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Popcorn germplasm resistance to fungal diseases caused by Exserohilum turcicum and Bipolaris maydis

ABSTRACT

Compared with the common corn, popcorn shows greater susceptibility to pests and diseases occurrence, being the use of resistant cultivars the most efficient strategy. In this regard, Germplasm Banks deserve special attention because they contain accessions that can be used as sources of resistance in breeding programs. The State University of Northern Rio de Janeiro (UENF) maintains a popcorn Germplasm Bank with accessions from tropical and temperate countries, including Diversity Centers for the species. In this study, we investigated the performance of 37 popcorn accessions landraces, hybrids, and inbreed lines ― from the Germplasm Collection of UENF’s Popcorn Breeding Program with respect to the fungal leaf diseases northern leaf blight (NLB) and southern leaf blight (SLB), caused by Exserohilum turcicum and Bipolaris maydis, aiming to select promising accessions for genetic resistance to be used in future crosses to generate new resistant cultivars for farmers. The dendrogram scattering by the UPGMA multivariate technique was efficient in discriminating resistant accessions. Satisfactory results were obtained for resistance to NLB in accessions L71, L75, L76, P7, and PARA-172, which can thus be considered remarkable sources of resistance. For resistance to SLB, the superior accessions that can be indicated as sources of resistance are ARZM-05083, ARZM-07049, and PARA-172.

Key words
Zea mays; northern leaf blight; genetic resistance; plant breeding

INTRODUCTION

Popcorn (Zea mays L.) is a type of corn whose main characteristics are its hard and small kernels and the ability to expand due to the pressure formed inside the grains upon heating. When compared with cultivars of common corn, popcorn plants usually display greater susceptibility of pests and diseases occurrence (Arnhold 2008Arnhold, E. (2008). Seleção para resistência a doenças foliares em famílias S1 de milho-pipoca. Revista Ceres, 55, 89-93.; Hallauer and Carena 2009Hallauer, A.R. and Carena, M.J. (2009). Maize Breeding. In M. J. Carena (Ed.), Handbook of Plant Breeding: Cereals (p. 3-98). New York: Springer.; Ribeiro et al. 2016Ribeiro, R.M., Amaral Júnior, A.T., Pena, G.F., Vivas, M., Kurosawa, R.N.F. and Gonçalves, L.S.A. (2016). History of northern corn leaf blight disease in the seventh cycle of recurrent selection of an UENF-14 popcorn population. Acta Scientiarum Agronomy, 38, 1-10. https://doi.org/10.4025/actasciagron.v38i4.30573.
https://doi.org/10.4025/actasciagron.v38...
). Among the leaf diseases affecting popcorn, the common blotch (northern leaf blight, NLB), caused by Exserohilum turcicum (Pass.) Leonard and Suggs (syn. Helminthosporium turcicum Pass.), is characterized as one of the major (Harlapur et al. 2008Harlapur, S.I., Kulkarni, M.S., Wali, M.C., Srikant, K., Yashoda, H. and Patil, B.C. (2008). Status of turcicum leaf blight of maize in Karnataka. Journal of Agricultural Science, 21, 55-60.; Hurni et al. 2015Hurni, S., Scheuermann, D., Krattinger, S.G., Kessel, B., Wicker, T., Herren, G., Fitze, M.N., Breen, J., Presterl, T., Ouzunova, M. and Keller, B. (2015). The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proceedings of the National Academy of Sciences, 112, 8780-8785. https://doi.org/10.1073/pnas.1502522112.
https://doi.org/10.1073/pnas.1502522112...
; Ishfaq et al. 2014Ishfaq, A., Dar, Z.A., Lone, A.A., Ali, G., Gazal, A., Hamid, B. and Mohiddin, F.A. (2014). Disease reaction studies of maize (Zea mays L.) against turcicum leaf blight involving indigenously identified cytosterile source. African Journal of Microbiology Research, 8, 2592-2597. https://doi.org/10.5897/ajmr2014.6708.
https://doi.org/10.5897/ajmr2014.6708...
; Sabato et al. 2013Sabato, E.O., Pinto, N.F.J.A. and Fernandes, F.T. (2013). Identificação e Controle de Doenças na Cultura do Milho. 2. ed. rev. e ampl. Brasília: Embrapa.; Wang et al. 2014Wang, X., Zhang, Y., Xu, X., Li, H., Wu, X., Zhang, S. and Li, X. (2014). Evaluation of maize inbred lines currently used in Chinese breeding programs for resistance to six foliar diseases. The Crop Journal, 2, 213-222. https://doi.org/10.1016/j.cj.2014.04.004.
https://doi.org/10.1016/j.cj.2014.04.004...
). Under favorable climatic settings and in susceptible hosts, the pathogen may cause loses in grain yield that range from 27 to 90% (Ferguson and Carson 2007Ferguson, L.M. and Carson, M.L. (2007). Temporal variation in Setosphaeria turcica between 1974 and 1994 and origin of races 1, 23, and 23N in the United States. Phytopathology, 97, 1501-1511. https://doi.org/10.1094/phyto-97-11-1501.
https://doi.org/10.1094/phyto-97-11-1501...
; Muiru et al. 2010Muiru, E., Koopmann, B., Tiedemann, A.V., Mutitu, E.W. and Kimenju, W. (2010). Race Typing and Evaluation of Aggressiveness of Exserohilum turcicum Isolates of Kenyan, German and Austrian Origin. World Journal of Agricultural Sciences, 6, 277-284.; Wang et al. 2010; 2012Wang, H., Xiao, Z.X., Wang, F.G., Xiao, Y.N., Zhao, J.R.R., Zheng, Y.L. and Qiu, F.Z. (2012). Mapping of HtNB, a gene conferring nonlesion 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. https://doi.org/10.4238/2012.july.10.7.
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).

Another disease, the southern leaf blight (SLB), caused by the fungus Bipolaris maydis (Nisik.) Shoemaker (synonym of Helminthosporium maydis Nisik. and Myiake), occurs in corn with different intensities, depending on the degree of resistance, the crop management system, and the climatic conditions during its growth (Ali et al. 2011Ali, F., Rahman, H., Durrishahwar, Nawaz, I., Munir, M. and Ullah, H. (2011). Genetic analysis of maturity and morphological traits under Maydis Leaf Blight (MLB) epiphytotics in maize (Zea mays L.). Journal of Agricultural and Biological Science, 6, 1990-6145.; Altaf et al. 2016Altaf, M., Raziq, F., Khan, I., Hussain, H., Shah, B., Ullah, W., Naeem, A., Adnan, M., Junaid, K., Shah, S.R.A. and Attaullah, M.I. (2016). Study on the response of different maize cultivars to various inoculum levels of Bipolaris maydis (Y. Nisik & C. Miyake) shoemaker under field conditions. Journal of Entomology and Zoology Studies, 4, 533-537.; Hussain et al. 2016Hussain, H., Raziq, F., Khan, I., Shah, B., Altaf, M., Attaullah, Ullah, W., Naeem, A., Adnan, M., Junaid, K., Shah, S.R.A. and Iqbal, M. (2016). Effect of Bipolaris maydis (Y. Nisik & C. Miyake) shoemaker at various growth stages of different maize cultivars. Journal of Entomology and Zoology Studies, 4, 439-444.). Southern leaf blight is one of the most important diseases affecting corn and represents a great threat to corn growing all around the globe (Altaf et al. 2016Altaf, M., Raziq, F., Khan, I., Hussain, H., Shah, B., Ullah, W., Naeem, A., Adnan, M., Junaid, K., Shah, S.R.A. and Attaullah, M.I. (2016). Study on the response of different maize cultivars to various inoculum levels of Bipolaris maydis (Y. Nisik & C. Miyake) shoemaker under field conditions. Journal of Entomology and Zoology Studies, 4, 533-537.; Kump et al. 2011Kump, K.I., Bradbury, P.J., Wisser, R.J., Buckler, E.S., Belcher, A.R., Rosas, M.A.O., Zwonitzer, J.C., Kresovich, S., McMullen, M.D., Ware, D., Balint-Kurti, P.J. and Holland, J.B. (2011). Genome-wide association study of quantitative resistance to southern leaf blight in maize nested association mapping population. Nature Genetics, 43, 163-168. https://doi.org/10.1038/ng.747.
https://doi.org/10.1038/ng.747...
; Noor et al. 2015Noor, M., Rahman, H. and Iqbal, M. (2015). Evaluation of popcorn inbred lines for disease severity. Pure and Applied Biology, 4, 288-295. https://doi.org/10.19045/bspab.2015.43002.
https://doi.org/10.19045/bspab.2015.4300...
). Under certain conditions, this fungus dramatically reduces the stand and yield of crops, with losses that can be as high as 70% (Ali et al. 2011Ali, F., Rahman, H., Durrishahwar, Nawaz, I., Munir, M. and Ullah, H. (2011). Genetic analysis of maturity and morphological traits under Maydis Leaf Blight (MLB) epiphytotics in maize (Zea mays L.). Journal of Agricultural and Biological Science, 6, 1990-6145.; Hussain et al. 2016Hussain, H., Raziq, F., Khan, I., Shah, B., Altaf, M., Attaullah, Ullah, W., Naeem, A., Adnan, M., Junaid, K., Shah, S.R.A. and Iqbal, M. (2016). Effect of Bipolaris maydis (Y. Nisik & C. Miyake) shoemaker at various growth stages of different maize cultivars. Journal of Entomology and Zoology Studies, 4, 439-444.). The factors determining the magnitude of losses are the growth stage of the crop, the susceptible varieties, and the planting time (Ali et al. 2011Ali, F., Rahman, H., Durrishahwar, Nawaz, I., Munir, M. and Ullah, H. (2011). Genetic analysis of maturity and morphological traits under Maydis Leaf Blight (MLB) epiphytotics in maize (Zea mays L.). Journal of Agricultural and Biological Science, 6, 1990-6145.).

Several control measures are implemented to minimize the damage caused by spot blotches (NLB and SLB), e.g., the spraying of fungicides and the planting of resistant varieties. Furthermore, some practices can be adopted, such as crop rotation, the use of the adequate planting density and spacing, and the use of balanced fertilization and elimination of crop residues (Bergamin Filho and Amorim 2011Bergamin Filho, A. and Amorim, L. (2011). Manejo integrado de doenças. In L. Amorim, J. Á. M. Rezende and A. Bergamin Filho. (Eds.), Manual de Fitopatologia: Princípios e conceitos, 4. ed. (p. 409-419). São Paulo: Ceres.). The use of cultivars with genetic-resistance potential against the main popcorn diseases is the most viable and economic control measure (Ayiga-Aluba et al. 2015Ayiga-Aluba, J., Edema, R., Tusiime, G., Asea, G. and Gibson, P. (2015). Response to two cycles of S1 recurrent selection for turcicum leave blight in an open pollinated maize variety population (Longe 5). Advances in Applied Science Research, 6, 4-12.; Ferguson and Carson 2007Ferguson, L.M. and Carson, M.L. (2007). Temporal variation in Setosphaeria turcica between 1974 and 1994 and origin of races 1, 23, and 23N in the United States. Phytopathology, 97, 1501-1511. https://doi.org/10.1094/phyto-97-11-1501.
https://doi.org/10.1094/phyto-97-11-1501...
; Ishfaq et al. 2014Ishfaq, A., Dar, Z.A., Lone, A.A., Ali, G., Gazal, A., Hamid, B. and Mohiddin, F.A. (2014). Disease reaction studies of maize (Zea mays L.) against turcicum leaf blight involving indigenously identified cytosterile source. African Journal of Microbiology Research, 8, 2592-2597. https://doi.org/10.5897/ajmr2014.6708.
https://doi.org/10.5897/ajmr2014.6708...
; Vieira et al. 2009bVieira, R.A., Tessmann, D.J., Hata, F.T., Souto, E.R. and Mesquini, R.M. (2009b). Resistência de híbridos de milho-pipoca a Exserohilum turcicum, agente causal da helmintosporiose do milho. Scientia Agrária, 10, 391-395. https://doi.org/10.5380/rsa.v10i5.15196.
https://doi.org/10.5380/rsa.v10i5.15196...
). Associated with this method, the knowledge of the type of control as well as of the heritability of the traits involved in the expression of resistance are highly important in the development of resistant cultivars. This is because these data provide guidance for more efficient selection in subsequent works of breeding programs (Vieira et al. 2009aVieira, R.A., Tessmann, D.J., Scapim, C.A., Hata, F.T., Rodovalho, M.A. and Barreto, R.R. (2009a). Genetic resistance of new popcorn hybrids to foliar diseases. Crop Breeding and Applied Biotechnology, 9, 140-146. https://doi.org/10.12702/19847033.v09n02a06.
https://doi.org/10.12702/19847033.v09n02...
).

In this scenario, germplasm banks take on an indispensable importance in regard to the congregation of genetic variability, which is necessary especially to give basis to breeding programs of plants to obtain superior genotypes (Newton et al. 2011Newton, A.C., Akar, T., Baresel, J.P., Bebeli, P.J., Bettencourt, E., Bladenopoulos, K. V, Czembor, J.H., Fasoula, D.A., Katsiotis, A., Koutis, K., Koutsika-Sotiriou, M. Kovacs, G., Larsson, H., Pinheiro de Carvalho, M.A.A., Rubiales, D., Russell, J., Dos Santos, T.M.M. and Vaz Patto, M.C. (2011). Cereal landraces for sustainable agriculture. Agronomy for Sustainable Development. 2, 147-186. https://doi.org/10.1007/978-94-007-0394-0_10.
https://doi.org/10.1007/978-94-007-0394-...
; Quintal et al. 2012; Vivas et al. 2015Vivas, M., Silveira, S.F., Viana, A.P., Amaral Junior, A.T., Ferreguetti, G.A. and Pereira, M.G. (2015). Resistance to multiple foliar diseases in papaya genotypes in Brazil. Crop Protection, 71, 138-143. https://doi.org/10.1016/j.cropro.2015.02.007.
https://doi.org/10.1016/j.cropro.2015.02...
). UENF has a popcorn Germplasm Bank with accessions from different eco-geographic regions of Brazil and abroad, obtained from grants and exchanges, which have the potential to be investigated for resistance to diseases. This investigation should start with the identification of sources of resistance to leaf diseases in popcorn, as a result of the high losses caused by leaf pathogens and of the economic importance of the crop.

That said, in this study we investigated the performance of 37 popcorn genotypes with respect to fungal leaf diseases caused by E. turcicum and B. maydis and to select promising genotypes with genetic resistance to be used in future popcorn breeding programs, aiming to generate new resistant cultivars for farmers.

MATERIAL AND METHODS

Genetic material

Thirty-seven popcorn accessions from the Germplasm Bank were used (Table 1). Nine of them were crossbreeds originating from CIMMYT (ARZM-05083, ARZM-0749, ARZM-13050, BOYA-462, BOZM-260, CHZM-13134, PARA-172, URUG-298-Amarelo, and URUG-298-Roxo); one commercial hybrid (IAC-125); and 27 inbreed lines – six of the ‘Beija-Flor’ population (L51, L52, L53, L54, L55, and L59), six of the BRS-Angela population (L61, L63, L65, L66, L70, and L71); five of the ‘Viçosa’ population (L75, L76, L77, L80, and L88), three of the Zaeli hybrid (P5, P6, and P7), three of the IAC-112 hybrid (P8, P9, and P10), two of the CMS-42 compound (P2 and P3), one of the Zélia hybrid (P1), and one of South-American breeds (P4).

Table 1
Description of popcorn genotypes from the Germplasm Bank of the State University of Northern Rio de Janeiro.

Implementation of the experiment

Two experiments were implemented in the municipality of Campos dos Goytacazes, Rio de Janeiro, Brazil, during a 1st season (October 2013 to March 2014), with an average temperature of 26 °C, and a 2nd season (May to September 2014), with an average temperature of 22 °C.

The experiment was implanted as a randomized-block design with four replications, in both growing seasons. The experimental units consisted of simple 3.0 m row containing 16 plants each. The experimental field was prepared mechanically by harrowing followed by furrowing. Seeding was performed manually, with plants spaced 0.20 m apart and rows by 0.90 m. Cultivation practices included thinning the seedlings 15 days after emergence, weeding out, periodic irrigation maintaining the soil under field capacity, and topdressing applied 30 and 45 after emergence, using a 20-0-20 NPK formulation with 300 kg.ha-1 and 200 kg.ha-1 urea, respectively. The ears of each genotype were collected after visual observation of the moment when the bracts were dry, in each growing season, to prevent early or late harvests. The useful plot of the experiment consisted of six competitive plants, totaling 0.90 m2.

Evaluated traits

The performance of the genotypes concerning the leaf diseases was monitored by estimating the incidence and severity of the symptoms. To this end, two estimation methods were adopted:

  1. Measurement of incidence of the disease symptoms along the plant, expressed as a percentage;

  2. Quantification of severity symptoms along the first leaf below the first ear, expressed as a percentage.

Leaf diseases were manifested by a natural infection of the etiological agents on the field. Evaluations were performed by taking six competitive plants per plot, this is, only plants with correct spacing and in the center of the plot were evaluated.

The incidence of NLB and SLB symptoms based on the plant was estimated by using a diagrammatic scale adopted by Agroceres (1996)Agroceres (1996). Guia Agroceres de Sanidade. São Paulo: Agroceres.. The scale presents an interval of 1 through 9, in which 1 = 0 % incidence; 2 = 0.5% incidence; 3 = 10% incidence; 4 = 30% incidence; 5 = 50% incidence; 6 = 70% incidence; 7 = 80% incidence; 8 = 90% incidence; and 9 = 100% incidence. To evaluate the severity of NLB in the leaf, six competitive plants were used per plot, and the evaluations occurred every seven days from flowering to the senescence stage. Considering that only three evaluations were conducted, and that our goal was simply to compare genetic materials, we believe that the analysis based on the average of the evaluations better reflects the potential of the evaluated genotypes. For this variable, the diagrammatic scale proposed by Lazaroto et al. (2012)Lazaroto, A., Santos, I., Konflanz, V.A., Malagi, G. and Camochena, R.C. (2012). Escala diagramática para avaliação de severidade da helmintosporiose comum em milho. Ciência Rural, 42, 2131-2137. https://doi.org/10.1590/s0103-84782012005000112.
https://doi.org/10.1590/s0103-8478201200...
was adopted, containing the severity intervals in percentage corresponding to 0.5%, 1.0%, 2.5%, 6.5%, 15.5%, 30.0%, and 54.0%, based on which the percentage of the leaf area compromised by the disease was estimated. The scale proposed by James (1971)James, W.C. (1971). A manual of assessment keys for plants diseases. No. 1458. St. Paul: APS Press. was used to estimate the leaf severity of SLB, with severity intervals expressed by the following scale: 0%, 1%, 5%, 25%, and 50%.

Statistical analysis

The traits were statistically evaluated by analysis of variance, and when a significant difference was detected, Scott-Knott’s mean clustering algorithm was employed at the 5% probability level. Phenotypic (rp), genotypic (rg) and environmental (re) correlation coefficients were estimated, and the significance level was evaluated by the t test. In the estimate of genetic diversity, Generalized Mahalanobis Distance was used as a dissimilarity measure, and subsequently the accessions were grouped based on the UPGMA method, using, for this, the traits incidence and severity of SLB and NLB. The adjustment between the matrix of distances and the dendrogram was estimated by the cophenetic correlation coefficient (CCC), developed by Sokal and Rohlf (1962)Sokal, R.R. and Rohlf, F.J. (1962). The comparison of dendrograms by objective methods. Taxonomy, 11, 30-40. https://doi.org/10.2307/1217208.
https://doi.org/10.2307/1217208...
. All analyses were performed using the computer resources of Genes software (Cruz 2013Cruz, C.D. (2013). GENES - a software package for analysis in experimental statistics and quantitative genetics. Acta Scientiarum Agronnomy, 35, 271-276. https://doi.org/10.4025/actasciagron.v35i3.21251.
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).

RESULTS AND DISCUSSION

Resistance to Northern Leaf Blight (NLB)

There was a significant genotype effect for incidence of plants with symptoms in both growing seasons. Two groups were formed in the first, and four in the second growing season. Genotypes L71, L75, L76, P7, and PARA-172 were allocated in the group with highest resistance in both evaluated periods (Table 2).

Table 2
Average of three assessments in percentage of incidence and severity of the fungal leaf diseases northern leaf blight (NLB), caused by E. turcicum, in the first and second popcorn growing seasons.

For leaf severity, a significant effect of genotype was only observed in the second evaluation period. The means clustering tests also revealed the presence of more than one group in the second harvest (Table 2). Thirty-one genotypes were included in the group with the lowest means, with noteworthy values found for L71, L75, L76, P7, and PARA-172. In addition to these, L61, L66, P3, P8, ARZM-05083, BOYA-462, BOZM-260, URUG-298-Amarelo, URUG-298-Roxo, and IAC-125 were highlighted for showing values lower than 5% of their leaf area affected, considering the average between the first and second harvests (Table 2). P3, P7, and P8 are lines from the State University of Maringá (UEM); P3 was extracted from the CMS-42 compound of Embrapa Maize & Sorghum; P7, from the ‘Zaeli’ triple hybrid; and P8 from the IAC-112 hybrid (Silva et al. 2011Silva, V.Q.R., Amaral Júnior, A.T., Gonçalves, L.S.A., Freitas Júnior, S.P. and Ribeiro, R.M. (2011). Heterotic parameterizations of crosses between tropical and temperate lines of popcorn. Acta Scientiarum Agronomy, 33, 243-249. https://doi.org/10.4025/actasciagron.v33i2.9607.
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). The resistance of line P3 is possibly related to the fact that it originates from the genetically bred population CMS-42 (Pacheco et al. 1998Pacheco, C.A.P., Gama E.E.G., Guimarães, P.E.O., Santos, M.X. and Ferreira, A.S. (1998). Estimativas de parâmetros genéticos nas populações CMS-42 e CMS-43 de milho pipoca. Pesquisa Agropecuária Brasileira, 33, 1995-2001.). The line P7 may have its expression of resistance because its genealogy – Zaeli – holds alleles favorable to NLB, as stated by Vieira et al. (2009b)Vieira, R.A., Tessmann, D.J., Hata, F.T., Souto, E.R. and Mesquini, R.M. (2009b). Resistência de híbridos de milho-pipoca a Exserohilum turcicum, agente causal da helmintosporiose do milho. Scientia Agrária, 10, 391-395. https://doi.org/10.5380/rsa.v10i5.15196.
https://doi.org/10.5380/rsa.v10i5.15196...
. The P8 line probably showed good performance because it originated from hybrid IAC-112, which has recognized resistance to NLB (Vieira et al. 2009bVieira, R.A., Tessmann, D.J., Hata, F.T., Souto, E.R. and Mesquini, R.M. (2009b). Resistência de híbridos de milho-pipoca a Exserohilum turcicum, agente causal da helmintosporiose do milho. Scientia Agrária, 10, 391-395. https://doi.org/10.5380/rsa.v10i5.15196.
https://doi.org/10.5380/rsa.v10i5.15196...
).

Among genotypes developed by UENF that stood out — L61, L66, L71, L75, and L76 —, lines L61, L66, and L71 had good performance, likely because they originated from cultivar BRS Angela, developed by Embrapa Maize & Sorghum, after six cycles of intrapopulation recurrent selection (Pacheco et al. 2005Pacheco, C.A.P., Gama, E.E.G., Parentoni, S.N., Santos, M.X. and Guimarães, P.E.O. (2005). Avanços no processo seletivo da variedade de milho pipoca BRS Ângela. Revista Brasileira de Milho Sorgo, 4, 436-444. https://doi.org/10.18512/1980-6477/rbms.v4n3p436-444.
https://doi.org/10.18512/1980-6477/rbms....
). According to Bleicher and Balmer (1993)Bleicher, J. and Balmer, E. (1993). Efeitos da seleção recorrente fenotípica sobre a resistência a Exserohilum turcicum (Pass.) Leonarde & Suggs em milho. Pesquisa Agropecuária Brasileira, 28, 1291- 1295., recurrent selection is efficient to increase the level of resistance to NLB in susceptible corn cultivars, confirming the assertion of Parteniani and Miranda Filho (1978). Based on this premise, Kasozi et al. (2015)Kasozi, L.C., Derera, J. and Tongoona, P. (2015). Response of maize population “Longe5” to two cycles of modified S 1 recurrent selection for resistance to maize weevil. Euphytica, 204, 587-598. https://doi.org/10.1007/s10681-014-1341-8.
https://doi.org/10.1007/s10681-014-1341-...
observed that two S1 recurrent selection cycles were effective in improving the “Longe5” population for yield and resistance to the damage caused by the maize weevil and to the main corn diseases, among them NLB. These authors achieved a 29% increase in grain yield and 15% reduction of the NLB disease from C0 to C2, demonstrating the potential for improvement of these traits through recurrent selection. In an evaluation of the history of the NLB disease in seven cycles of recurrent selection, Ribeiro et al. (2016)Ribeiro, R.M., Amaral Júnior, A.T., Pena, G.F., Vivas, M., Kurosawa, R.N.F. and Gonçalves, L.S.A. (2016). History of northern corn leaf blight disease in the seventh cycle of recurrent selection of an UENF-14 popcorn population. Acta Scientiarum Agronomy, 38, 1-10. https://doi.org/10.4025/actasciagron.v38i4.30573.
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concluded that selection was effective in maintaining the equilibrium of the disease in the improved population of popcorn UENF-14 and that the source of resistance was not lost with the advance of the selection cycles. These authors also stated that it is possible to combine genes for resistance to NLB with the other agronomic traits of interest.

The superiority of lines L75 and L76 can be attributed to the fact that they originated from cultivar Viçosa, which was evaluated under natural conditions of NLB infestation by Miranda et al. (2003)Miranda, G.V., Coimbra, R.R., Godoy, C.L., Souza, L.V., Guimarães, L.J.M. and Melo, A.V. (2003). Potencial de melhoramento e divergência genética de cultivares de milho pipoca. Pesquisa Agropecuária Brasileira, 38, 681-688. https://doi.org/10.1590/s0100-204x2003000600003.
https://doi.org/10.1590/s0100-204x200300...
and was considered an expressive source of resistance. Nevertheless, Arnhold et al. (2008)Arnhold, E. (2008). Seleção para resistência a doenças foliares em famílias S1 de milho-pipoca. Revista Ceres, 55, 89-93. evaluated S1 progenies from Viçosa population for resistance to diseases and expression of agronomic features, and found superior resistance to NLB compared with the control IAC-112.

The breeds ARZM-05083, BOYA-462, BOZM-260, URUG-298-Amarelo, URUG-298-Roxo, and PARA-172 originate from CIMMYT, and genealogies or any expression of resistance to diseases for them are unknown. These accessions expressed similar resistance to that of commercial hybrid IAC-125, which is recognized for having moderate resistance to NLB (Cruz et al. 2014Cruz, J.C., Pereira Filho, I.A. and Queiroz, L.R. (2014). Milho -Cultivares para 2013/2014; [accessed 2016 Jan 16]. http://www.cnpms.embrapa.br/milho/cultivares/
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). Of these, PARA-172 stood four for showing an even superior resistance to that of hybrid IAC-125, which makes its use in breeding programs for introgression of resistance to NLB strategic.

Considering the performance of the genotypes in both growing seasons, lines L71, L75, L76, P7 and accession PARA-172 are considered superior.

Resistance to Southern Leaf Blight (SLB)

There was a significant effect of genotype in all evaluations performed, with three groups formed in the first harvest and four in the second, for incidence in the plant. Genotypes ARZM0-5083, ARZM-07049 and PARA-172 had the lowest estimates for incidence of SLB in both evaluation periods (Table 3). For severity of SLB in the leaf, there was a significant genotype effect only in the second growing season, with three and four groups formed for the first and second periods, respectively (Table 3). The genotypes that expressed the highest levels of resistance to SLB, in both growing seasons, were L61, L66, L70, L76, P2, P3, P4, P7, ARZM-05083, ARZM-07049, BOZM-260, PARA-172, URUG-298-Amarelo, and IAC-125 (Table 3).

Table 3
Average of three assessments in percentage of incidence and severity of the fungal leaf diseases southern leaf blight (SLB), caused by B. maydis, in the first and second popcorn growing seasons.

Lines L61, L66, and L70 are from recurrent selection (Pacheco et al. 2005Pacheco, C.A.P., Gama, E.E.G., Parentoni, S.N., Santos, M.X. and Guimarães, P.E.O. (2005). Avanços no processo seletivo da variedade de milho pipoca BRS Ângela. Revista Brasileira de Milho Sorgo, 4, 436-444. https://doi.org/10.18512/1980-6477/rbms.v4n3p436-444.
https://doi.org/10.18512/1980-6477/rbms....
), whereby it is concluded that the resistance shown was due to the combination of favorable alleles stemming from the implementation of recurrent selection. Of the accessions from UEM, the resistance of lines P2 and P3 is attributed to the fact that they are from the improved population originating from compound CMS-42 (Pacheco et al. 1998Pacheco, C.A.P., Gama E.E.G., Guimarães, P.E.O., Santos, M.X. and Ferreira, A.S. (1998). Estimativas de parâmetros genéticos nas populações CMS-42 e CMS-43 de milho pipoca. Pesquisa Agropecuária Brasileira, 33, 1995-2001.). The resistance observed in hybrid top cross IAC-125 was expected to occur, as described in the table provided by EMBRAPA about the behavior of corn cultivars available in the Brazilian market in the 2013/14 crop regarding the main diseases (Cruz et al. 2014Cruz, J.C., Pereira Filho, I.A. and Queiroz, L.R. (2014). Milho -Cultivares para 2013/2014; [accessed 2016 Jan 16]. http://www.cnpms.embrapa.br/milho/cultivares/
http://www.cnpms.embrapa.br/milho/cultiv...
).

The breeds from CIMMYT — ARZM-05083, ARZM-07049, BOZM-260, PARA-172 and URUG-298-Amarelo — have shown to be materials of interest for breeding aiming at resistance to diseases. These cases are genotypes from temperate countries, like Argentina (ARZM-05083, ARZM-07049), Paraguay (PARA-172), and Uruguay (URU-298-Amarelo) and tropical country like Bolivia (BOZM-260). These findings indicate these genotypes can be recommended in crosses with plants that have desirable agronomic traits, given the expansion of the genetic basis of popcorn accessions and the development of new cultivars. In addition, the selection could be applied within some accession, in order to achieve improved lines for explore hybrids, for instance Silva et al. (2015)Silva, T. A., Cantagalli, L.B., Saavedra, J., Lopes, A.D., Mangolin, C.A., Machado, M.F.P.S. and Scapim, C.A. (2015). Population structure and genetic diversity of Brazilian popcorn germplasm inferred by microsatellite markers. Electronic Journal of Biotechnology. 18, 181-187. https://doi.org/10.1016/j.ejbt.2015.03.005.
https://doi.org/10.1016/j.ejbt.2015.03.0...
evaluated the genetic divergence among and within accessions of popcorn and found that accession BOZM-260 showed the highest proportion of heterozygous plants among the evaluated accessions and also exhibited allelic variation in all microsatellite loci analyzed. These authors also found that ARZM-05083 was genetically distant from the other genotypes assessed, which corroborates the strategy of use of popcorn germplasm from temperate climates to broaden the genetic base of breeding programs.

Considering the accessions performance in both growing seasons, for both incidence and severity, three accession can be indicated as the highest sources of resistance to SLB: breeds ARZM-05083, ARZM-07049, and PARA-172, all originating from CIMMYT. Special emphasis should be placed on genotype PARA-172, which expressed the highest degree of resistance for both NLB and SLB (Table 3), thus showing to be an excellent alternative in crosses aiming at resistance to popcorn leaf diseases or for the extraction of lines for the generation of superior hybrids. With this goal, UENF’s Popcorn Breeding Program has acted intensely in the development of lines from superior germplasms; nine S6 descendants of PARA-172 are already under growth in the field for the generation of individuals from the next inbred generation.

Cluster analysis

There was a good fit in the graphic representation of the clustering distances, since the cophenetic correlation coefficients (CCC) were 0.87 for the first and 0.78 for the second growing season. For the first harvest, the genotypes were gathered in three larger groups (Figure 1a), one of which was formed by lines L51 and L52, that were the most susceptible to the two diseases evaluated here (Tables 2 and 3). The second group included 18 of the 35 remaining genotypes. A subgroup was formed in this group, consisting of L59, P8, L88, IAC-125, P10, P3, P7, P9, and PARA-172, which were the genotypes most resistant to both diseases (Tables 2 and 3). The third group contained 17 accessions, and except for P2 and L71, which showed resistance to NLB and SLB in the first harvest, the others were moderately resistant to the action of the fungus Bipolaris maydis.

Figure 1
Dendrograms of 37 genotypes of popcorn by the UPGMA method using Generalized Mahalanobis Distance as a measure of genetic dissimilarity, for both growing seasons. (a) Growing season from October 2013 to March 2014 and (b) Growing season from May to September 2014.

Four groups were formed for the second harvest (Figure 1b); the first included the genotypes of highest susceptibility – L53, L54, L80, L52, and CHZN-13134, whilst the second group allocated lines L55 and L65, which were susceptible to NLB in the second harvest and moderately resistant to NLB and SLB in the second harvest. It is thus unquestionable that these reactions facilitated the agglutination of these genotypes in the same group for both growing seasons. The third group contained 23 accessions, which were moderately resistant to NLB and SLB, except for the subgroup formed by lines P5, P1, L77, L51, and L59, which were all moderately resistant to NLB and susceptible to SLB. In the second group, a subgroup was formed containing accessions PARA-172, ARZM-05083, and ARZM-07049, which stood out for having consistently the highest levels of resistance to SLB in the second growing season, especially PARA-172, which revealed the highest estimates for severity to both diseases in the second growing season (Table 3). In this way, these are populations with high potential to be used as sources of resistance. Moreover, the consistent variability present between these populations — confirmed by the high genetic diversity estimates as estimated by ISSR markers (Amaral Júnior et al. 2011Amaral Junior, A.T., Oliveira, E.C., Gonsalves, L.S.A., Scapim, C.A., Candido, L.S., Silva, T.R.C., Vitorazzi, C. and Cunha, K.S. (2011). Assessment of genetic diversity among maize accessions using inter simple sequence repeats (ISSR) markers. African Journal of Biotechnology, 10, 15462-15469. https://doi.org/10.5897/ajb10.2624.
https://doi.org/10.5897/ajb10.2624...
) — make them even more interesting for the production of superior segregants.

The efficiency of the UPGMA clustering method is thus proven in the discrimination of reaction to NLB and SLB. As such, it is an interesting multivariate statistical alternative in the indication of genotypes for breeding programs aimed at the introgression of genes providing resistance to NLB and SLB in segregating populations, or even to obtain superior hybrids.

Estimates of correlations

Elevated estimates for phenotypic and genotypes correlations were detected for incidence and severity of NLB in both growing seasons, similarly to what occurred for incidence and severity of SLB (Table 4). The magnitude of genetic correlations were superior to the phenotypic correlations, evidencing a strong correspondence of selection based on the phenotype with the genetic effects between incidence and severity. Thus, only one of the two traits would already be sufficient for the selection of resistant genotypes and, in this aspect, because of the greater practicality, it is recommended to use the incidence traits as the main variable in experiments conducted in the field, under natural inoculation conditions. Under controlled inoculation conditions, however, it is suggested to use severity as a criterion of selection. This is because in experiments undertaken in greenhouses, the distribution of diseases is dependent upon the inoculation being performed; on the other hand, for experiments in the field, the disease is typically distributed more evenly. Furthermore, incidence is a more practical variable to be evaluated.

Table 4
Estimates of correlations among incidence of NLB in the plant (ETP), severity of NLB in the leaf (ETF), incidence of SLB in the plant (BMP), and severity of SLB in the leaf (BMF) for two popcorn growing seasons.

In turn, were observed genetic, phenotypic and environmental correlation estimates varying of low to high magnitude for incidence and severity of NLB and SLB, depending on the pair of traits assessed and the season in which this evaluation took place (Table 4). Therefore, there is no direct relationship between traits that provide resistance to these diseases. These results are probably because the mechanisms of resistance to these diseases have distinct origins. According to Chang and Peterson (1995)Chang, R. and Peterson, P.A. (1995). Genetic control of resistance to Bipolaris maydis: one gene or two genes?. Journal of Heredity, 86, 94-97. https://doi.org/10.1093/oxfordjournals.jhered.a111555.
https://doi.org/10.1093/oxfordjournals.j...
, Bipolaris maydis is controlled by two recessive genes in corn, in which the dominant gene provides susceptibility to SLB. On the other hand, for E. turcicum, the genetic control of NLB can be achieved by quantitative resistance (by using several genes of small effects) or even by qualitative resistance (from few genes of high effect in reducing the intensity of the disease) (Vieira et al. 2009bVieira, R.A., Tessmann, D.J., Hata, F.T., Souto, E.R. and Mesquini, R.M. (2009b). Resistência de híbridos de milho-pipoca a Exserohilum turcicum, agente causal da helmintosporiose do milho. Scientia Agrária, 10, 391-395. https://doi.org/10.5380/rsa.v10i5.15196.
https://doi.org/10.5380/rsa.v10i5.15196...
). Ogliari et al. (2005)Ogliari, J.B., Guimarães, M.A., Geraldi, I.O. and Camargo, L.E.A. (2005). New resistance genes in the Zea mays. Exserohilum turcicum pathosystem. Genetic and Molecular Biology, 28, 435-439. https://doi.org/10.1590/s1415-47572005000300017.
https://doi.org/10.1590/s1415-4757200500...
emphasize that these two types of mechanisms of resistance to E. turcicum may work separately or together, suggesting the existence of different mechanisms providing resistance to NLB and SLB, which will require greater accuracy in the development of breeding programs when aiming at the combination of these diseases in progenies under selection.

CONCLUSION

A good source of resistance was found to NLB through accessions L71, L75, L76, P7 and PARA-172, which can thus be considered remarkable sources of resistance. For resistance to SLB, the superior accessions that can be indicated as sources of resistance are ARZM-05083, ARZM-07049, and PARA-172. Thus, with respect to leaf fungal diseases caused by E. turcicum and B. maydis, promising genotypes with genetic resistance may be used in future crosses in popcorn breeding programs, in order to generate new resistant cultivars for farmers.

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Publication Dates

  • Publication in this collection
    18 Dec 2017
  • Date of issue
    Jan-Mar 2018

History

  • Received
    01 Feb 2017
  • Accepted
    10 Apr 2017
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