SciELO - Scientific Electronic Library Online

 
vol.7 número6Valoración económica del agua potable en la delegación Iztapalapa, D. F.Sangre Maya, variedad de frijol de grano rojo para el estado de Chiapas índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Revista mexicana de ciencias agrícolas

versión impresa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.7 no.6 Texcoco ago./sep. 2016

 

Investigation notes

Incidence and severity of ear rot on genetically modified and conventional maize in Sinaloa, Mexico

Agustín Hernández Juárez1 

Luis A. Aguirre Uribe1  § 

Mariano Flores Dávila1 

Ernesto Cerna Chávez1 

Jerónimo Landeros Flores1 

Yisa M. Ochoa Fuentes1 

Gustavo A. Frías Treviño1 

1Universidad Autónoma Agraria Antonio Narro-Departamento de Parasitología. Calzada Antonio Narro, núm. 1923. Buenavista, Saltillo, Coahuila de Zaragoza, México. C. P. 25315. Tel: 844 411 03 26. (chinoahj14@hotmail.com; cisef9@hotmail.com; jabaly1@yahoo.com; jlanflo@hotmail.com; yisa8a@yahoo.com; servesa_gfriast@hotmail.com).


Abstract

It was assessed in genetically modified (GM) maize with Agrisure® VipteraTM 3111, the incidence and severity of ear rot by Fusarium sp., in two locations from Culiacan, Sinaloa. In El Camalote, the hybrid showed incidence and severity of 47.2 and 22.5% respectively; compared to conventional hybrid with pest control showed 54.7 and 27.1% of incidence and severity of rot and conventional hybrid (control), had further damage with an incidence of 59.4 and severity of 35.2%. In assessing Oso Viejo, the hybrid Agrisure® VipteraTM 3111 showed less damage with 25.7 and 7.6% incidence and severity of the disease respectively; the conventional hybrid with pest control had an incidence of 67.5% and severity of 38.7%, and control had the highest damage 80.8 and 53.5% of incidence and severity. Agrisure® VipteraTM 3111 corn was not developed for disease management, however; the findings show that the genetically modified maize confers an indirect additional benefit to pest resistance, preventing the formation of entry points for pathogens that develop in susceptible tissue, causing ear rot.

Keywords: Bacillus thuringiensis; Zea mays L.; ear diseases; fungi; transgenic plants

Resumen

Se evaluó en maíz genéticamente modificado (GM) con el evento Agrisure® VipteraTM 3111, la incidencia y severidad de pudrición de mazorca por Fusarium sp., en dos localidades de Culiacán, Sinaloa. En El Camalote, el híbrido observó una incidencia y severidad de 47.2 y 22.5% respectivamente; comparado con el híbrido convencional con control de plagas que presentó 54.7 y 27.1% de incidencia y severidad de pudrición y el híbrido convencional (testigo absoluto), tuvo un mayor daño con una incidencia de 59.4 y 35.2% de severidad. En la evaluación de Oso Viejo, el hibrido Agrisure® VipteraTM 3111 presentó menor daño con 25.7 y 7.6% de incidencia y severidad de la enfermedad respectivamente; el híbrido convencional con control de plagas tuvo una incidencia de 67.5% y una severidad de 38.7%, y el testigo absoluto tuvo el mayor daño 80.8 y 53.5% de incidencia y severidad. El maíz Agrisure® VipteraTM 3111 no fue desarrollado para el manejo de enfermedades, no obstante; el resultado encontrado demuestra que el maíz genéticamente modificado confiere un beneficio adicional indirecto al de resistencia a insectos plaga, previniendo la formación de puntos de entrada para fitopatógenos que se desarrollan en el tejido susceptible, provocando la pudrición de mazorca.

Palabras clave: Bacillus thuringiensis; Zea mays L.; enfermedades de mazorca; hongos; plantas transgénicas

Introduction

Mexico is one of the main producers of maize (Zea mays L.) in the world, whose production in 2014 was 23 273 256.54 t, over other cereals such as wheat, sorghum, barley, rice and oats, highlighting the state of Sinaloa with higher production of 3 686 274.43 t. The economic importance of this state has been increasing due to its production through double crop cycle [spring-summer and autumn-winter] (SAGARPA / SIAP, 2015). This type of planting throughout the year, favors the development of pests and the spread of disease, the incidence of which represents a potential risk for crop management.

Among the most economically important diseases is ear rot caused by Fusarium sp., which is located in all regions where maize is grown, mainly in tropical areas with high relative humidity. This pathogen is able to colonize and cause damage at all stages of the crop and survive extended periods in plant residues (Thomas and Buddenhagen, 1980; Desjardins et al., 1994; De León, 1997; Mendoza et al., 2003). In Seed, can invade and cause stains on the outside, reducing the germination rate by death of the embryo (De Leon, 1997; González et al., 2007; Morales et al., 2007), it also produces mycotoxins that affect human and animal health (Robledo et al., 2001; Bakan et al., 2002, Desjardins et al., 2006). The severity of this disease in maize causes a direct effect in decreasing yield, which for central Mexico, ranges from 6-55% (González et al., 2007; Briones et al., 2015) and on agricultural area from Sinaloa report losses above 30% (García et al., 2012).

Rot incidence has increased in recent years, partly due to the effect of precipitation from spike formation to harvest, and the presence of mechanical damage on cob and grain caused by corn earworm Helicoverpa zea ( Boddie), armyworm Spodoptera frugiperda (J. E. Smith) and other insects, which contribute to the spread of Fusarium spores (De León, 1997; Paliwal et al., 2001; Wu, 2006).

The development of genetically modified (GM) maize hybrid, encoding proteins of Bacillus thuringiensis Berliner to express the ∂-endotoxin (Bt maize), confers resistance to a wide spectrum of lepidopteran and coleopteran (Buntin et al., 2004a; Buntin et al., 2004b; Buntin, 2008; Duan et al., 2008; Hardke et al., 2011); being a practical option to control these insects in the field, reducing the entry points for pathogenic fungi.

Whereas GM maize was authorized to prove its effectiveness during 2009-2013 in Mexico under experimental conditions, this research was to evaluate the incidence and severity of ear rot by Fusarium sp., in GM maize with Agrisure® VipteraTM 3111, in the agricultural area of Sinaloa.

The research was conducted in the sinaloense coastal plain ecoregion, in the towns of El Camalote and Oso Viejo, in Culiacan, Sinaloa, Mexico, during autumn-winter cycle. The corn hybrid used with the event Agrisure® VipteraTM 3111 that express Cry1Ab toxin from B. thuringiensis var. Kurstaki strain HD1 and Vip3Aa20 from B. thuringiensis strain AB88 that confer resistance to Lepidoptera such as Agrotis ipsilon (Hufnagel), Diatraea saccharalis (Fabricius), S. frugiperda, Spodoptera exigua (Hübner), Heliothis virescens (Fabricius), H. zea, among others and mCry3A toxin from B. thuringiensis subspecies tenebrionis which confers resistance to Diabrotica (Chevrolat in Dejean )species; and also expresses the mutated enzyme 5-enolpyruvylshikimate-3-phosphate-synthase (mEPSPS) which confers tolerance to the herbicide glyphosate and glufosinate ammonium and as control was used, the conventional hybrid without the insertion of Cry toxins, materials that were provided by the company Syngenta Agro S.A. de C.V. of Mexico.

The experimental study was conducted under a randomized complete block with three treatments and four replications. Treatments were Agrisure® VipteraTM 3111, conventional hybrid and conventional hybrid with insect control (conventional hybrid + ci); whose establishment in the towns of El Camalote and Oso Viejo took place on March 14 and 15 2013 respectively. Each treatment consisted of 10 rows 5 m long and row spacing of 0.8 m, with a seeding density of 40 seeds per row and subsequent thinning to 34 plants per row. The trial was surrounded with conventional maize board consisting of six rows 5 m long and another border of the same dimensions separating each replication of the study. At the end of the production cycle, before harvest, 10 ears at random were counted among the four central rows in each replication and incidence was assessed, understood as the number of ears showing disease symptoms and severity (total area %) of disease (rot). The data were transformed by square root of arcsine and subjected to ANOVA and comparison of means of the treatment was performed with a multiple range test of Tukey (p< 0.05) using SAS/STAT software (SAS Institute, 2002).

It is worth mentioning that plantings were conducted under biosafety conditions, in plots with a distance of more than 500 m from any other commercial planting of corn and with a lag of 50 days at the recommended planting date, to not match with flowering stage of neighboring fields and avoid cross-pollination; protocol to follow to meet regulatory requirements for field experiments with GM maize in Mexico (LBOGM, 2005; Halsey et al., 2005).

Under this biosafety condition, it was not allowed to extract plant tissue, avoiding any spread of GM material, for this reason the causative agent of ear rot was identified only under field conditions, from visual symptoms in each ear, observing the development of a cottony white mycelium to pink on the surface or between grains and in some grains of premature germination, characteristic of Fusarium sp, probably moniliforme species; according to the description from De León (1997) and based on the identification guide on field of corn crop diseases developed by the International Maize and Wheat Improvement Center (CIMMYT, 2004).

Insecticide application was addressed to control lepidoptera, mainly S. frugiperda under an infestation threshold of 10% in plants smaller to 20 cm and 20% in plants higher than 20 cm, based on conventional, at rate of two applications during the growing cycle with emamectin benzoate (Denim® 19 CE, 200 mL ha, Syngenta Agro S.A. de C.V. of Mexico). Agronomic crop management during the course of the experiment was conducted based on typical practices of the region and according to the technical guide for the cultivation of corn developed by the National Institute of Forestry, Agriculture and Livestock (INIFAP, 2010).

The percentage of ears affected and severity degree of the disease attributed to phyto pathogenic fungus Fusarium sp., was lower in plots with corn Agrisure® VipteraTM 3111, compared to conventional maize plots, including control with insecticide in both experimental locations. However, in El Camalote there was no significant difference in the incidence and severity of ear rot among the materials, while in Oso Viejo there was significant difference between treatments (p< 0.05) (Table 1).

Table 1. Incidence and severity (± SD) of ear rot by Fusairum sp., in genetically modified and conventional maize in the localities of El Camalote and Oso Viejo, Culiacan, Sinaloa, Mexico. 

Material genético Localidad Incidencia (%) 1 Severidad (%) 1
Agrisure® VipteraTM 3111 El Camalote 47.2 ± 16.9 a 22.5 ± 8.2 a
Híbrido convencional + ci El Camalote 54.7 ± 16.7 a 27.1 ± 6.8 a
Híbrido convencional El Camalote 59.4 ± 14 a 35.2 ± 6.2 a
F=0.48; gl=2,11 ns F=2.71; gl=2,11 ns
Agrisure® VipteraTM 3111 Oso Viejo 25.7 ± 9.8 a 7.6 ± 4.5 a
Híbrido convencional + ci Oso Viejo 67.5 ± 4.7 b 38.7 ± 14.2 b
Isolínea Oso Viejo 80.8 ± 10.6 b 53.5 ± 9.9 b
F=64.61; gl=2,11*** F=23.62; gl=2,11**

The lower incidence and severity of ear rot in Agrisure® VipteraTM 3111, it is probably due to the protection of the plant to the attack of pests, mainly corn earworm and armyworm (the latter feeds on the cob), giving as a result fewer infested cobs, or significantly smaller lesions, preventing infestation pathogens, which is contrary to the conventional hybrid without insect control. For hybrid with control with insecticide, this sometimes does not match the developmental stages of the pest and its effect is temporary, since the chemical only protects the plant during the residual period thereof, besides not having an effective effect on these insects, because the larva inside the ear is not exposed to the active ingredient, being protected by corn bract.

Crop protection to lepidopteran attack, assessed through ear damage by corn earworm H.zea, was demonstrated in this GM hybrid in 2013, at the same time with the assessment of ear rot for this agricultural area by Aguirre et al. (2015); who demonstrated the effectiveness of inserted proteins in corn on earworm observing that these hybrids conferred resistance to attack of this pest by killing it or reducing its growth causing less damage to corn; effect that confers to corn an indirect additional benefit, because preventing damage by infestations of corn earworm and reducing the damage on the cob, also reduces the formation of entry points for pathogenic fungi that develop in susceptible tissue, causing a reduction in contamination of corn kernels that produce rots caused by Fusarium compared to conventional maize plants, which under favorable conditions ear rot can make the difference between a crop with low yields or a good harvest, mainly in regions where the disease is favored by high humidity in the environment.

It is important to minimize the presence of Fusarium in grain, since ear rot causes severe crop losses (Betanzos, 2001), limiting their marketing, because the tolerable level of contamination is 5% of allowable damage and constitutes a problem to public health by mycotoxins produced by the plant pathogen when its incidence and damage is high (Mendoza et al., 2006 Betanzos et al., 2009; García et al., 2012).

This GM maize has not been developed for the control of diseases such as ear rot, however; the result found in this study shows that corn hybrids with event Agrisure® VipteraTM 3111 show lower incidence and severity of Fusarium sp., which could indicate that under certain conditions, the use of Bt corn could favor human and animal safety due to the reduced risk by mycotoxin consumption [aflatoxins, fumonisins, trichothecenes, zearalenones, etc.] that affect grain quality; consistent with the findings of Munkvold et al. (1997); Munkvold et al. (1999); Munkvold and Hellmich (1999); Masoero et al. (1999); Bakan et al. (2002); Clements et al. (2003); Wu (2006); Aguirre et al. (2014); who suggest that GM maize hybrids with the insertion of a Cry toxin to control insect influence the incidence and severity of ear rot caused by Fusarium sp, reporting these as lower ear rot and even less fumonisins content, in some cases 9-10 times less in genetically modified maize compared to conventional maize.

Conclusions

This is one of the first results under the environmental conditions of Mexico, offering an approach on ear rot in genetically modified maize; this because experimental trials with GM maize in the country were only conducted during the years 2009-2013, as permits for subsequent experiments were canceled or detained, which did not allow to monitor this types of assessments. Therefore, it is required to give a step to the next round of experimental tests, more years of analysis and with more replications, to strengthen this type of information in our country and strengthen the conclusions.

Literatura citada

Aguirre, L. A.; Hernández, A; Flores, M.; Frías, G. A.; Cerna, E.; Landeros, J. and Harris, M. K. 2015. Genetically modified maize resistant to corn earworm (Lepidoptera: Noctuidae) in Sinaloa, Mexico. Florida Entomologist. 98(3):821-826. [ Links ]

Aguirre, U. L. A.; Frías, T. G. A.; Hernández, J. A.; Flores, D. M.; Cerna, C. E.; Landeros, F. J. and Ochoa, F. Y. M. 2014. Interaction between Helicoverpa zea damage with corncob diseases on genetically modified corn in Sinaloa, México. J. Life Sci. 8(4):329-334. [ Links ]

Bakan, B.; Melcion, D.; Richard, M. D. and Cahagnier, B. 2002. Fungal growth and Fusarium mycotoxin content in isogenic traditional maize and genetically modified maize grown in France and Spain. J. Agric. Food Chem. 50(4):728-731. [ Links ]

Betanzos, M. E.; Ramírez, F. A.; Coutiño, E. B.; Espinosa, P. N.; Sierra, M. M.; Zambada, M. A. y Grajales, S. M. 2009. Híbridos de maíz resistentes a pudrición de mazorca en Chiapas y Veracruz, México. Agric. Téc. Méx. 35(4):389-398. [ Links ]

Betanzos, M. E. 2001. Variedades resistentes, una opción para reducir la pudrición de mazorca en Chiapas, México. Agric. Téc. Méx. 27(1):57-67. [ Links ]

Briones, R. D.; Castillo, G. F.; Chávez, S. J. L.; Aguilar, R. V. H.; García, A. C. L. y Ramírez, H. A. 2015. Respuesta del maíz nativo del altiplano mexicano a pudrición de mazorca, bajo infección natural. Agron. Mesoam. 26(1):73-85. [ Links ]

Buntin, G. D. 2008. Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm (Lepidoptera: Noctuidae) management in field corn for grain production. Florida Entomologist. 91(4): 523-530. [ Links ]

Buntin, G. D.; All, J. N.; Lee, R. D. and Wilson, D. M. 2004a. Plant- incorporated Bacillus thuringiensis resistance for control of fall armyworm and corn earworm (Lepidoptera: Noctuidae) in Corn. J. Econ. Entomol. 97(5):1603-1611. [ Links ]

Buntin, G. D.; Flanders, K. L. and Lynch, R. E. 2004b. Assessment of experimental Bt events against fall armyworm and corn earworm in field corn. J. Econ. Entomol. 97(2):259-264. [ Links ]

Centro Internacional de Mejoramiento de Maíz y Trigo (CIMMYT). 2004. Enfermedades del maíz: una guía para su identificación en el campo. Cuarta edición. México, D. F. 118 p. [ Links ]

Clements, M. J.; Campbell, K. W.; Maragos, C. M.; Pilcher, C.; Headrick, J. M.; Pataky, J. K. and White, D. G. 2003. Influence of Cry1Ab protein and hybrid genotype on Fumonisin contamination and Fusarium ear rot of corn. Crop Sci. 43(4):1283-1293. [ Links ]

De León, C. 1997. Enfermedades del maíz causadas por hongos. In: I curso Internacional sobre diagnóstico y enfermedades en maíz. Seminario taller de cosecha de maíces de la zona andina. Centro Internacional de Mejoramiento de Maíz y Trigo (CIMMYT). Cochabamba, Bolivia. Editorial PRODUMEDIOS. Bogotá, Colombia. 94 p. [ Links ]

Desjardins, A. E.; Plattner, R. D. and Nelson, P. E. 1994. Fumonisin production and other traits of Fusarium moniliforme strains from maize in northeast Mexico. Appl. Environ. Microbiol. 60(5):1695-1697. [ Links ]

Desjardins, A. E.; Maragos, C. M. and Proctor, R. H. 2006. Maize ear rot and moniliformin contamination by cryptic species of Fusarium subglutinans. J. Agric. Food Chem. 54(19):7383-7390. [ Links ]

Duan, J. J.; Teixeira, D.; Huesing, J. E. and Jiang, C. 2008. Assessing the risk to nontarget organisms from Bt corn resistant to corn rootworms (Coleoptera: Chrysomelidae): tier-I testing with Orius insidiosus (Heteroptera: Anthocoridae). Environ. Entomol. 37(3):838-844. [ Links ]

García, G. C.; Lizárraga, S. G. J.; Armenta, B. A. D. y Apodaca, S. M. A. 2012. Efecto de productos biorracionales en la incidencia de hongos y concentración de aflatoxinas en maíz blanco cultivado en Sinaloa, México. Rev. Científica UDO Agrícola. 12(4):830-838. [ Links ]

González, H. A.; Vázquez, G. L. M.; Sahagún, C. J.; Rodríguez, P. J. E. y Pérez, L. D. J. 2007. Rendimiento del maíz de temporal y su relación con la pudrición de mazorca. Agric. Téc. Méx. 33(1):33-42. [ Links ]

Halsey, M. E.; Remund, K. M.; Davis, C. A.; Qualls, M.; Eppard. P. J. and Berberich, S. A. 2005. Isolation of maize from pollen mediated gene flow by time and distance. Crop Sci. 45(6):2172-2185. [ Links ]

Hardke, J. T.; Leonard, B. R.; Huang, F. and Jackson, R. E. 2011. Damage and survivorship of fall armyworm (Lepidoptera: Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins. Crop Protection. 30(2):168-172. [ Links ]

INIFAP. 2010. Centro de Investigación Regional del Noreste (CIRNO). Campo Experimental Valle de Culiacán (CEVACU). Maíz. In: guía técnica para el área de influencia del Campo Experimental Valle de Culiacán. Culiacán, Sinaloa; México. 224 p. [ Links ]

LBOGM. 2005. Diario Oficial de la Federación 18 de marzo de 2005. México, D. F. [ Links ]

Masoero, F.; Moschini, M.; Rossi, F.; Prandini, A. and Pietri, A. 1999. Nutritive value, mycotoxin contamination and in vitro rumen fermentation of normal and genetically modified corn (Cry1A9b) grown in northern Italy. Maydica. 44:205-209. [ Links ]

Mendoza, E. M.; Andrio, E. E.; López, B. A.; Rodríguez, G. R.; Latournerie, M. L. y Rodríguez, H. S. A. 2006. Tasa de infección de la pudrición del tallo en maíz causada por Fusarium moniliforme. Agron. Mesoam. 17(1):19-24. [ Links ]

Mendoza, E. M.; López, B. A.; Oyervides, G. A.; Martínez, Z. G.; De León, C. y Moreno, M. E. 2003. Herencia genética y citoplásmica de la resistencia a la pudrición de la mazorca del maíz (Zea mays L.) causada por Fusarium moniliforme Sheld. Rev. Mex. Fitopatol. 21(3):267-271. [ Links ]

Morales, R. I.; Yañez, M. M. J.; Silva, R. H. V.; García, S. G. and Guzmán, P. D. A. 2007. Biodiversity of Fusarium species in Mexico associated with ear rot in maize, and their identification using a phylogenetic approach. Mycopathologia. 163(1):31-39. [ Links ]

Munkvold, G. P. and Hellmich, R. L. 1999. Genetically modified insect resistant corn: Implications for disease management. APSnet Feature. http://www.apsnet.org/publications/apsnetfeatures/Pages/InsectResistantCorn.aspx. Online. doi: 10.1094/APSnetFeature-1999-1199. [ Links ]

Munkvold, G. P.; Hellmich, R. L. and Showers, W. B. 1997. Reduced fusarium ear rot and symptomless infection in kernels of maize genetically engineered for European corn borer resistance. Phytopathology. 87(10):1071-1077. [ Links ]

Munkvold, G. P.; Hellmich, R. L. and Rice, L. G. 1999. Comparison of fumonisin concentrations in kernels of transgenic Bt maize hybrids and non-transgenic hybrids. Plant Dis. 83(2):130-138. [ Links ]

Paliwal, R. L.; Granados, G.; Lafitte, H. R. y Violic, A. D. 2001. El maíz en los trópicos: mejoramiento y producción. Depósito de documentos de la Organización de las Naciones Unidas para la Agricultura y la Alimentación (FAO). Roma, Italia. http://www.fao.org/docrep/003/x7650s/x7650s00.htm. [ Links ]

Robledo, M. L.; Marín, S. y Ramos, A. J. 2001. Contaminación natural con micotoxinas en maíz forrajero y granos de café verde en el estado de Nayarit (México). Rev. Iberoam. Micol. 18:141-144. [ Links ]

SAGARPA. 2015. Servicio de Información Agroalimentaria y Pesquera (SIAP). http://www.siap.gob.mx/index. [ Links ]

SAS. Institute. 2002. The SAS System for Windows, Release 9.0. SAS, Institute, Cary N. C. U.S.A. [ Links ]

Thomas, M. D. and Buddenhagen, I. W. 1980. Incidence and persistence of fusarium moniliforme in symptomless maize kernels and seedlings in Nigeria. Mycologia. 72(5):882-887. [ Links ]

Wu, F. 2006. Mycotoxin reduction in Bt corn: potential economic, health, and regulatory impacts. Transgenic Res. 15(3):277-289. [ Links ]

Received: August 2016; Accepted: September 2016

Creative Commons License Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons