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Revista mexicana de fitopatología

versión On-line ISSN 2007-8080versión impresa ISSN 0185-3309

Rev. mex. fitopatol vol.39 no.3 Texcoco sep. 2021  Epub 13-Dic-2021

https://doi.org/10.18781/r.mex.fit.2106-2 

Phytopathological notes

Incidence and effect on grain yield of the “monkey’s hand” disease in 29 maize genotypes

José Jesús Márquez-Diego1 

Carlos De León-García de Alba2  * 

Reyna Isabel Rojas-Martínez2 

José Ricardo Sánchez-Pale3 

1 Estudiante de doctorado, Colegio de Postgraduados (CP), Campus Montecillo, km 36.5 Carretera México-Texcoco. Montecillo, Estado de México, C.P. 56230, México.

2 Programa de Postgrado en Fitosanidad-Fitopatología, Colegio de Postgraduados (CP), Campus Montecillo, km 36.5 Carretera México-Texcoco. Montecillo, Estado de México, C.P. 56230, México.

3 Universidad Autónoma del Estado de México, El Cerrillo Piedras Blancas, Toluca, Estado de México, C.P. 50295, México.


Abstract.

Recently, an increase in the presence of symptom of a possible new disease on maize has been observed which farmers have called “mano de chango” (monkey´s hand) due to the prolificacy shown by the ears. Initial reports, in the 1960s, indicated, with no proofs, that this disease was caused by fungi, insects, or nutritional deficiencies with incidences up to 100% and losses in grain yield. This is the first work where evaluation of incidence of the disease, in 21 commercial hybrids in the Toluca Valley, State of Mexico, a comercial hybrid and a native variety in the Mezquital Valley, Hidalgo State, and six improved open pollinated in Montecillo, State of Mexico. The highest incidences and grain yield losses were recorded in the genotype Aspros HC8 and the native variety “Hidalgo”, in Mezquital Valley, Hidalgo State, where disease symptoms showed considerable yield reduction. It is necessary to continue studies to determine the etiology and generate information to select genetic resistance to this possible new disease.

Key words: Monkey´s hand; phytoplasms; maize diseases

Resumen.

Recientemente, se ha observado un incremento en la presencia de una posible nueva enfermedad en plantas de maíz que genera prolificidad de mazorcas que los agricultores denominan “mano de chango”. Estos síntomas se han observado en áreas tropicales, subtropicales y del altiplano de México. Observaciones iniciales, en los años 1960s, indicaron, sin pruebas, que esta enfermedad era causada por hongos, insectos, o deficiencias nutricionales con incidencia de hasta 100% y pérdidas en producción de grano. Este es el primer trabajo en que se evalúa la incidencia de la enfermedad en 21 híbridos comerciales en el Valle de Toluca, México, un híbrido comercial y una variedad nativa de polinización libre en el Valle del Mezquital, Hidalgo, y seis variedades mejoradas de polinización libre en Montecillo, Texcoco, México. La mayor incidencia y pérdidas en rendimiento de grano por la enfermedad se observó en los genotipos Aspros HC8 y la variedad nativa “Hidalgo”, en el Valle del Mezquital, Hidalgo, en donde la presencia de síntomas de la enfermedad mostró una considerable reducción en rendimiento. Es necesario continuar estudios para investigar su etiología y generar información para selección de resistencia genética a esta posible nueva enfermedad.

Palabras clave: Mano de chango; fitoplasmas; enfermedades de maíz

Maize is one of the three main cereal crops grown due to its nutritional characteristics for humans and animals, as well as for industrial use. In Mexico it has great economic, social and cultural importance (SAGARPA, 2017). However, this crop is affected by diverse phytosanitary problems that considerably reduce its production, with fungal diseases being amongst the most important (CIMMYT, 2005). In recent years, a group of phytopathogens of the Mollicutes Class, including spiroplasms and phytoplasms, originally considered as a secondary group, have become increasingly important in diverse crops, including maize (Galvão et al., 2020).

The term “corn stunt” was used for the first time by Kunkel (Kunkel, 1946), who attributed the symptoms to a virus as a causal agent. Doi et al. (1967) described this group as microorganisms similar to mycoplasmas, sensitive to tetracycline, which were initially named mycoplasma-like organisms (MLO) (CIPF, 2016). Davis (1973), in a phase contrast microscope, observed and reported helicoidal filaments that he associated as being the causal agent of corn stunt and named it “corn stunt spiroplasma”. In addition, as a result of observations carried out in Mexico on maize with symptoms of corn stunt, Davis (1974) published the possibility of leafhoppers being the causal agent of corn stunt, as well as another non-mobile organism that caused another disease in maize. The presence of an additional organism to spiroplasm in the vectors was confirmed by Bascopé (1977) and later by Nault (1980), after observing mycoplasm-like structures in phloem cells of infected plants related to corn stunt in the insect Dalbulus (Moya and Nault, 1998). The new disease reported by these authors was named “Maize Bushy Stunt Disease” (MBSD). These investigations showed that the “Corn Stunt Disease” (CSS) and MBSD were different diseases transmitted by insects of the genus Dalbulus. It was in the last decade of the 20th Century that, with molecular tests based on the analysis of ribosomal RNA 16S, the phylogenetics of phytoplasms were established as members of the Mollicutes Class (Lee et al., 1998).

Among the maize diseases caused by Mollicutes, Costa et al. (2019) mention corn stunt caused by Spiroplasma kunkelii and the maize bushy stunt disease, the latter of which was, according to Pérez-López et al. (2018), found, without a basis, for the first time in Mexico in 1955. Both diseases are transmitted by several species of homoptera, the main one being the maize leafhopper (Dalbulus maidis), an insect found in soutern Mexico, considered the birthplace of the Dalbulus genus (Nault, 1980; Tsai and Miller, 1995; Casuso, 2017). In 1994, the Committee for the Taxonomy of Mollicutes, of the International Organization for Mycoplasmology (IOM), established the name currently used of phytoplasms (Kirkpatrick, 1994).

The symptoms of MBSD on maize include the formation of long lateral branches, a reduction in the development of ears and the proliferation of in the same rachis with the appearance of bracts, often twisted, with slanted edges showing chlorosis and reddening (Pecher et al., 2013) even leading to the production of an ear without killing the plant. Alcántara-Mendoza et al. (2010) indicated that the “monkey’s hand” disease is not a symptom that is related to MBSD, yet they describe that this disease does cause the death of the plant. The description of symptoms indicates a confusion and unawareness of the separation of corn stunt, MBSD and monkey’s hand (Figure 1). The latter disease was initially reported as “Manita” (little hand) by Cruz (1991) and later by Aguilar and Molina (1996).

The “monkey’s hand” disease has become destructive, causing variable losses in production, with reports of 35% in the Mezquital area, in Hidalgo, Mexico (Ortega, 2021. Personal communication) and up to losses of 35 to 93%, depending on the population of vector insects (González et al., 2018).

For their management, several cultural strategies have been studied, including planting dates, the elimination of crop residues, treatments to seeds and control of possible vectors, which have displayed a low efficiency in the control of the MBSD, therefore the use of genetically resistant germplasm is accepted as the main alternative to reduce damages and the incidence caused by the phytoplasm, although there are few studies related to the identification of sources of resistance and of genetic control (Costa et al., 2019), which is one of the aims of the present studies.

Locations of evaluation. The incidence and the effect of “monkey’s hand” were evaluated in commercial hybrids and free pollination varieties of maize in three locations. In the Experimental Field of the Autonomous University of the State of Mexico (UAEM) in Cerrillo, Piedras Blancas, Toluca, State of Mexico (19º 27´ 56” N, 99º 39´ 20” O, 2667 masl), 21 commercial hybrids were evaluated in a randomized block design with three replications. Each plot consisted of 2 rows, 3 m long, with 80 cm between rows and 22 cm between plants, for a total of 28 plants per plot. In the Cinta Larga Technology Innovation Center, in Mixquiahuala, Hidalgo (20° 13´ 52” N, 99° 12´ 47” W, 2100 masl), a commercial hybrid was established (Aspros HC8) along with the native open pollinated variety “Hidalgo”, which were planted each in 20 rows, 50 m long, with 80 cm between rows and 25 cm between plants, for a density of 85,000 plants ha-1. In the Experimental Field of the Colegio de Postgraduados, Campus Montecillo (19° 28’ 26” N and 98° 53’ 18” W, 2250 masl) in Texcoco, State of Mexico, the incidence of the disease was evaluated in six improved open pollinated synthetic varieties, each planted in 12 rows, 100 m long, with 80 cm between the rows and 22 cm between plants. In the Experimental Field of the Autonomous University of the State of Mexico, the incidence was evaluated at harvest time. In all three locations, a conventional agronomic production scheme was followed for the crops and insects and weeds were not controlled.

Figure 1 Symptoms of monkey’s hand disease related to phytoplasms in maize ears. 

Evaluation of incidence and damages. For the variable of incidence in the germplasm in the location of the UAEM, approximately one month before harvest, ears with symptoms of the disease were collected. In the experimental plot located in Mixquiahuala, Hidalgo, 600 plants were counted in 15 rows of the Aspros HC8 commercial hybrid, and likewise for the native open pollinated variety “Hidalgo”, for which 600 plants were counted, including those with symptoms of the disease. In the Campus Montecillo of the Colegio de Postgraduados, in the five improved open pollinated synthetic varieties planted, 400 plants were counted per variety in plants close to maturity, observing them closely looking for typical symptoms of ear proliferation to determine the disease incidence. Among those plants, the ones which presented symptoms of the disease were paired with immediately adjacent plants without symptoms to then determine the effect on grain yield. The paired plants were collected in pairs to weigh them, remove their kernels and record the percentage of humidity in the fresh grains using a Dicky John miniGAC plus® moisture meter to measure humidity and adjusting this to 14%. The weight of the grain produced by the plants with symptoms of the disease and that of adjacent healthy plants were analyzed using a paired t test design, and the means of disease incidence were compared with those of the grains in pairs of transformed ears, using the Shapiro-Wilk test of normality of the data with α=0.05 for the transformation of the arcsine of the incidence (0.077), so the residues have a normal distribution, and justifying their analysis. The means obtained were separated using Tukey’s test at 5% significance with the SAS analysis package, version 9.0.

The 21 hybrids evaluated in the UAEM showed a very low incidence of the disease with poor development of the ears and grains, therefore the trial in this location was eliminated.

In the location of Mixquiahuala, the commercial hybrid and the native variety “Hidalgo”, as well as the six free pollination varieties evaluated in Montecillo, Texcoco (Table 1) analyzed jointly, showed that the germplasm evaluated in Montecillo showed lower incidences than in the material evaluated in Mixquiahuala. The differences in incidence between the materials grown in Mixquiahuala and Montecillo were significant, particularly between the varieties of origin MO19 (Montecillo 2019) with 5.5, 5.2, 3.5, 1.0, 0.75 and 0.75% against the hybrid Aspros HC8 and the native “Hidalgo”, with 17 and 13%, respectively. In the trial established and evaluated in the Campus Montecillo of the Colegio de Postgraduados, the grain yield analysis applying the paired t test analysis showed a significant loss in grain production per ear in all the varieties, which reduced their yield by 86% in MO19:15# Bco (Colpos) to 20% in MO19: CP Hilda 2 Amar (Colpos).

Preliminary information is presented on the presence of monkey’s hand and its effect on the yield of maize plants with symptoms of the disease in subtropical conditions (Mezquital, Hidalgo) and the Mexican highlands (Montecillo, State of Mexico), although its effect on grain yield must be determined in a greater number of locations, including the conditions of the humid tropics, where maize producers indicate they have found symptoms similar to those described. This information is confirmed in reports by Alcántara-Mendoza et al. (2010) and Costa et al. (2019) in investigations carried out in tropical areas of Mexico and Brazil, respectively.

Table 1 Incidence of the “monkey’s hand” disease and its effect on the grain yield of hybrids and maize varieties evaluated in Mixquiahuala, Hidalgo, and in Montecillo, Mexico, 2020. 

Germoplasma evaluado Media Incidencia (%) Incidencia (Arco seno) Grano de mazorcas sanas (g) Grano de mazorcas enfermas (g) Disminución rendimiento de grano (%)
Aspros HC8 (Hidalgo) 17.5 0.427 az 128.24 62.75 ** 44.65 az
Criollo Hidalgo 13.5 0.375 ab 169.61 73.25 ** 42.13 a
MO19: CP Elvia 3 TSR# Bco (Colpos) 5.5 0.225 bc 148.33 76.80 ** 46.86 a
MO19: CP-Vero1 Bco (Colpos) 5.2 0.217 bc 156.45 111.04 * 73.34 a
MO19: 15# Bco (Colpos) 3.5 0.185 c 133.84 114.88 NS 86.76 a
MO19: CP Hilda 2 Amar. (Colpos) 1.0 0.068 c 111.00 12.25 ** 20.77 a
MO19: 11# Amar. (Colpos) 0.7 0.065 c 110.66 99.00 NS 69.75 a
MO19:19+2# Bco (Colpos) 0.7 0.065 c 104.00 51.00 ** 48.25 a
DMS: 0.176 CV (%): 73.5 DMS: 77.45 CV(%): 60.4

zzMeans with the same letter in each column are not statistically different (Tukey, P ≤ 0.05)

*: Significant P=0.05. **: Highly significant P=0.01. NS: not significant.

Symptoms of “monkey’s hand” and grain yield loss were found in the germplasm of the maize evaluated, with a higher incidence and grain loss in the hybrid Aspros HC8 and the native variety “Hidalgo” in the location of Mixquiahuala, Hidalgo. The plants affected by the disease significantly reduce their grain yield. Research must continue to determine the etiology of the disease and evaluate a larger number of variants in maize germplasm to identify and select possible sources of resistance to the disease.

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Received: June 28, 2021; Accepted: August 13, 2021

* Autor para correspondencia: cdeleon@colpos.mx

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