306. http://dx.doi.org/10.1111/j.1439-0434.2009.01618.x.
Kmoch, M., Šafránková, I., Holková, L., Polišenská, I., Krédl, Z., & Pokorný, R. (2012). Fungi of the Fusarium genus in the grains of conventional hybrids and transgenic Bt-hybrids of maize (Zea mays L,) in the Czech Republic. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 60 (5), 115-124. http://dx.doi.org/10.11118/actaun201260050115.
Krenchinski, F. H., Albrecht, L. P., Albrecht, A. J. P., Cesco, V. J. S., Rodrigues, D. M., Portz, R. L., & Zobiole, L. H. S. (2017). Glyphosate affects chlorophyll, photosynthesis and water use of four Intacta RR2 soybean cultivars. Acta Physiologiae Plantarum, 39, 63. http://dx.doi.org/10.1590/1808-1657000732017.
Lazebnik, J., Arpaia, S., Baldacchino, F., Banzato, P., Moliterni, S., Vossen, J. H., van de Zande, E. M., & van Loon, J. J. A. (2017). Effects of a genetically modified potato on a non-target aphid are outweighed by cultivar diferences. Journal of Pest Science, 90, 855. http://dx.doi.org/10.1007/s10340-017-0831-6.
Liu, W., Zhang, Z., Liu, X., & Jin, W. (2020). iTRAQ-based quantitative proteomic analysis of two transgenic soybean lines and the corresponding non-genetically modified isogenic variety. The Journal of Biochemistry, 167 (1), 67-78. https://dx.doi.org/10.1093/jb/mvz081.
Mallowa, S. O., Esker, P. D., Paul, P. A., Bradley, C. A., Chapara, V. R., Conley, S. P., & Robertson, A. E. (2015). Effect of maize hybrid and foliar fungicides on yield under low foliar disease severity conditions. Phytopathology, 105, 10801089. http://dx.doi.org/10.1094/PHYTO-08-14-0210-R.
Marcuzzo, L. L., Duarte, T. S. Fernandes, J. M. C., Hilleshein, P. C., & Scheidt, B. T. (2015). Progresso temporal da cercosporiose da beterraba em diferentes genótipos e épocas de semeadura na primavera. Summa Phytopathology, 41 (3), 219-223. http://dx.doi.org/10.1590/0100-5405/1938.
Mueller, D. S., Wise, K. A., Sisson, A. J., Allen, T. W., Bergstrom, G. C., Bosley, D. B., Bradley, C. A., Broders, K. D., Byamukama, E., & Chilvers, M. I. (2016). Corn yield loss estimates due to diseases in the United States and Ontario, Canada from 2012 to 2015. Plant Health Progress Journal, 17, 211-222. https://dx..doi.org/10.1094/PHP-RS-16-0030.
Munkvold G. P., Hellmich, R. L., & Showers, W. B. (1997). Reduced fusarium ear rot and symptomless infection in kernels of maize fenetically engineered for European corn borer resistence. Phytopathology, 87, 1071–1077. http://dx.doi.org/10.1094/PHYTO.1997.87.10.1071.
Munkvold, G. P., & Desjardins, A. E. (1997). Fumonisins in maize: Can we reduce their occurence? Plant Disease, 81, 556–565. https://dx.doi.org/10.1094/PDIS.1997.81.6.556.
Munkvold, G. P., & Hellmich, R. L. (1999). Comparison of fumonisin concentrations in kernels of transgenic Bt maize hybrids and non-transgenic hybrids. Plant Disease, 83, 130–138. http://dx.doi.org/10.1094/PDIS.1999.83.2.130.
Nwanosike, M. R. O., Mabagala, R. B., & Kusolwa, P. M. (2013). Effect of Northern Leaf Blight (Exserohilum turcicum) Severity on Yield of Maize (Zea Mays L.) in Morogoro, Tanzania. International Journal of Science and Research., 4, 466-474. SUB157735.
O’Keeffe, K. R., Carbone, I., Jones, C. D., & Mitchell, C. E. (2017). Plastic potential: how the phenotypes and adaptations of pathogens are influenced by microbial interactions within plants. Current Opinion Plant Biology, 38, 78–83. http://dx.doi.org/10.1016/j.pbi.2017.04.014.
Ogliari, J. B (2018). Presença do milho geneticamente modificado em um microcentro de diversidade, no sul do Brasil. In Del Cura, F. (Ed.), Cuaderno de la Biored Iberoamérica, Cuaderno 6 (pp. 30-45). Venezuela: Universidad Politécnica Territorial de Mérida.
Ogliari, J. B., Guimarães, M. A., & Camargo, L. E. A. (2007). Chromosomal locations of the maize (Zea mays L.) HtP and rt genes that confer resistance to Exserohilum turcicum. Genet. Mol. Biol., 30, 630–634. http://dx.doi.org/10.1590/S1415-47572007000400021.
Ogliari, J. B., Guimarães, M. A., Geraldi, I. O., & Camargo, L. E. A. (2005). New resistance genes in the Zea mays L. - Exserohilum tucicum pathosystem. Genetic Molecular Biology, 28, 435-439. http://dx.doi.org/10.1590/S141547572005000300017.
Owen, M. D. K., Beckie, H. J., Leeson, J. Y., Norsworthy, J. K., & Steckel, L. E. (2015). Integrated pest management and weed management in the United States and Canada. Pest Management Science, 71, 357–376. http://dx.doi.org/10.1002/ps.3928.
Padgette, S. R., Nida, D. L., Biest, N. A., Bailey, M. R., & Zobel, J. F. (1993). Glyphosate tolerant soybeans in the US in 1992: field test, processing studies, and analytical evaluation. Monsanto Study, 92, 30–32.
Pereira Filho, I. A., & Borghi, E. (2020). Sementes de milho: nova safra, novas cultivares e continua a dominância dos transgênicos. Sete Lagoas, Minas Gerais: Embrapa Milho e Sorgo.
Prado, W. S., Estevão, W. L., Maeda, A. K. M., Carlesso, A., Gonçalves, M. C., & Davide, L. M. C. (2016). Agronomic performance of transgenic and isogenic corn hybrids in the state of Mato Grosso do Sul. Revista Ceres, 63 (6), 796-806. http://dx.doi.org/10.1590/S0100-204X2017000700004.
Prochazkova, D., Sairam, R. K., Srivastava, G. C., & Singh, D.V. (2001). Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. Plant Science, 161, 765–771. https://dx.doi.org/10.1016/S0168-9452(01)00462-9.
R Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing,
Ramathani, I., Biruma, M., Martin, T., Dixelius, C., & Okori, P. (2014). Disease severity, incidence and races of Setosphaeria turcica on sorghum in Uganda. European Journal of Plant Pathology, 131, 383-392. http://dx.doi.org/10.1007/s10658-0119815-1.
Reddy, T. R., Reddy, P. N., & Reddy, R. R. (2014). Turcicum Leaf Blight Incited by Exserohilum turcicum. International Journal of Applied Biology and Pharmaceutical Technology, 5 (1), 54-59. http://dx.doi.org/10.1007/s41348-016-0054-8.
ROLAS - Rede Oficial de Análise de Solo e de Tecido Vegetal. (2004). Manual de adubação e calagem para os estados do Rio Grande do Sul e Santa Catarina. 20. ed. Porto Alegre-RS: Sociedade Brasileira de Ciência do Solo.
Severns, P. M., Estep, L. K., Sackett, K. E., & Mundt, C. C. (2014). Degree of host susceptibility in the initial disease outbreak influences subsequent epidemic spread. Journal of Applied Ecology, 51, 1622–1630. http://dx.doi.org/10.1111/1365-2664.12326.
Silva, K. J., Armas, R. D., Soares, C. R. F. S., & Ogliari, J. B. (2016a). Communities of endophytic microorganisms in different growth stages in local variety, and transgenic and conventional isogenic hybrids of maize. World Journal of Microbiology and Biotechnology, 32, 189. http://dx.doi.org/10.1007/s11274-016-2149-6.
Silva, N. C. A., Vidal, R., Costa, F. M., Vaio, M., & Ogliari, J. B. (2015). Presence of Zea luxurians (Durieu and Ascherson) Bird in southern Brazil: implications for the conservation of wild relatives of maize. PloS ONE, 10 (10), e0139034. http://dx.doi.org/10.1371/journal.pone.0139034.
Silva, N. C. A., Vidal, R., & Ogliari, J. B. (2016b). New popcorn races in a diversity microcenter of Zea mays L. in the far west of Santa Catarina, southern Brazil. Genetic Resources and Crop Evolution, 64 (6), 1191-1204. http://dx.doi.org/10.1007/s10722-016-0429-5.
Smith, J. L., Lepping, M. D., Rule, D. M., Farhan, Y., & Schaafsma, A. W. (2017). Evidence for Field-Evolved Resistance of Striacosta albicosta (Lepidoptera: Noctuidae) to Cry1F Bacillus thuringiensis Protein and Transgenic Corn Hybrids in Ontario, Canada. Journal of Economic Entomology, 110 (5), 2217–2228. https://dx.doi.org/10.1093/jee/tox228.
Thomas, W. E., Pline-Srnic, W. A., Thomas, J. F., Edmisten, K. L., Wells, R., & Wilcut, J. W. (2004). Glyphosate negatively affects pollen viability but not pollination and seed set in glyphosate resistant corn. Weed Science, 52 (4), 725-734. http://dx.doi.org/10.1614/WS-03-134R.
TIBCO Statistica 13.3. (2017). Tibco Software Inc. 3307. Califórnia, USA: Hillview Avenue Palo Alto. https://docs.tibco.com/products/tibco-statistica-13-3-0.
Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Le Van, A., & Dufresne, A. (2015). The importance of the microbiome of the plant holobiont. New Phytologist, 206, 1196–1206. http://dx.doi.org/10.1111/nph.13312.
Wang, H., Xiao, Z. X., Wang, F. G., Xiao, Y. N., Zhao, J. R. R., Zheng, Y. L., & Qiu, F. Z. (2012). Mapping of HtNB, a gene conferring non lesion resistance before heading to Exserohilum turcicum (Pass.), in a maize inbred line derived from the Indonesian variety Bramadi. Genetics and Molecular Research, 11, 2523-2533. http://dx.doi.org/10.4238/2012.
Wang, X., Zhang, X., Yang, J., & Wang, Z. (2018). Effect on transcriptome and metabolome of stacked transgenic maize containing insecticidal cry and glyphosate tolerance epsps genes. The Plant Journal, 93, 1007–1016. http://dx.doi.org/10.1111/tpj.13825.
Wise, K., & Mueller, D. (2011). Are fungicides no longer just for fungi? An analysis of foliar fungicide use in corn. APSnet feature article. doi:10.1094/APSnetFeature-2011-0531.
Zhang, X. L., Si, B. W., Fan, C. M., Li, H. J., & Wang, X. M. (2014). Proteomics identification of differentially expressed leaf proteins in response to Setosphaeria turcica infection in resistant maize. Journal of Integrative Agriculture, 13, 789–803. http://dx.doi.org/10.1016/S2095-3119(13)60513-4.
Zobiole, L. H. S., Bonini, E. A., de Oliveira Jr., R. S., Kremer, R. J., & Ferrarese-Filho, O. (2010b). Glyphosate affects lignin content and amino acid production in glyphosate-resistant soybean. Acta Physiologiae Plantarum, 32 (5), 831-837. http://dx.doi.org/10.1007/s11738-010-0467-0.
Zobiole, L. H. S., de Oliveira Jr., R. S., Kremer, R. J., Constantin, J., Bonato, C. M., & Muniz, A. S. (2010c). Water use efficiency and photosynthesis of glyphosate-resistant soybean as affected by glyphosate. Pesticide Biochemistry and Physiology, 97 (3), 182-193. https://dx.doi.org/10.1016/j.pestbp.2010.01.004.
Zobiole, L. H. S., Oliveira, R. S., Kremer, R. J., Constantin, J., Yamada, T., Castro, C., Oliveira, F. A., & Oliveira, A. (2010a). Effect of glyphosate on symbiotic N2 fixation and nickel concentration in glyphosateresistant soybeans. Applied Soil Ecology, 44 (2), 176-180. http://dx.doi.org/10.1016/j.apsoil.2009.12.003.
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