Reação de linhagens de milho à estria bacteriana

PAB Pesquisa Agropecuária Brasileira Pesq. agropec. bras. 1678-3921 0100-204X Embrapa Secretaria de Pesquisa e Desenvolvimento; Pesquisa Agropecuária Brasileira Resumo O objetivo deste trabalho foi selecionar linhagens experimentais de milho geneticamente resistentes à estria bacteriana causada por Xanthomonas vasicola pv. vasculorum, em duas safras. Os tratamentos foram realizados em um delineamento experimental em blocos ao acaso, nas safras 2019/2020 e 2020/2021, em ambiente coberto e com ventilação aberta, com quatro repetições. Sete linhagens resistentes e sete suscetíveis a doenças foliares foram avaliadas, além de dois híbridos comerciais, utilizados como controles. No estágio de florescimento do milho, foi realizada a inoculação artificial com 3,78x1010 UFC mL−1 de suspensão bacteriana, e a incidência e a severidade da doença foram avaliadas, com base em escala diagramática, a cada sete dias. A partir destas avaliações, as áreas abaixo da curva de progresso da doença foram calculadas para cada linhagem, e as análises de variância individuais e conjuntas foram realizadas. Há variabilidade genética entre os genótipos de milho quanto à reação à estria bacteriana, com efeito significativo para as áreas sob as curvas de progresso da doença quanto à incidência (AUDPCI) e à severidade (AUDPCS) entre genótipos e entre safras, e quanto à interação genótipo x safra. As linhagens LV1 e L14 são possíveis genótipos fontes de resistência genética à estria bacteriana. Introduction Several foliar diseases can affect corn (Zea mays L.) during its cycle, directly iinfluencing the yield and final quality of grains. In recent years, a new foliar disease, called bacterial leaf streak, whose etiological agent is the bacterium Xanthomonas vasicola pv. vasculorum (Cobb, 1894), has been observed in the main corn producing countries, including Brazil (Leite et al., 2019; Tebaldi et al., 2022). Bacterial leaf streak manifests mainly in areas subjected to irrigation or areas with regular rainfall (Ortiz-Castro et al., 2020), presenting its initial symptoms through small punctures, due to cell extravasation. These spots progress to elongated lesions, surrounded by a yellowish halo limited by the veins. The disease can progress to such a point that it affects a large leaf area, compromising the crop productivity (Leite et al., 2019). In general, the control of bacterial diseases is, difficult due to the rapid spread of the pathogen, the severity of losses, and the limitations of chemical control (Sundin et al., 2016). The main management measures include the use of windbreaks, equipment disinfestation, diseased plants eradication, and the use of copper-based fungicides (Peitl et al., 2017), which are inefficient for the majority of crops affected by phytopathogenic bacteria (Longhi et al., 2022). Plant genetic resistance comes as a possibility of control, and it is more efficient and less costly to the farmer, as it allows of the adoption of other techniques (Sousa et al., 2020). For diseases caused by species of the Xanthomonas genus, the genetic resistance is the main strategy for reducing losses (Bernal et al., 2020), since some species are insensitive to copper and, under high disease pressure, these molecules lose effectiveness (Liao et al., 2019). To obtain hybrids that are resistant to a plant pathogen, it is necessary to evaluate different genotypes from different origins, which may provide phenotypes of interest. The existence of genetic variability is important for the study of these genotypes, so that they can be included in a breeding program (Faleiro et al., 2008). The objective ofthis work was to select experimental corn lines which are resistant to bacterial leaf streak, for two seasons. Materials and Methods The experiments were carried out in the municipality of Guarapuava, in the state of Paraná (PR), Brazil, in the Department of Agronomy of Universidade Estadual do Centro-Oeste (Unicentro), in the Cedeteg Campus (25°23'00"S, 51°29'38.50"W, at 1,024 m altitude), in the 2019/2020 and 2020/2021 growing seasons. The climate of the region is Cfb, mesothermal humid subtropical, according to the Köppen-Geiger's classification. The bacteria isolate Xanthomonas vasicola pv. vasculorum (Xvv) was obtained from corn plants in the region of Guarapuava. For taxonomic confirmation of the isolate, the material was sent to a specialized laboratory and identified by a genetic sequencing of the 16S region. The isolate is stored in the phytopathological collection of the phytopathology laboratory of Unicentro, where subcultures are carried out periodically. The corn lines used to conduct the experiment came from the corn breeding program of Unicentro, taking into account the productive potential and some level of resistance to foliar diseases (Table 1). Based on the history of disease assessments in previous seasons, fourteen lines with different levels of susceptibility or resistance to foliar diseases were selected. In addition to these, the B2401PWU and BG7318YH commercial hybrids were used as standard checks of resistance and susceptibility to bacterial leaf streak (BLS), respectively, based on field observations by experienced researchers. Table 1 Lines and hybrids of corn (Zea mays) selected for genetic resistance to bacterial leaf streak (Xanthomonas vasicola pv. vasculorum), in the 2019/2020 and 2020/2021 growing seasons, in the municipality of Guarapuava, in the state of Paraná, Brazil. Genetic material Origin Generation B2401PWU Corteva Hybrid(1) BG7318YH Corteva Hybrid(2) LV1 AG8080 S8 LV4 DKB350 S8 LV5 AG6018 S8 L160 POP30 (P30P37 x 8460) S7 L18 POP30 (P30P37 x 8460) S7 L54.1 POP102 (P30B39) S5 L4.1 POP103 (AS1572) S5 L52.3 POP103 (AS1572) S5 LV2 CD303 S8 LV6 P30F33 S8 L14 POP29 (Penta x P30F53) S7 L20 POP31 (Penta) S7 L71 POP31 (Penta) S7 L73.1 POP103 (AS1572) S4 (1) Resistant check. (2) Susceptible check. An area covered with 150-micra transparent plastic film, with open windows and ample ventilation was used during two growing seasons for the experiment, and the genotypes were sown on November 11, 2019 and November 13, 2020. An experimental randomized block design was carried out with 16 genotypes (Table 1), which composed the treatments, and four replicates. Each plot consisted of three pots containing one plant each, totaling three plants per plot per replicate. The plants were grown in 18 L polypropylene pots, containing a mixture of soil (50%), sand (25%) and bio-stabilized pine bark-based substrate (25%). The soil used is classified as a Brown Oxisol (Santos et al., 2018), with a very clayey texture. At sowing, the substrate was fertilized with the 08-30-20 NPK formulation. Seed of the evaluated lines were subjected to treatment with imidacloprid + thiodicarb, to protect them against initial pests. Three seed were sown per pot, with one plant remaining after thinning 20 days after sowing. The plants were irrigated by drip, and cultural treatments related to nitrogen fertilization and insect management were carried out in accordance with the technical recommendations for the crop (Pauletti & Motta, 2019). A bacterial suspension (Xvv) in 0.85% saline solution (NaCl) was prepared using young colonies (48 hours). The suspension was adjusted to 0.6 absorbance in a spectrophotometer (OD580 nm, BEL Photonics, model UV-M51), with 3.78x1010 CFU mL−1, according to Lautenchleger et al. (2023). Plant irrigation was performed two hours before the inoculation to fully open the stomata. Plant inoculation was carried out at full flowering, by spraying the bacterial suspension with a manual sprayer on the adaxial surface of all plant leaves, until they drained (Lautenchleger et al., 2023). In the 2019/2020 growing season, the inoculation was carried out in the thirteenth week, and the evaluation period lasted for six weeks. In the 2020/2021 growing season, in the 12th week, the plants were subjected to inoculation and evaluated until the twentieth week. As the experimental area is a space with open ventilation, climate data from the external environment, coming from the local meteorological station, were considered. In the 2019/2020 growing season, the average temperature at the experimental site was 18.8°C. and the relative humidity (RH) was 67%. In the 2020/2021 growing season, the averages were higher: 20.5°C and 80%. From the inoculation time until the end of the evaluations, the averages were 21°C and 73% RH, and 20.5°C and 78% RH for the 2019 and 2020 seasons, respectively (Figure 1). Figure 1 Weekly average temperature and relative humidity (RH) data from the meteorological station, in the municipality of Guarapuava, in the state of Paraná (PR), Brazil, during the 2019/2020 and 2020/2021 corn (Zea mays) growing seasons. From the inoculation date on, the genotypes’ reaction to the pathogen were assessed every seven days. In each plot, symptomatic leaves were counted to calculate the incidence, and severity scores were assigned with basis on the diagrammatic scale proposed by Braga et al. (2020). The incidence and severity values obtained were submitted to the calculation of the area under the disease progress curve (AUDPC) according to Shaner & Finney (1977). Individual and joint analyses of variance were performed for the two growing seasons. Hybrids and lines were evaluated together, due to the unavailability of other genotypes, especially lines that showed resistance to the disease. Then, the significant variables were submitted to comparison of the means by the Scott-Knott’s test, at 5% probability, using the Sisvar program, version 4.0 (Ferreira, 2019). Results and Discussion There was a significant effect for the areas under the progress curve of incidence (AUDPCI) and severity (AUDPCS) among genotypes, between seasons, and for the genotypes x seasons interaction. For the developments of the interaction, there was a significant difference for AUDPCI (Table 2), in both seasons, and for only AUDPCS (Table 3) in the 2020/2021 season. When considering season within each genotype, AUDPCI was significant for both growing seasons. For AUDPCS, there was significance for the LV4, LV5, L160, L18, L54.1, L4.1, L20, L71, and L73.1 lines. Table 2 Breakdown of the genotype x season interaction, based on the means of the area under the incidence progress curve of bacterial leaf streak caused by Xanthomonas vasicola pv. vasculorum in corn (Zea mays), in the municipality of Guarapuava, in the state of Paraná, Brazil(1). Genotype Season 2019/2020 2020/2021 B2401PWU 0.00 Aa 2377.26 Ba BG7318YH 1029.00 Ab 3220.99 Ba LV1 147.00 Aa 2920.28 Ba LV4 401.62 Aa 3704.52 Bb LV5 141.75 Aa 3003.58 Ba L160 663.25 Aa 3602.80 Bb L18 1404.37 Ab 3811.22 Bb L54.1 1411.37 Ab 3986.74 Bb L4.1 113.75 Aa 4118.43 Bb L52.3 130.37 Aa 3579.44 Bb LV2 1250.37 Ab 3561.79 Bb LV6 289.62 Aa 3540.46 Bb L14 336.00 Aa 3117.85 Ba L20 1544.37 Ab 3912.80 Bb L71 925.75 Ab 3950.82 Bb L73.1 512.75 Aa 4238.54 Bb (1) Means followed by equal letters, lowercases in the columns and uppercases in the rows, belong to the same group, by Scott-Knott’s test, at 5% probability. Table 3 Breakdown of the genotype x season interaction, based on the means of the area under the severity progress curve of bacterial leaf streak, caused by Xanthomonas vasicola pv. vasculorum in corn (Zea mays), in the municipality of Guarapuava, in the state of Paraná, Brazil(1). Genotype Season 2019/2020 2020/2021 B2401PWU 0.00 Aa 31.00 Aa BG7318YH 16.72 Aa 35.66 Aa LV1 0.72 Aa 33.19 Aa LV4 4.16 Aa 48.66 Ba LV5 0.71 Aa 64.63 Bb L160 6.52 Aa 64.60 Ba L18 20.99 Aa 97.44 Bb L54.1 30.63 Aa 93.15 Bb L4.1 0.92 Aa 142.45 Bc L52.3 0.89 Aa 39.34 Aa LV2 14.62 Aa 51.87 Aa LV6 2.32 Aa 36.49 Aa L14 3.49 Aa 42.95 Aa L20 15.04 Aa 280.06 Bd L71 8.83 Aa 61.14 Ba L73.1 2.87 Aa 91.31 Bb (1) Means followed by equal letters, lowercases in the columns and uppercases in the rows, belong to the same group, by Scott-Knott’s test, at 5% probability. In the 2020/2021 growing season, the averages for AUDPCI (Table 2) and AUDPCS (Table 3) of bacterial leaf streak in corn were significantly higher than in the 2019/2020 season. Considering that the experiment was under the influence of external climatic variables, variations of temperature and humidity over the years may have influenced the expression of the disease (Figure 1). All genotypes showed higher AUDPCI values in the second growing season than in the first one (Table 2). The AUDPCS was higher in the second season only for some lines (Table 3), showing that the expression of the disease is influenced by environmental factors, such as air temperature and relative humidity, as well as for other foliar diseases in corn (Hooda et al., 2017; Ortiz-Bustos et al., 2019). When analyzing each growing season separately, the genotypes also showed differences for the incidence and severity of the disease. The B2401PWU hybrid, considered a resistant check, showed low values for both AUDPCI and AUDPCS, within the genotypes. The BG7318YH hybrid, used as susceptible check, showed high incidence values of area under the progress curve, in the 2019/2020 season, but showed no statistical difference in comparison with the resistant control in the 2020/2021 season. The L4.1 and L20 lines showed higher means for AUDPCS and were even more susceptible to the pathogen than the susceptible check itself in the 2020/2021 season. Genotypes resistant to a pathogen may have some form of limitation to their multiplication, or even delay their development (Råberg, 2014). When evaluating a foliar disease, it is expected that lines that have resistance genes will show no or little progress of the disease over time. However, as most disease resistance inheritance in corn has a polygenic origin, it is natural that there are different levels of incidence and severity between genotypes and between seasons (Ferreira et al., 2024). Even so, it is important that stable genotypes (those showing similar responses between environments and seasons) be identified (Bocianowski et al., 2020). Preliminary studies indicate that corn resistance to BLS is quantitative (Qiu et al., 2020). Historically, this is the main type of resistance implemented in commercial hybrids, and it is preferable in relation to the qualitative resistance because, as it is governed by a large number of genes, it is generally effective against several races of the same pathogen, thus becoming more durable over time (Miedaner & Juroszek, 2021). The fact that the checks showed discrepant values between seasons suggests that the performances can vary, even in genotypes considered stable, due to climatic variables (Figure 1) and the nature of resistance. This highlights the complexity of managing bacterial diseases in corn and the need to comprehensively assess the susceptibility to BLS in commercial hybrids. It is worth pointing out that, at the time this experiment was carried out, there was little information on the susceptibility of commercial hybrids, and that this work was a pioneer in studies regarding genetic resistance to the disease. Combinations of genetic control with other cultural practices, such as crop rotation, and the use of chemicals can help manage the disease (Duin et al., 2022). Bacterial leaf streak was quantified as a function of commercial corn hybrids, associated with chemical control and identified resistant and susceptible genotypes by Pietrobon et al. (2021). However, in susceptible material, the adoption of chemical control allowed of 55% reduction in AUDPC in relation to the control. The L18, L54.1, LV2, L20, and L71 lines undergone high incidence of disease in both growing seasons, which could be a negative aspect. Even with a significant difference for incidence between the growing seasons, the LV1, LV5, and L14 lines stood out positively, showing lower incidence values in both seasons (Table 2). In the evaluation period of the 2019/2020 growing season, in which incidence and severity values were lower, a peak of the average temperature was recorded (22.5°C), together with the minimum average RH, throughout the entire period (60%) (Figure 1). In the 2020/2021 growing season, the weekly average RH, in the evaluation period, was not less than 69%, and the average maximum temperature was 21.8°C. These data indicate that higher RH favored the development of the disease, corroborating the results found by Hartman et al. (2020), who identified an increase in the severity of BLS, in conditions of 100% relative humidity. Any irrigation system in corn cultivations, combined with high relative humidity, favors the occurrence of the disease, as this combination allows of longer stomatal opening time, the main gateway to Xvv (Korus et al., 2017). When comparing the progression of incidence and severity, especially in the 2020/2021 growing season, it can be observed that the incidence was high in practically all genotypes (Table 2). However, the same performance was not observed for severity (Table 3). This indicates that the pathogen was able to infect plants, but conditions were not favorable for its colonization, suggesting that these lines have some type of defense mechanism to the bacteria (Amaral et al., 2019). These results corroborate preliminary studies which report that resistance to BLS is quantitative in nature and that genetic control can be used in the disease management, together with other techniques, especially chemical control. Therefore, the lines that showed the lowest disease progress curves are indicated to make part of a breeding program, in which they can be crossed with other promising genotypes with high productive potential, and their combining capabilities can be estimated (Lima & Borém, 2018). Conclusions There is genetic variability among the evaluated corn (Zea mays) genotypes regarding the reaction to corn bacterial leaf streak (Xanthomonas vasicola pv. vasculorum). A significant effect for incidence and severity of bacterial leaf streak occurs among genotypes and among seasons, as well as in the genotype x season interaction. Lines LV1 and L14 show the lowest values of area under the incidence and severity progress curve, and are presented as possible genotypes as source of corn resistance to bacterial leaf streak. Acknowledgments To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Finance Code 001), for providing a scholarship to the first author; and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for granting scholarships to the fifth and sixth authors. References AMARAL, L.S.; DEBONA, D.; COSTA, L.C.; SILVA, A.L.R.; OLIVEIRA, J.R.; RODRIGUES, F.A. Biochemical insights into basal and induced resistance in cabbage to black rot. Journal of Phytopathology, v.167, p.390-403, 2019. DOI: https://doi.org/10.1111/jph.12808. AMARAL L.S. DEBONA D. COSTA L.C. SILVA A.L.R. OLIVEIRA J.R. RODRIGUES F.A. Biochemical insights into basal and induced resistance in cabbage to black rot Journal of Phytopathology 167 390 403 2019 https://doi.org/10.1111/jph.12808 BERNAL, E.; LIABEUF, D.; FRANCIS, D.M. Evaluating quantitative trait locus resistance in tomato to multiple Xanthomonas spp. Plant Disease, v.104, p.423-429, 2020. DOI: https://doi.org/10.1094/PDIS-03-19-0669-RE. BERNAL E. LIABEUF D. FRANCIS D.M. Evaluating quantitative trait locus resistance in tomato to multiple Xanthomonas spp Plant Disease 104 423 429 2020 https://doi.org/10.1094/PDIS-03-19-0669-RE BOCIANOWSKI, J.; TRATWAL, A.; NOWOSAD, K. Genotype by environment interaction for area under the disease-progress curve (AUDPC) value in spring barley using additive main effects and multiplicative interaction model. Australasian Plant Pathology, v.49, p.525-529, 2020. DOI: https://doi.org/10.1007/s13313-020-00723-7. BOCIANOWSKI J. TRATWAL A. NOWOSAD K. Genotype by environment interaction for area under the disease-progress curve (AUDPC) value in spring barley using additive main effects and multiplicative interaction model Australasian Plant Pathology 49 525 529 2020 https://doi.org/10.1007/s13313-020-00723-7 BRAGA, K.; FANTIN, L.H.; ROY, J.M.T.; CANTERI, M.G.; CUSTÓDIO, A.A. de P. Development and validation of a diagrammatic scale for the assessment of the severity of bacterial leaf streak of corn. European Journal of Plant Pathology, v.157, p.367-375, 2020. DOI: https://doi.org/10.1007/s10658-020-02008-7. BRAGA K. FANTIN L.H. ROY J.M.T. CANTERI M.G. CUSTÓDIO A.A. de P. Development and validation of a diagrammatic scale for the assessment of the severity of bacterial leaf streak of corn European Journal of Plant Pathology 157 367 375 2020 https://doi.org/10.1007/s10658-020-02008-7 DUIN, I.M.; FORASTEIRO, T.A.; RODRIGUES, V.H.S.; BALBI-PEÑA, M.I.; LEITE JÚNIOR, R.P. In vitro sensitivity of Xanthomonas vasicola pv. vasculorum and the control of bacterial leaf streak of corn with copper oxychloride alone and in mixtures with mancozeb and fluxapyroxad. European Journal of Plant Pathology, v.164, p.263-268, 2022. DOI: https://doi.org/10.1007/s10658-022-02556-0. DUIN I.M. FORASTEIRO T.A. RODRIGUES V.H.S. BALBI-PEÑA M.I. LEITE R.P. JÚNIOR In vitro sensitivity of Xanthomonas vasicola pv. . vasculorum and the control of bacterial leaf streak of corn with copper oxychloride alone and in mixtures with mancozeb and fluxapyroxad European Journal of Plant Pathology 164 263 268 2022 https://doi.org/10.1007/s10658-022-02556-0 FALEIRO, F.G.; FARIAS NETO, A.L. de; RIBEIRO JUNIOR, W.Q. (Ed.). Pré-melhoramento, melhoramento e pósmelhoramento: estratégias e desafios. Planaltina: Embrapa Cerrados, 2008. 183p. FALEIRO F.G. FARIAS A.L. de NETO RIBEIRO W.Q. JUNIOR Pré-melhoramento, melhoramento e pósmelhoramento: estratégias e desafios Planaltina Embrapa Cerrados 2008 183 183 FERREIRA, C.M.; SALUCI, J.C.G.; VIVAS, M.; SANTOS, J.S.; ANDRADE JUNIOR, M.S. de; VIVAS, J.M.S.; RAMOS, G.K.S.; GRAVIANA, G.A. Characterization of the Bipolaris maydis: symptoms and pathogenicity in popcorn genotypes (Zea mays L.). Brazilian Journal of Biology, v.84, e256799, 2024. DOI: https://doi.org/10.1590/1519-6984.256799. FERREIRA C.M. SALUCI J.C.G. VIVAS M. SANTOS J.S. ANDRADE M.S. de JUNIOR VIVAS J.M.S. RAMOS G.K.S. GRAVIANA G.A. Characterization of the Bipolaris maydis: symptoms and pathogenicity in popcorn genotypes (Zea mays L.) Brazilian Journal of Biology 84 e256799 2024 https://doi.org/10.1590/1519-6984.256799 FERREIRA, D.F. Sisvar: a computer analysis system to fixed effects split plot type designs. Revista Brasileira de Biometria, v. 37, p.529-535, 2019. DOI: https://doi.org/10.28951/rbb.v37i4.450. FERREIRA D.F. Sisvar: a computer analysis system to fixed effects split plot type designs Revista Brasileira de Biometria 37 529 535 2019 https://doi.org/10.28951/rbb.v37i4.450 HARTMAN, T.; HARBOUR, J.; THARNISH, B.; METER, J. VAN; JACKSON-ZIEMS, T.A. Agronomic factors associated with bacterial leaf streak development caused by Xanthomonas vasicola pv. vasculorum in corn. Phytopathology, v.110, p.1132-1138, 2020. DOI: https://doi.org/10.1094/PHYTO-02-20-0043-R. HARTMAN T. HARBOUR J. THARNISH B. METER J. VAN JACKSON-ZIEMS T.A. Agronomic factors associated with bacterial leaf streak development caused by Xanthomonas vasicola pv. vasculorum in corn Phytopathology 110 1132 1138 2020 https://doi.org/10.1094/PHYTO-02-20-0043-R HOODA, K.S.; KHOKHAR, M.K.; SHEKHAR, M.; KARJAGI, C.G.; KUMAR, B.; MALLIKARJUNA, N.; DEVLASH, R.K.; CHANDRASHEKARA, C.; YADAV, O.P. Turcicum leaf blight - sustainable management of a re-emerging maize disease. Journal of Plant Diseases and Protection, v.124, p.101-113, 2017. DOI: https://doi.org/10.1007/s41348-016-0054-8. HOODA K.S. KHOKHAR M.K. SHEKHAR M. KARJAGI C.G. KUMAR B. MALLIKARJUNA N. DEVLASH R.K. CHANDRASHEKARA C. YADAV O.P. Turcicum leaf blight - sustainable management of a re-emerging maize disease Journal of Plant Diseases and Protection 124 101 113 2017 https://doi.org/10.1007/s41348-016-0054-8 KORUS, K.; LANG, J.M.; ADESEMOYE, A.O.; BLOCK, C.C.; PAL, N.; LEACH, J.E.; JACKSON-ZIEMS, T.A. First report of Xanthomonas vasicola causing bacterial leaf streak on corn in the United States. Plant Disease, v.101, p.1030, 2017. DOI: https://doi.org/10.1094/PDIS-10-16-1426-PDN. KORUS K. LANG J.M. ADESEMOYE A.O. BLOCK C.C. PAL N. LEACH J.E. JACKSON-ZIEMS T.A. First report of Xanthomonas vasicola causing bacterial leaf streak on corn in the United States Plant Disease 101 1030 1030 2017 https://doi.org/10.1094/PDIS-10-16-1426-PDN LAUTENCHLEGER, F.; FARIA, M.V.; FARIA, C.M.D.R.; SANTOS, L.A.; GASPEROTTO, L.M.; ANDREOLI, P.H.W.; GAVA, E.; SILVA, E.M.M. Bacterial leaf streak: inoculation methodology determination. Tropical Plant Pathology, v.48, p.720-727, 2023. DOI: https://doi.org/10.1007/s40858-023-00611-7. LAUTENCHLEGER F. FARIA M.V. FARIA C.M.D.R. SANTOS L.A. GASPEROTTO L.M. ANDREOLI P.H.W. GAVA E. SILVA E.M.M. Bacterial leaf streak: inoculation methodology determination Tropical Plant Pathology 48 720 727 2023 https://doi.org/10.1007/s40858-023-00611-7 LEITE JR., R.P.; CUSTÓDIO, A.A.P.; MADALOSSO, T.; ROBAINA, R.R.; DUIN, I.M.; SUGAHARA, V.H. First report of the occurrence of bacterial leaf streak of corn caused by Xanthomonas vasicola pv. vasculorum in Brazil. Plant Disease, v.103, p.145, 2019. DOI: https://doi.org/10.1094/PDIS-06-18-1100-PDN. LEITE R.P. JR. CUSTÓDIO A.A.P. MADALOSSO T. ROBAINA R.R. DUIN I.M. SUGAHARA V.H. First report of the occurrence of bacterial leaf streak of corn caused by Xanthomonas vasicola pv. vasculorum in Brazil Plant Disease 103 145 145 2019 https://doi.org/10.1094/PDIS-06-18-1100-PDN LIAO, Y.-Y.; STRAYER-SCHERER, A.L.; WHITE, J.; MUKHERJEE, A.; LA TORRE-ROCHE, R. de; RITCHIE, L.; COLEE, J.; VALLAD, G.E.; FREEMAN, J.H.; JONES, J.B.; PARET, M.L. Nano-magnesium oxide: a novel bactericide against copper-tolerant Xanthomonas perforans causing tomato bacterial spot. Phytopathology, v.109, p.52-62, 2019. DOI: https://doi.org/10.1094/PHYTO-05-18-0152-R. LIAO Y.-Y. STRAYER-SCHERER A.L. WHITE J. MUKHERJEE A. LA TORRE-ROCHE R. de RITCHIE L. COLEE J. VALLAD G.E. FREEMAN J.H. JONES J.B. PARET M.L. Nano-magnesium oxide: a novel bactericide against copper-tolerant Xanthomonas perforans causing tomato bacterial spot Phytopathology 109 52 62 2019 https://doi.org/10.1094/PHYTO-05-18-0152-R LIMA, R. de; BORÉM, A. (Ed.). Melhoramento de milho. Viçosa: UFV, 2018. 396p. LIMA R. de BORÉM A. Melhoramento de milho. Viçosa UFV 2018 396 396 LONGHI, T.V.; ROBAINA, R.R.; LEITE JÚNIOR, R.P.; BALBI-PEÑA, M.I. Sensibility of Xanthomonas vasicola pv. vasculorum to chemicals and efficiency of the chemical control of bacterial leaf streak on corn plants. Acta Scientiarum. Agronomy, v.44, e54952, 2022. DOI: https://doi.org/10.4025/actasciagron.v44i1.54952. LONGHI T.V. ROBAINA R.R. LEITE R.P. JÚNIOR BALBI-PEÑA M.I. Sensibility of Xanthomonas vasicola pv. vasculorum to chemicals and efficiency of the chemical control of bacterial leaf streak on corn plants Acta Scientiarum. Agronomy 44 e54952 2022 https://doi.org/10.4025/actasciagron.v44i1.54952 MIEDANER, T.; JUROSZEK, P. Global warming and increasing maize cultivation demand comprehensive efforts in disease and insect resistance breeding in north-western Europe. Plant Pathology, v.70, p.1032-1046, 2021. DOI: https://doi.org/10.1111/ppa.13365. MIEDANER T. JUROSZEK P. Global warming and increasing maize cultivation demand comprehensive efforts in disease and insect resistance breeding in north-western Europe Plant Pathology 70 1032 1046 2021 https://doi.org/10.1111/ppa.13365 ORTIZ-BUSTOS, C.M.; LÓPEZ-BERNAL, A.; TESTI, L.; MOLINERO-RUIZ, L. Environmental and irrigation conditions can mask the effect of Magnaporthiopsis maydis on growth and productivity of maize. Plant Pathology, v.68, p.1555-1564, 2019. DOI: https://doi.org/10.1111/ppa.13070. ORTIZ-BUSTOS C.M. LÓPEZ-BERNAL A. TESTI L. MOLINERO-RUIZ L. Environmental and irrigation conditions can mask the effect of Magnaporthiopsis maydis on growth and productivity of maize Plant Pathology 68 1555 1564 2019 https://doi.org/10.1111/ppa.13070 ORTIZ-CASTRO, M.; HARTMAN, T.; COUTINHO, T.; LANG, J.M.; KORUS, K.; LEACH, J.E.; JACKSON-ZIEMS, T.; BRODERS, K. Current understanding of the history, global spread, ecology, evolution, and management of the corn bacterial leaf streak pathogen, Xanthomonas vasicola pv. vasculorum. Phytopathology, v.110, p.1124-1131, 2020. DOI: https://doi.org/10.1094/PHYTO-01-20-0018-PER. ORTIZ-CASTRO M. HARTMAN T. COUTINHO T. LANG J.M. KORUS K. LEACH J.E. JACKSON-ZIEMS T. BRODERS K. Current understanding of the history, global spread, ecology, evolution, and management of the corn bacterial leaf streak pathogen, Xanthomonas vasicola pv. vasculorum. Phytopathology 110 1124 1131 2020 https://doi.org/10.1094/PHYTO-01-20-0018-PER PAULETTI, V.; MOTTA, A.C.V. (Coord.). Manual de adubação e calagem para o Estado do Paraná. 2.ed. Curitiba: Sociedade Brasileira de Ciência do Solo, 2019. 289p. PAULETTI V. MOTTA A.C.V. Manual de adubação e calagem para o Estado do Paraná. 2 Curitiba Sociedade Brasileira de Ciência do Solo 2019 289 289 PEITL, D.C.; ARAUJO, F.A.; GONÇALVES, R.M.; SANTIAGO, D.C.; SUMIDA, C.H.; BALBI-PEÑA, M.I. Biological control of tomato bacterial spot by saprobe fungi from semi-arid areas of northeastern Brazil. Semina: Ciências Agrárias, v.38, p.1251-1264, 2017. DOI: https://doi.org/10.5433/1679-0359.2017v38n3p1251. PEITL D.C. ARAUJO F.A. GONÇALVES R.M. SANTIAGO D.C. SUMIDA C.H. BALBI-PEÑA M.I. Biological control of tomato bacterial spot by saprobe fungi from semi-arid areas of northeastern Brazil Semina: Ciências Agrárias 38 1251 1264 2017 https://doi.org/10.5433/1679-0359.2017v38n3p1251 PIETROBON, A.J.; DUARTE JÚNIOR, J.B.; KUHN, O.J. Chemical products for corn bacterial streak control. Pesquisa Agropecuária Tropical, v.51, e68121, 2021. DOI: https://doi.org/10.1590/1983-40632021v5168121. PIETROBON A.J. DUARTE J.B. JÚNIOR KUHN O.J. Chemical products for corn bacterial streak control Pesquisa Agropecuária Tropical 51 e68121 2021 https://doi.org/10.1590/1983-40632021v5168121 QIU, Y.; KAISER, C.; SCHMIDT, C.; BRODERS, K.; ROBERTSON, A.E.; JAMANN, T.M. Identification of quantitative trait loci associated with maize resistance to bacterial leaf streak. Crop Science, v.60, p.226-237, 2020. DOI: https://doi.org/10.1002/csc2.20099. QIU Y. KAISER C. SCHMIDT C. BRODERS K. ROBERTSON A.E. JAMANN T.M. Identification of quantitative trait loci associated with maize resistance to bacterial leaf streak Crop Science 60 226 237 2020 https://doi.org/10.1002/csc2.20099 RÅBERG, L. How to live with the enemy: understanding tolerance to parasites. PLoS Biology, v.12, e1001989, 2014. DOI: https://doi.org/10.1371/journal.pbio.1001989. RÅBERG L. How to live with the enemy: understanding tolerance to parasites PLoS Biology 12 e1001989 2014 https://doi.org/10.1371/journal.pbio.1001989 SANTOS, H.G. dos; JACOMINE, P.K.T.; ANJOS, L.H.C. dos; OLIVEIRA, V.Á. de; LUMBRERAS, J.F.; COELHO, M.R.; ALMEIDA, J.A. de; ARAÚJO FILHO, J.C. de; OLIVEIRA, J.B. de; CUNHA, T.J.F. Sistema brasileiro de classificação de solos. 5.ed. rev. e ampl. Brasília: Embrapa, 2018. 356p. SANTOS H.G. dos JACOMINE P.K.T. ANJOS L.H.C. dos OLIVEIRA V.Á. de LUMBRERAS J.F. COELHO M.R. ALMEIDA J.A. de ARAÚJO J.C. de FILHO OLIVEIRA J.B. de CUNHA T.J.F. Sistema brasileiro de classificação de solos. 5 Brasília Embrapa 2018 356 356 SHANER, G.; FINNEY, R.E. The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knox wheat. Phytopathology, v.67, p.1051-1056, 1977. DOI: https://doi.org/10.1094/Phyto-67-1051. SHANER G. FINNEY R.E. The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knox wheat Phytopathology 67 1051 1056 1977 https://doi.org/10.1094/Phyto-67-1051 SOUSA, A.M. de C.B. de; CHAVAGLIA, A.C.; CIVARDI, E.A.; PINTO, J.F.N.; REIS, E.F. dos. Genetic dissimilarity for resistance to foliar diseases associated with the agronomic potential in maize. Revista Caatinga, v.33, p.936-944, 2020. DOI: https://doi.org/10.1590/1983-21252020v33n408rc. SOUSA A.M. de C.B. de CHAVAGLIA A.C. CIVARDI E.A. PINTO J.F.N. REIS E.F. dos. Genetic dissimilarity for resistance to foliar diseases associated with the agronomic potential in maize Revista Caatinga 33 936 944 2020 https://doi.org/10.1590/1983-21252020v33n408rc SUNDIN, G.W.; CASTIBLANCO, L.F.; YUAN, X.; ZENG, Q.; YANG, C.-H. Bacterial disease management: challenges, experience, innovation and future prospects. Molecular Plant Pathology, v.17, p.1506-1518, 2016. DOI: https://doi.org/10.1111/mpp.12436. SUNDIN G.W. CASTIBLANCO L.F. YUAN X. ZENG Q. YANG C.-H. Bacterial disease management: challenges, experience, innovation and future prospects Molecular Plant Pathology 17 1506 1518 2016 https://doi.org/10.1111/mpp.12436 TEBALDI, N.D.; PEREIRA, J.N.P.; SAGATA, E.; MOTA, L.C.B.M.; HORA JUNIOR, B.T. da; PIAZZOLI, D.; KLOSOWSKI, A.C. Occurrence and detection of Xanthomonas vasicola pv. vasculorum in naturally contaminated maize seeds in Brazil. Tropical Plant Pathology, v.47, p.698-702, 2022. DOI: https://doi.org/10.1007/s40858-022-00514-z. TEBALDI N.D. PEREIRA J.N.P. SAGATA E. MOTA L.C.B.M. HORA B.T. da JUNIOR PIAZZOLI D. KLOSOWSKI A.C. Occurrence and detection of Xanthomonas vasicola pv. vasculorum in naturally contaminated maize seeds in Brazil Tropical Plant Pathology 47 698 702 2022 https://doi.org/10.1007/s40858-022-00514-z