Potential of popcorn germplasm as a source of resistance to ear rot

ABSTRACT

Because of its multi-purpose nature, popcorn has sparked the interest of the World Trade Organization as regards fungal contamination by mycotoxins. However, no investigations have been conducted on popcorn for resistance of genotypes to ear rot. The aim of this study was to evaluate the potential of popcorn genotypes as to resistance to ear rot and rotten kernels, as an initial step for the implementation of a breeding program with the popcorn crop in Northern Rio de Janeiro State, Brazil. Thirty-seven accessions from different ecogeographic regions of Latin America were evaluated in 2 cultivation periods, in a randomized block design with 4 replications. We evaluated the incidence of rotten ears, incidence of rotten ears caused by Fusarium spp., severity of ears with Fusarium spp. rot, and incidence of rotten kernels. The results were subjected to analysis of variance, and means were compared by the Scott-Knott clustering test (p < 0.05). A significant effect was observed for all evaluated variables, characterizing them as efficient in the discrimination of genotypic variability for reaction to fungal injuries in popcorn. The gene pool of the tropical and temperate Germplasm Collection evaluated here has the potential to generate superior segregants and provide hybrid combinations with alleles of resistance to diseases affecting ears and stored kernels. Based on the different variables and times, the experiment was conducted, and genotypes L65, L80, and IAC 125 showed the highest levels of resistance.

Key words
Zea mays; Fusarium spp.; genetic resistance

INTRODUCTION

Mycotoxins are products of the secondary metabolism of fungi that can affect one’s health when ingested, inhaled, or in simple contact with the skin. Mycotoxins can appear in food primarily by fungal infection of crops from agricultural productions, being directly absorbed by men, or indirectly, when contaminated diets are supplied to animals in whom mycotoxins can accumulate in different organs or tissues and enter the human diet through consumption of meat, milk, and eggs (Marin et al. 2013). In the Italian market, for instance, the presence of mycotoxins was detected in baby foods in at least 31% of cereal-based nutrients, and 27% of contaminated samples showed simultaneous occurrence of different mycotoxins. The mycotoxin levels found reveal a situation that puts at risk the health of vulnerable populations, as is the case of the infant group (Juan et al. 2014). A study in Northern Nigeria investigated the occurrence of mycotoxins in urine samples of 120 farmers of the region, most of whom depended on corn, sorghum, peanut, and millet growing. Of the studied samples, 50.8% showed contamination by mycotoxins (Ezekiel et al. 2014).

In general, questions about food safety are complex, requiring more than 1 control measure to effectively overcome the risk posed to health, which includes actions involving the different steps of the food production chain (Pitt et al. 2013). In the agricultural production scenario, the occurrence of damaged, namely rotten kernels, is a consequence of ear rots in corn, which is always related to the presence of mycotoxins, caused by fungi of the genus Fusarium spp. in batches of grains stored either for human consumption or to be used as a component in the formulation of animal diets (Juliatti et al. 2007). Besides the hazard of contamination by mycotoxins, the effects of fungal development markedly reduce grain yield and the quality of the end product (Mendes et al. 2012). Moreover, fungi of the genus Fusarium spp. have caused serious damage to cereal production, resulting in reductions of 10 to 40% (Bottalico and Perrone 2002; Linkmeyer et al. 2016). Nevertheless, the quantification of economic losses in popcorn production remains unknown.

Only in the last decade, studies about the control of diseases in popcorn have become a concern to breeders (Arnhold 2008; Vieira et al. 2011; Sanches et al. 2011; Vieira et al. 2012; Noor et al. 2015; Vieira et al. 2016). To complicate matters, no research has been developed on resistance to ear rot in popcorn. In this regard, the evaluation of germplasm banks is of great importance during pre-breeding, mainly to support breeding programs in the identification of sources of resistance genes (Sanches et al. 2011; Resh et al. 2015; Vivas et al. 2015).

Corn has a great genetic importance worldwide held in genetic reservoirs, such that there is no shortage of favorable alleles in germplasm banks capable of contributing, among other aspects, with resistance to diseases, tolerance to abiotic stresses, greater productivity, and better nutritional quality (Prasanna 2012). The institution of development of this study has a popcorn germplasm bank with accessions from different eco-geographic regions that have been made available for research focused on resistance to diseases. This collection contains germplasm from Brazil and abroad ― Latin America, Mexico, and USA ― obtained from grants and exchanges.

Given the impacts of mycotoxins, along with the scarcity of investigations on resistance to ear rot in popcorn, the present study was developed to evaluate the performance of genotypes from the Germplasm Collection concerning ear rot by quantifying the incidence and severity of symptoms and the percentage of rotten kernels resulting from susceptibility to infection by Fusarium spp.

MATERIAL AND METHODS

Genotypes

Thirty-seven accessions of popcorn from the Germplasm Bank were used to evaluate their reaction to Fusarium ear rot (Table 1).

Table 1
Description of popcorn genotypes from the Germplasm Bank.

Genotype		Type		Originating variety		Climatic adaptation		Institution of development
L 88		Line S7		Viçosa: UFV		Temperate/Tropical		UENF
L 70		Line S7		Ângela: Embrapa		Tropical		UENF
L 65		Line S7		Ângela: Embrapa		Tropical		UENF
L 80		Line S7		Viçosa: UFV		Temperate/Tropical		UENF
L51		Line S7		Beija-flor: UFV		Temperate/Tropical		UENF
L 77		Line S7		Viçosa: UFV		Temperate/Tropical		UENF
L 76		Line S7		Beija-flor: UFV		Temperate/Tropical		UENF
L 75		Line S7		Viçosa: UFV		Temperate/Tropical		UENF
L 66		Line S7		Ângela: Embrapa		Tropical		UENF
L 53		Line S7		Beija-flor: UFV		Temperate/Tropical		UENF
L 52		Line S7		Beija-flor: UFV		Temperate/Tropical		UENF
L 55		Line S7		Beija-flor: UFV		Temperate/Tropical		UENF
L 54		Line S7		Beija-flor: UFV		Temperate/Tropical		UENF
L 61		Line S7		Ângela: Embrapa		Tropical		UENF
L63		Line S7		Ângela: Embrapa		Tropical		UENF
L 59		Line S7		Beija-flor: UFV		Temperate/Tropical		UENF
L 71		Line S7		Ângela: Embrapa		Tropical		UENF
P1		Line		Hybrid Zélia		Temperate/Tropical		UEM
P2		Line		Compound CMS-42		Temperate/Tropical		UEM
P3		Line		Compound CMS-42		Temperate/Tropical		UEM
P4		Line		South-American varieties		Temperate/Tropical		UEM
P5		Line		Hybrid Zaeli		Temperate/Tropical		UEM
P6		Line		Hybrid Zaeli		Temperate/Tropical		UEM
P7		Line		Hybrid Zaeli		Temperate/Tropical		UEM
P8		Line		Hybrid IAC112		Temperate/Tropical		UEM
P9		Line		Hybrid IAC112		Temperate/Tropical		UEM
P10		Line		Hybrid IAC112		Temperate/Tropical		UEM
BOYA 462		Variety		Unknown		Temperate/Tropical		CIMMYT
URUG 298 Roxo		Variety		Unknown		Temperate/Tropical		CIMMYT
URUG 298 Amarelo		Variety		Unknown		Temperate/Tropical		CIMMYT
BOZM 260		Variety		Unknown		Temperate/Tropical		CIMMYT
ARZM 07049		Variety		Unknown		Temperate/Tropical		CIMMYT
CHZM 13134		Variety		Unknown		Temperate/Tropical		CIMMYT
ARZM 13050		Variety		Unknown		Temperate/Tropical		CIMMYT
ARZM 05083		Variety		Unknown		Temperate/Tropical		CIMMYT
PARA 172		Variety		Unknown		Temperate/Tropical		CIMMYT
IAC 125		Triple hybrid		Unknown		Temperate/Tropical		IAC

• UENF = Northern Fluminense State University “Darcy Ribeiro”; UEM = Maringá State University; CIMMYT = International Maize and Wheat Improvement Center; IAC = Agronomic Institute of Campinas.

Implementation of the experiment

The experiment was implemented in Campos dos Goytacazes, Northern Rio de Janeiro State, Brazil, in the first harvest (October 2013 to March 2014), when the average temperature was 26 °C, and in the second harvest (May to September 2014), with an average temperature of 22 °C.

A randomized block design with 4 replications was adopted in the 2 harvests. Experimental units consisted of simple 3.0 m rows containing 16 plants per row. The experimental field was prepared mechanically by harrowing followed by furrowing. Seeding was performed manually, with 0.2 m spacing between plants and 0.9 m between rows. Cultivation practices included seedling thinning 15 days after emergence, control of weeds by hoeing, periodic irrigation with maintenance of soil at field capacity, and topdressing performed 30 and 45 days after emergence using a 20-0-20 NPK formulation with 300 and 200 kg∙ha⁻¹ urea, respectively.

The ears of each genotype were harvested by visually observing when the bracts were dry, at each cultivation period, to prevent early or late harvesting.

Evaluated traits

Incidence of rotten kernels (IRK): after the ears were threshed, two 100-kernel samples were counted and represented the portions of work. The incidence of rotten kernels was expressed in percentage, determined according to the criteria for classification of corn established by Ordinance no. 11 from the Brazilian Ministry of Agriculture, Livestock and Food Supply, of April 12, 1996. The method consists of the visual segregation of symptomatic kernels showing discoloration in over ¼ of their total surface.

Incidence of rotten ears (IRE): determined adopting the total number of ears obtained from the harvest of each experimental unit. Ears infected at more than 50% by the action of ear-rot fungi were counted, and the incidence of rotten ears was the result of the division between the number of rotten ears and the total number of ears harvested per plot on the field, with values expressed in percentage.

Severity of ear rot caused by Fusarium spp. (SRF): the diagrammatic scale for ear rot caused by Fusarium spp. proposed by the International Maize and Wheat Improvement Center (CIMMYT 1985) was adopted, with values of 0, 10, 20, 30, and 40%, according to the rot severity level.

Incidence of ears damaged by Fusarium spp. (IDF): after the characteristic symptom of the disease was detected, all symptomatic ears infected by Fusarium spp. were counted. The incidence was obtained in percentage, as the division between the number of symptomatic ears and the total number of ears harvested per plot on the field, with values expressed in percentage.

Statistical analysis

Data were subjected to analysis of variance, and, when a significant difference was detected, the Scott-Knott means-clustering algorithm was used (p < 0.05). All analyses were performed using the computer resources of Genes software (Cruz 2013).

RESULTS AND DISCUSSION

There was a significant effect of the sources of variation genotype and time for the group of evaluated traits (data not shown), revealing the existence of genotypes with contrasting responses, among the evaluated accessions. This is of fundamental importance for applied breeding, from the perspective of potentiation of variability for the generation of superior segregants, or even for studies of heritability. These results also suggest that the 2 planting times were distinct enough to cause differences between the evaluated traits. The source of variation genotype versus time interaction revealed a significant effect on IDF, SRF, and IRK, whereby we concluded that the genotypes have different performances, determining the use of estimates of means based on each cultivation time.

On the other hand, for the trait incidence of rotten ears (IRE), no significant genotype versus time interaction effect was detected; consequently, the clustering of genotypes was presented and discussed with respect to means between harvests, since the cultivation time does not change the performance of genotypes. For this trait, by clustering the means, 2 groups were formed (Figure 1). The group of resistant genotypes included 83.78% of the studied accessions; of those from the Northern Fluminense State University “Darcy Ribeiro” (UENF), the following lines stood out: L53, L54, L59, L61, L63, L65, L66, L70, L71, L76, L77, and L80; and among those from the Maringá State University (UEM), lines P1, P2, P3, P4, P5, P6, P7, P9, and P10 were notable. For the accessions from the CIMMYT, varieties ARZM 05083, ARZM 07049, ARZM 13050, BOYA 462, BOZM 260, CHZM 13134, PARA 172, URUG 298 Amarelo, and URUG 298 Roxo manifested resistance to ear rot, as well as hybrid IAC 125, originating from the Agronomic Institute of Campinas (IAC; Figure 1).

Figure 1
Incidence of rotten ears estimated in 37 popcorn genotypes evaluated in the first (2013/2014) and second (2014) harvests.

The means-clustering test for IDF performed for the conditions of the first harvest formed 4 groups (Table 2).

Table 2
Incidence of ears damaged by Fusarium spp. and severity of ear rot caused by Fusarium spp. in 37 popcorn genotypes evaluated in the first (2013/2014) and second (2014) crops.

Genotype	IDF					SRF
		1st harvest		2nd harvest		1st harvest		2nd harvest
L51		100.00a*		50.11a		71.00a		79.54a
L52		90.48a		35.72b		89.33a		59.17a
L53		87.20a		19.97c		91.67a		43.75b
L54		65.21b		17.86c		88.58a		59.17a
L55		95.83a		11.31c		100.00a		43.75b
L59		89.59a		12.73c		93.23a		58.33a
L61		70.00b		9.82c		80.00a		70.00a
L63		37.34c		18.02c		67.50a		28.75b
L65		20.96d		9.90c		47.50b		26.25b
L66		46.49c		8.85c		67.69a		33.33b
L70		25.64d		9.98c		75.63a		59.75a
L71		37.91c		3.57c		48.54b		25.00b
L75		83.33a		49.11a		100.00a		72.92a
L76		59.66b		13.19c		60.83b		56.88a
L77		43.33c		14.92c		49.59b		24.38b
L80		11.82d		3.57c		40.00b		25.00b
L88		97.50a		67.31a		69.03a		63.61a
P1		70.83b		18.13c		97.29a		23.50b
P2		69.36b		25.54c		72.71a		64.96a
P3		42.55c		14.26c		76.15a		48.33b
P4		52.58c		14.38c		67.29a		69.58a
P5		64.76b		24.04c		66.74a		64.21a
P6		51.94c		20.14c		37.68b		55.79a
P7		57.55b		14.14c		75.00a		62.71a
P8		35.60c		25.99c		54.44b		65.94a
P9		44.16c		14.77c		57.06b		82.29a
P10		60.57b		24.13c		71.97a		78.33a
ARZM 05083		42.64c		6.89c		67.50a		41.25b
ARZM 07049		46.29c		23.82c		63.67a		84.32a
ARZM 13050		73.76b		31.95b		75.58a		49.50b
BOYA 462		40.63c		15.57c		17.32b		78.75a
BOZM 260		36.26c		4.85c		72.17a		66.25a
CHZM 13134		41.39c		24.59c		88.33a		72.92a
PARA 172		19.71d		13.46c		43.75b		71.46a
URUG298 Amarelo		31.41d		17.64c		43.39b		57.08a
URUG 298 Roxo		20.06d		4.55c		86.17a		13.13b
IAC 125		31.92d		16.01c		53.19b		44.92b

• ^*
  Means followed by common letters represent a statistically homogeneous group by the Scott-Knott algorithm. IDF = Incidence of ears damaged by Fusarium spp.; SRF = Severity of ear rot caused by Fusarium spp.

The group of genotypes resistant to the occurrence of the disease was composed of 18.92% of the studied accessions, namely L80, L65, L70, from UENF; varieties PARA 172, URUG 298, Amarelo, and URUG 298 Roxo, from CIMMYT; and, lastly, hybrid IAC 125 (Table 2). There were no resistant genotypes in this harvest originating from UEM. For the second harvest, the means-clustering test formed 3 groups. The group of most resistant genotypes corresponded to 86.48% of the evaluated accessions: L53, L54, L55, L59, L61, L63, L65, L66, L70, L71, L76, L77, and L80. For this second harvest, all accessions from UEM showed resistance to incidence of Fusarium spp. As for the accessions originating from CIMMYT, varieties ARZM 05083, ARZM 07049, BOYA 462, BOZM 260, CHZM 13134, PARA 172, URUG 298 Amarelo, and URUG 298 Roxo stood out. Triple hybrid IAC 125 also manifested resistance.

Concerning SRF, for the first harvest, 2 statistically distinct groups were formed regarding severity of Fusarium ear rot. The group of resistant genotypes included 32.43% of the studied accessions, and variations between resistant and susceptible accessions reached 82.68% between genotypes BOYA 462 and L55, respectively (Table 2). For the second harvest, the means test generated statistically distinct groups, among which the group of most resistant genotypes comprised 37.84% of the studied accessions that responded positively to severity of Fusarium spp. The most significant variation between resistant and susceptible genotypes reached the magnitude of 71.19% (Table 2).

For a reliable indication of promising genotypes in terms of resistance to ear rots, especially those caused by Fusarium spp, it is necessary to study the set of factors influencing the occurrence and severity of post-harvest diseases. Thus, considering the 3 variables simultaneously and the cultivation times, it was found that lines L65, L80 and triple hybrid IAC 125 possess favorable alleles for traits that provide resistance to ear rots, such as those caused by fungi of the genus Fusarium spp. Pacheco et al. (2005), evaluating cycles of selection of BRS Angela, observed that, up to selection cycle VI, variety BRS Angela showed higher levels of ear health when compared with controls IAC 112 and Zélia. This fact may indicate congregation of favorable alleles for resistance to ear diseases for lines extracted from the genetically improved cultivar BRS Angela, as is the case of line L65. Inferring about the potential of popcorn cultivars, Miranda et al. (2003) evaluated variety Viçosa for agronomic traits, and, for percentage of diseased ears, this cultivar showed an average resistance of 20% in relation to the others investigated in the range of 10% to 30%. Regarding triple commercial hybrid IAC 125, the estimates for ear health are possibly linked to the good performance per se of the genotype.

For the trait IRK, 3 groups were formed in the first harvest, whereas there was no statistical difference between the genotypes for the second cultivation period (Table 3).

Table 3
Incidence of rotten kernels in in 37 popcorn genotypes evaluated in the first (2013/2014) and second (2014) harvests.

Genotype	Incidence of rotten kernels
		1st harvest		2nd harvest
L51		69.500a*		13.375a
L52		50.833a		6.000a
L53		44.375b		3.000a
L54		23.125c		2.500a
L55		65.655a		3.750a
L59		41.750b		3.000a
L61		19.250c		0.500a
L63		12.750c		1.375a
L65		10.750c		1.250a
L66		24.375c		1.750a
L70		15.750c		0.375a
L71		29.375c		0.625a
L75		56.168a		8.125a
L76		40.500b		1.500a
L77		14.875c		1.125a
L80		23.125c		0.375a
L88		57.500a		3.625a
P1		37875b		4.500a
P2		24.000c		2.875a
P3		19.125c		0.000a
P4		8.625c		1.250a
P5		24.875c		1.375a
P6		10.375c		1.250a
P7		23.125c		2.125a
P8		8.750c		3.500a
P9		10.375c		0.250a
P10		18.875c		2.875a
ARZM 05083		9.875c		0.750a
ARZM 07049		12.625c		2.875a
ARZM 13050		27.375c		2.375a
BOYA 462		36.500b		0.125a
BOZM 260		12.875c		0.000a
CHZM 13134		35.250b		0.750a
PARA 172		6.500c		0.250a
URUG 298 Amarelo		9.750c		2.875a
URUG 298 Roxo		21.375c		0.500a
IAC 125		12.250c		2.750a

• ^*
  Means followed by common letters represent a statistically homogeneous group by the Scott-Knott algorithm.

That being said, the factor cultivation time significantly changed the rates of contamination of in rotten kernels, making the season effect remarkable. The first harvest, in general, favored the occurrence of rotten kernels for all studied genotypes and, therefore, all accessions evaluated showed values above the maximum tolerated limits for commercial classification, according to Normative Instruction no. 61 of the Brazilian Ministry of Agriculture, Livestock, and Supply (MAPA) of December 22, 2011. The second harvest significantly favored the health quality of the kernels, at a magnitude of 54.05% of the genotypes evaluated when compared with the first harvest. However, the values fitting the maximum commercial tolerance limits established by MAPA in 2011 do not necessarily apply to all genotypes that showed significant reductions of rotten kernels between the first and second harvests. For instance, lines L51, L52, and L75 showed significant reductions in the rotten-kernel incidence between periods; however, their lowest incidence values did not meet the minimum tolerance requirements established. However, at the second harvest, 54.05% of genotypes fitted type 01, with variations of 0% to 1.75% of rotten kernels; 21.62% fitted type 02, with variations of 2.12% to 2.87% of rotten kernels; and 16.21% of genotypes fitted group 03, with variations of 3% to 4.5% of rotten kernels (Table 3). It is known that the rotten kernels are a reflection of ear rots, caused mainly by fungi, still on the field. Initially, it was found that genotypes L65, L80, and IAC 125, which best stood out against ear rots, were also present in the group of genotypes most resistant to the incidence of kernel rot, and are thus promising to be used in breeding programs.

CONCLUSION

The adopted variables were efficient in detecting the existing variability for severity of Fusarium spp., allowing a reliable discrimination of superior accessions.

Genotypes L65, L80, and IAC 125 displayed the highest levels of resistance to incidence and severity of rot caused by Fusarim spp. and can thus be considered of interest for the introgression of resistance genes in popcorn breeding programs.

REFERENCES

• Arnhold, E. (2008). Seleção para resistência a doenças foliares em famílias S₁ de milho pipoca. Revista Ceres, 55, 89-93.
• Bottalico, A. and Perrone, G. (2002). Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. European Journal of Plant Pathology, 108, 611-624. http://dx.doi.org/10.1023/A:1020635214971
  » http://dx.doi.org/10.1023/A:1020635214971
• Centro Internacional de Mejoramiento de Maíz y Trigo (1985). Managing trials and reporting data for CIMMYT’s international: maize testing program. México: CIMMYT.
• Cruz, C. D. (2013). GENES - a software package for analysis in experimental statistics and quantitative genetics. Acta Scientiarum. Agronomy, 35, 271-276. http://dx.doi.org/10.4025/actasciagron.v35i3.21251
  » http://dx.doi.org/10.4025/actasciagron.v35i3.21251
• Ezekiel, C. N., Warth, B., Ogara, I. M., Abia, W. A., Ezekiel, V. C., Atehnkeng, J., Sulyok, M., Turner, P. C., Tayo, G. O., Krska, R. and Bandyopadhyay, R. (2014). Mycotoxin exposure in rural residents in northern Nigeria: A pilot study using multi-urinary biomarkers. Environment International, 66, 138-145. http://dx.doi.org/10.1016/j.envint.2014.02.003
  » http://dx.doi.org/10.1016/j.envint.2014.02.003
• Juan, C., Raiola, A., Mañes, J. and Ritieni, A. (2014). Presence of mycotoxin in commercial infant formulas and baby foods from Italian market. Food Control, 39, 227-236. http://dx.doi.org/doi:10.1016/j.foodcont.2013.10.036
  » http://dx.doi.org/doi:10.1016/j.foodcont.2013.10.036
• Juliatti, F. C., Zuza, J. L. M. F., Souza, P. P. and Polizel, A. C. (2007). Efeito do genótipo de milho e da aplicação foliar de fungicidas na incidência de grãos ardidos. Bioscience Journal, 23, 34-41.
• Linkmeyer, A., Hofer, K., Rychlik, M., Herz, M., Hausladen, H., Hückelhoven, R. and Hess, M. L. (2016). Influence of inoculum and climatic factors on the severity of Fusarium head blight in German spring and winter barley. Food Additives & Contaminants: Part A, 33, 489-499. http://dx.doi.org/10.1080/19440049.2015.1133932
  » http://dx.doi.org/10.1080/19440049.2015.1133932
• Marin, S., Ramos, A. J., Cano-Sancho, G. and Sanchis, V. (2013). Mycotoxins: Occurrence, toxicology, and exposure assessment. Food and Chemical Toxicology, 60, 218-237. http://dx.doi.org/10.1016/j.fct.2013.07.047
  » http://dx.doi.org/10.1016/j.fct.2013.07.047
• Mendes, M. C., Pinho, R. G. V., Pinho, E. V. R. V. and Faria, M. V. (2012). Comportamento de híbridos de milho inoculados com os fungos causadores do complexo grãos ardidos e associação com parâmetros químicos e bioquímicos. Ambiência, 8, 275-292. http://dx.doi.org/10.5777/ambiencia.2012.02.04
  » http://dx.doi.org/10.5777/ambiencia.2012.02.04
• 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. http://dx.doi.org/10.1590/S0100-204X2003000600003
  » http://dx.doi.org/10.1590/S0100-204X2003000600003
• Noor, M., Rahman, H. and Iqbal, M, (2015). Evaluation of Popcorn inbred lines for disease severity. Pure and Applied Biology, 4, 288-295.
• Pacheco, 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 e Sorgo, 4, 436-444.
• Pitt, J. I., Taniwaki, M. H. and Cole, M. B. (2013). Mycotoxin production in major crops as influenced by growing, harvesting, storage and processing, with emphasis on the achievement of Food Safety Objectives. Food Control, 32, 205-215. http://dx.doi.org/10.1016/j.foodcont.2012.11.023
  » http://dx.doi.org/10.1016/j.foodcont.2012.11.023
• Prasanna, B. M. (2012). Diversity in global maize germplasm: Characterization and utilization. Journal of Biosciences, 37, 843-855. http://dx.doi.org/10.1007/s12038-012-9227-1
  » http://dx.doi.org/10.1007/s12038-012-9227-1
• Resh, F. S., Scapim, C. A., Machado, M. F. P. S., Mangolin, C. A., Amaral Junior, A. T., Ramos, H. C. C. and Vivas, M. (2015). Genetic diversity of popcorn genotypes using molecular analysis. Genetics and Molecular Research, 14: 9829-9840. http://dx.doi.org/10.4238/2015.August.19.16
  » http://dx.doi.org/10.4238/2015.August.19.16
• Sanches, R. E., Scapim, C. A., Tessmann, D. J., Vieira, R. A., Rodovalho, M. A. and Milani, K. F. (2011). Genetic analysis of tropical rust resistance in popcorn lines. Ciência Rural, 41, 967-971. http://dx.doi.org/10.1590/S0103-84782011000600008
  » http://dx.doi.org/10.1590/S0103-84782011000600008
• Vieira, R. A., Scapim, C. A., Moterle, L. M. B., Tessmann, D. J., Amaral Júnior, A. T. and Gonçalves, L. S. A. (2012). The breeding possibilities and genetic parameters of maize resistance to foliar diseases. Euphytica, 185, 325-336. http://dx.doi.org/10.1007/s10681-011-0454-6
  » http://dx.doi.org/10.1007/s10681-011-0454-6
• Vieira, R. A., Scapim, C. A., Tessmann, D. J., Ferreira, F. R. A., Vivas, M. and Amaral Junior, A. T. (2016). A nonparametric approach to selection popcorn hybrids to resistance to foliar diseases. Científica, 44, 165-169. http://dx.doi.org/10.15361/1984-5529.2016v44n2p165-169
  » http://dx.doi.org/10.15361/1984-5529.2016v44n2p165-169
• Vieira, R. A., Scapim, C. A., Tessmann, D. J. and Hata, F. T. (2011). Diallel analysis of yield, popping expansion, and southern rust resistance in popcorn lines. Revista Ciência Agronômica, 42, 774-780. http://dx.doi.org/10.1590/S1806-66902011000300025
  » http://dx.doi.org/10.1590/S1806-66902011000300025
• Vivas, 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. http://dx.doi.org/10.1016/j.cropro.2015.02.007
  » http://dx.doi.org/10.1016/j.cropro.2015.02.007

Publication Dates

• Publication in this collection
  05 June 2017
• Date of issue
  Jul-Sept 2017

History

• Received
  11 May 2016
• Accepted
  22 Nov 2016