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Ecosistemas y recursos agropecuarios

versão On-line ISSN 2007-901Xversão impressa ISSN 2007-9028

Ecosistemas y recur. agropecuarios vol.10 no.2 Villahermosa Mai./Ago. 2023  Epub 22-Set-2023

https://doi.org/10.19136/era.a10n2.3538 

Scientific articles

Introgression of transgenic events and accompanying sequences into Mexican maize varieties

Introgresión de eventos transgénicos y secuencias acompañantes en maíces mexicanos

Jessica Nallely Siller-García1 

Miguel Ángel Cruz-González1 

Francisco Castillo-Reyes2 
http://orcid.org/0000-0002-6121-7313

Sergio Alfredo Rodríguez-Herrera3 

Jesús Antonio Morlett-Chávez1 
http://orcid.org/0000-0001-7988-423X

Cristóbal N. Aguilar1 
http://orcid.org/0000-0001-5867-8672

Raúl Rodríguez-Herrera1  * 
http://orcid.org/0000-0002-6428-4925

1Food Research Department. School of Chemistry. Universidad Autónoma de Coahuila. Blvd. Carranza y Ing. José Cárdenas V. s/n. Col. República Oriente. CP. 25280. Saltillo, Coahuila. México.

2National Research Institute of Forestry, livestock and Agriculture. Saltillo Experimental Station. Carretera Saltillo-Zacatecas km 8.5, No. 9515, Col. Hacienda de Buenavista, CP. 25315. Saltillo, Coahuila, México.

3Plant Breeding Department, Universidad Autónoma Agraria Antonio Narro. Calz. Antonio Narro No. 1923, Buenavista, CP. 25315. Saltillo, Coahuila, México.


Abstract

Representative seed samples of 215 of maize varieties from four (Jalisco, Michoacán, Oaxaca and Puebla) Mexican States were collected. The total genotypes collected in each State were 53, 96, 46 and 20 samples, respectively. Each seed collection was geo-referenced, then seed was planted and leaf tissue was used for DNA isolation, after that a PCR analysis was performed to determine the presence or absence of eight accompanying sequences and nine transgenic events in the 215 maize genotypes. Results showed introgression of accompanying sequences and transgenic events (cry1Ab) into some maize varieties. The major proportion of cry1Ab residues was observed in maize samples from Puebla (70%) followed by that displayed in the Oaxaca samples (52%), while Jalisco samples showed 15 and 7.5% of the cry1Ab gene and ntpII accompanying sequence, respectively, and Michoacán samples exhibited 44 and 17.7% for cry1Ab gene and the accompanying sequence, respectively. These results supported for applicate corrective measures for to prevent the genetic contamination of Mexican maize varieties and to clean up out-of-type phenotypes that could be sources of contamination of transgenic genes within maize populations contaminated with transgenes.

Key words: Mexican maize varieties; genetic contamination; transgenic events; Cry1Ab; ntpII

Resumen:

Se recolectaron muestras de semillas de 215 de variedades de maíz representativas de cuatro (Jalisco, Michoacán, Oaxaca y Puebla) estados de México. El total de genotipos colectados en cada Estado fue de 53, 96, 46 y 20, respectivamente. Cada colecta de semilla fue georreferenciada; posteriormente cada colecta se sembró y el tejido foliar se usó para el aislamiento de ADN, luego se realizó un análisis de PCR para determinar la presencia o ausencia de ocho secuencias acompañantes y nueve eventos transgénicos en los 215 genotipos. Los resultados mostraron la introgresión de secuencias acompañantes y eventos transgénicos (cry1Ab) en el genoma de algunas variedades locales de maíz. La mayor proporción de residuos de cry1Ab observados en las variedades locales de maíz fue la muestra de Puebla (70%), seguida por las muestras de Oaxaca donde se observó 52%, mientras que 15 y 7.5% de los maíces nativos del estado de Jalisco presentaron el gen cry1Ab y la secuencia acompañante ntpII, respectivamente. Las muestras de Michoacán mostraron 44 y 17.7% para el gen cry1Ab y la secuencia acompañante, respectivamente. Estos resultados deben respaldar la aplicación de medidas correctivas para prevenir la contaminación genética de variedades locales de maíz y limpiar fenotipos fuera de tipo que podrían ser fuentes de contaminación de genes transgénicos dentro de poblaciones de variedades locales de maíz contaminadas con estos transgenes.

Palabras clave: Variedades mexicanas de maíz; contaminación genética; eventos transgénicos; Cry1Ab; ntpII

Introduction

Currently, the most important transgenic crops worldwide are: soybeans, maize, cotton and canola. Soybean ranks first, followed by maize, cotton and canola with 105, 60.9, 25.7 and 10 million ha, respectively (ISAAA 2019, Voora et al. 2020). Because of the agronomic benefits that the use of genetically modified seeds represents, GM crops have gained acceptance in some countries in such a way that the estimated global area of transgenic crops has increased from 1.7 million ha in 1996 to 273.4 million at the present time (Brookes 2022). However, use of these transgenic organisms has generated an intense debate that goes from the scientific field to economic, social, political, ethical and moral levels (Sharma et al. 2022). Maize is the most important agricultural crop in Mexico, from the point of view of food, as well as industrial, political and social sector (Ibarrola-Rivas et al. 2020), as referred to the different archaeological, genetic, biochemical and historical studies that allow understanding the use of corn in the Mexican history, and evolutionary history of this cereal (Erenstein et al. 2022), that helps to understand the diversity of endemic maize varieties in this country (Orozco-Ramírez et al. 2016, Fonseca et al. 2023).

Worldwide, only 20% of maize production goes to human consumption, and 80% is used as animal feed or industrial raw material (Grote et al. 2021, Erenstein et al. 2022), however, in Mexico, 68% of its maize production is used for human consumption (Ibarrola-Rivas et al. 2020, Arce et al. 2020). Based on these antecedents and adding that Mexico has a wide diversity of natural conditions that provides numerous environments for maize growth (Vidal and Brusca 2020, Grote et al. 2021). In addition, these particular diverse environmental conditions have allowed to developing by selection and interaction with environment, very specific populations, which are commonly referred as maize varieties, a term used to refer to a population native of the community, region, state or country, differing from a foreign material as a hybrid or an improved variety. Local varieties are heterogeneous populations of plants that are differentiated by farmers based on their color, texture, and shape of the grain, shape of the ear, crop cycle and use. They are maize populations developed by farmers for many years, through the management and conservation of seeds and genes through a system of exchange year after year. Maize varieties (hybrid or improved varieties) is also considered to be the set of plants that are the product of a natural or artificial crossing (crossed by farmers, by breeders or both) with an improved material, respecting that this set of plants. It is constituted with 75% of the original variety’s genetic material and 25% of the improved material (Salgotra and Chauhan 2023).

Maize in a large percentage is an open pollinated crop, which facilitates its crossing between varieties (Guzzon et al. 2021, Li et al. 2023) and with some of the species considered as ancestors as Zea perennis (Lohn et al. 2021), but also with commercial hybrids (Eze et al. 2020). This situation has led to a genetic contamination by transgenes in the natural ecosystems of Mexico, as it has been documented. Since 2001, there are isolated reports that indicate the presence of GM sequences in maize varieties in Oaxaca and some others Mexican states (Quist and Chapela 2001, Cleveland et al. 2005, Serratos-Hernández et al. 2007, Mercer and Wainwright 2008, Piñeyroet al. 2009, Orozco-Ramírez et al. 2016, Rendón-Aguilar et al. 2019). Based on these antecedents, and in view of the degree of contamination of these native maize with transgenic genes is unknown in other Mexican states, as well as the transgenic sequence (s) that have been introduced. The objectives of this study were to determine the level of introgression of transgenes into maize varieties of Puebla, Oaxaca, Jalisco and Michoacán States, to estimate of frequencies of maize contamination and to identify the main transgenic events transferred to the maize varieties.

Materials and methods

Collection of maize varieties

Samples were collected by field trips to rural community from the states of Puebla, Jalisco, Michoacán and Oaxaca. Each sample weighted 1000 g of composite seed and was obtained from participate producer which were randomly chosen. In this study, a total of 215 maize local varieties were obtained, 53 out of 215 seed samples were collected from Jalisco, 96 samples from Michoacán, 46 samples from Oaxaca and 20 samples from Puebla State (Table 1). Each sampling site was geo-referenced in terms of altitude, latitude and longitude. Seed from each sample was placed for conservation in the maize germplasm bank of the Universidad Autonoma Agraria Antonio Narro.

Table 1 Localities and maize genotypes collected from Jalisco (J), Michoacán (M), Oaxaca (O) and Puebla (P) states. 

No Key Genotype Locality Latitude (N) Longitude (W) Altitude (masl)
1 J1 Celaya 2010 (C-2) Jamay 20°17’ 17.60" 102°41’ 39.46" 1530
2 J2 Celaya 2010 (3) Jamay 20°17’ 18.44" 102°40’ 35.91" 1528
3 J3 Celaya 2010 (4) La Barca 20°18’ 14.07" 102°31’ 57.01" 1535
4 J4 Celaya 2010 (5) La Barca 20°17’ 17.89" 102°31’ 45.67" 1538
5 J5 Celaya 2010 (6) La Barca 20°17’ 20.72" 102°33’ 14.11" 1533
6 J6 Celaya 2010 (7) Jesus Maria 20°36’ 33.29" 102°12’ 57.00" 2121
7 J7 Celaya 2010 (8) Arandas 20°41’ 54.89" 102°20’ 0.67" 2045
8 J8 Celaya 2010 (10) Arandas 20°41’ 47.11" 102°21’ 39.20" 2054
9 J9 Celaya 2010 (11) Arandas 20°41’ 10.49" 102°20’ 23.92" 2063
10 J10 Celaya 2010 (12) San Juan de los Lagos 21°14’ 34.26" 102°21’ 40.89" 1870
11 J11 Celaya 2010 (15) San Juan de los Lagos 21°16’ 1.50" 102°21’ 2.47" 1750
12 J12 Celaya 2010 (16) San Juan de los Lagos 21°15’ 22.04" 102°18’ 52.99" 1784
13 J13 Celaya 2010 (17) Lagos de Moreno 21°21’ 4.92" 101°54’ 54.31" 1875
14 J14 Celaya 2010 (18) Lagos de Moreno 21°20’ 25.71" 101°56’ 23.89" 1868
15 J15 Celaya 2010 (19) Jesus Maria 20°36’ 44.99" 102°13’ 35.45" 2047
16 J16 Celaya 2010 (20) Lagos de Moreno 21°21’ 3.65" 101°54’ 19.99" 1883
17 J17 Celaya 2010 (22) San Diego 20°9’ 38.30" 103°3’ 25.44" 1541
18 J18 Celaya 2010 (23) Mazamitla 19°54’ 55.78" 103°0’ 44.19" 2237
19 J19 Celaya 2010 (24) San Diego 20°10’ 20.59" 103°3’ 43.75" 1528
20 J20 Celaya 2011 (25) Atoyac 20°0’ 45.84" 103°31’ 15.87" 1356
21 J21 Celaya 2010 (26) Mazamitla 19°54’ 53.76" 103°1’ 41.44" 2197
22 J22 Celaya 2010 (27) Tala 20°38’ 54.70" 103°42’ 56.39" 1317
23 J23 Celaya 2010 (28) Tala 20°39’ 0.69" 103°43’ 24.04" 1310
24 J24 Celaya 2010 (29) Tala 20°39’ 39.62" 103°43’ 16.07" 1312
25 J25 Celaya 2010 (30) Tapalpa 19°56’ 25.18" 103°45’ 33.94" 2039
26 J26 Celaya 2010 (32) Tapalapa 19°56’ 37.41" 103°46’ 7.16" 2038
27 J27 Celaya 2010 (34) Atoyac 20°0’ 35.07" 103°31’ 25.77" 1353
28 J28 Celaya 2010 (35) Sayula 19°52’ 22.70" 103°34’ 57.37" 1365
29 J29 Celaya 2010 (37) Sayula 19°53’ 45.17" 103°35’ 49.82" 1359
30 J30 Celaya 2010 (38) Gomez Farias 19°47’ 56.00" 103°28’ 55.90" 1516
31 J31 Celaya 2010 (39) Zapotiltic 19°37’ 32.73" 103°26’ 9.10" 1370
32 J32 Celaya 2010 (40) Zapotiltic 19°37’ 10.96" 103°25’ 34.27" 1335
33 J33 Celaya 2010 (42) Tuxpan 19°32’ 48.94" 103°22’ 8.36" 1130
34 J34 Celaya 2010 (43) Tuxpan 19°32’ 48.28" 103°23’ 0.04" 1124
35 J35 Celaya 2010 (45) Techaluta 20°4’ 26.72" 103°33’ 25.90" 1470
36 J36 Celaya 2010 (46) Tamazula 20°0’ 58.77" 104°3’ 3.71" 929
37 J37 Celaya 2010 (47) Techaluta 20°4’ 40.19" 103°33’ 28.47" 1486
38 J38 Celaya 2010 (48) Tamazula 20°1’ 13.20" 104°3’ 8.47" 938
39 J39 Celaya 2010 (49) Zapotitlan 19°32’ 58.41" 103°49’ 13.04" 1098
40 J40 Ancho de color Atengo 20°16’ 16.23" 104°14’ 40.43" 1425
41 J41 Ancho blanco Atengo 20°15’ 58.93" 104°14’ 25.38" 1406
42 J42 Elotes occidentales Atengo 20°16’ 13.88" 104°14’ 29.07" 1432
43 J43 Amarillo Varieties Tapalpa 19°57’ 11.55" 103°45’ 50.05" 2114
44 J44 Dulce de jalisco Navidad, Mascota 20°31’ 36.12" 104°46’ 29.61" 1236
45 J45 Amarillo Atengo 20°43’ 3.65" 103°7’ 12.37" 1700
46 J46 Coamilero Atengo 20°16’ 18.50" 104°14’ 39.88" 1426
47 J47 Tabloncillo perla Luis A. Arciga, Atengo 20°16’ 36.77" 104°13’ 53.33" 1449
48 J48 Bofo Atengo 20°16’ 30.78" 104°13’ 55.47" 1440
49 J49 Tabloncillo pequeño Alista, San Gabriel 19°37’ 53.66" 103°47’ 12.89" 1344
50 J50 Maíz dulce de Jalisco Alista, San Gabriel 19°37’ 55.96" 103°47’ 34.75" 1338
51 J51 Maíz dulce de Jalisco Alista, San Gabriel 19°38’ 7.92" 103°46’ 55.58" 1369
52 J52 Maíz dulce de Jalisco Alista, San Gabriel, 19°37’ 46.56" 103°47’ 35.42" 1317
53 J53 Amarillo de ocho Plan de las Flores 19°44’ 58.48" 103°45’ 35.22" 1293
54 M1 Argentino Buenavista 19°11’ 55.24" 102°35’ 16.77" 432
55 M2 Argentino Periban 19°30’ 45.19" 102°25’ 22.86" 1686
56 M3 Argentino Cotija 19°47’ 50.68" 102°41’ 27.85" 1649
57 M4 Argentino Villamar 20°1’ 17.44" 102°35’ 24.18" 1571
58 M5 Argentino Jocotepec 20°16’ 42.93" 103°25’ 37.81" 1537
59 M6 Argentino Vista Hermosa 19°45’ 20.62" 102°37’ 35.35" 1625
60 M7 Argentino Pajacuaran 20°7’ 5.54" 102°33’ 2.75" 1527
61 M8 Argentino Venustiano Carranza 20°7’ 6.49" 102°39’ 36.33" 1530
62 M9 Argentino Tanganmandapio 19°57’ 8.47" 102°26’ 38.89" 1713
63 M10 Argentino Cotija 19°47’ 57.64" 102°42’ 3.65" 1717
64 M11 Celaya Cotija 19°48’ 0.99" 102°42’ 11.61" 1717
65 M12 Celaya Huaniqueo 19°17’ 59.68" 101°40’ 42.18" 2273
66 M13 Celaya Huaniqueo 19°18’ 2.46" 101°41’ 12.31" 2276
67 M14 Chalqueño Epitacio Huerta 20°8’ 10.63" 100°17’ 4.45" 2473
68 M15 Chalqueño Angangueo 19°36’ 33.89" 100°17’ 33.98" 2604
69 M16 Chalqueño Ocampo 19°35’ 3.43" 100°20’ 39.46" 2296
70 M17 Conico Morelos 18°40’ 46.67" 99°6’ 4.78" 951
71 M18 Conico Morelos 19°13’ 10.75" 101°42’ 24.42" 1960
72 M19 Conico Morelos 19°13’ 11.96" 101°42’ 9.11" 1959
73 M20 Conico Huiramba 19°32’ 30.98" 101°26’ 7.10" 2173
74 M21 Conico Patzcuaro 19°30’ 19.67" 101°37’ 47.10" 2194
75 M22 Conico Patzcuaro 19°31’ 15.74" 101°37’ 21.50" 2097
76 M23 Elotes occidentales Caurio 19°53’ 33.42" 101°49’ 28.86" 2164
77 M24 Elotes occidentales Caurio 19°53’ 49.57" 101°49’ 59.41" 2126
78 M25 Elotes occidentales Caurio 19°53’ 36.49" 101°49’ 47.83" 2142
79 M26 Elotes occidentales Caurio 19°53’ 27.89" 101°49’ 28.56" 2161
80 M27 Elotes occidentales Caurio 19°54’ 16.98" 101°48’ 48.50" 2250
81 M28 Ancho Charapan 19°38’ 43.64" 102°14’ 37.76" 2273
82 M29 Ancho Tlajomulco 20°28’ 28.02" 103°26’ 18.97" 1590
83 M30 Ancho Jungampeo 19°29’ 33.93" 100°29’ 24.99" 1581
84 M31 Ancho Jungampeo 19°29’ 37.21" 100°29’ 17.80" 1603
85 M32 Mushito Madero 19°26’ 44.58" 100°19’ 4.16" 2163
86 M33 Mushito Ario 20°1’ 40.22" 102°20’ 19.06" 1564
87 M34 Mushito Tacambaro 19°13’ 32.38" 101°27’ 19.27" 1576
88 M35 Mushito Salvador 20°18’ 15.04" 103°10’ 47.80" 1538
89 M36 Mushito Chilchota 19°50’ 33.78" 102°6’ 33.43" 1796
90 M37 Ratón tamaulipas Tzizio 19°35’ 3.08" 100°55’ 13.99" 1592
91 M38 Ratón tamaulipas Arteaga 18°21’ 40.01" 102°16’ 55.00" 909
92 M39 Ratón tamaulipas Tepalcatepec 19°11’ 6.01" 102°49’ 45.57" 366
93 M40 Ratón tamaulipas Huetamo 18°38’ 5.56" 100°54’ 44.23" 303
94 M41 Ratón tamaulipas Tuzantla 19°13’ 14.28" 100°34’ 16.00" 603
95 M42 Ratón tamaulipas Ziracuaretiro 19°24’ 41.60" 101°54’ 19.58" 1366
96 M43 Ratón tamaulipas Benito Juarez 19°18’ 49.73" 100°25’ 46.97" 1341
97 M44 Ratón tamaulipas Chinicuila 18°2’ 1.05" 102°12’ 50.64" 55
98 M45 Ratón tamaulipas Tumbiscatio 18°31’ 7.86" 102°22’ 56.99" 955
99 M46 Ratón tamaulipas Coalcoman 18°45’ 56.63" 103°8’ 42.43" 1260
100 M47 Ratón tamaulipas Huacana 18°58’ 6.94" 101°48’ 38.59" 509
101 M48 Tuxpeño Churumuco 19°3’ 48.96" 102°21’ 14.05" 302
102 M49 Tuxpeño Aguililla 18°43’ 53.78" 102°46’ 51.64" 912
103 M50 Tuxpeño Coalcoman 18°46’ 2.68" 103°8’ 39.19" 1257
104 M51 Tuxpeño Tiquicheo 18°54’ 3.98" 100°44’ 39.38" 404
105 M52 Tuxpeño Tepalcatepec 19°10’ 15.83" 102°51’ 10.16" 373
106 M53 Tuxpeño Tepalcatepec 19°10’ 4.51" 102°50’ 39.39" 357
107 M54 Vandeño Turicaro 19°34’ 10.17" 101°56’ 4.08" 2370
108 M55 Vandeño San Lucas 18°34’ 33.51" 100°47’ 14.59" 298
109 M56 Vandeño San Lucas 18°34’ 45.81" 100°47’ 1.00" 317
110 M57 Zamorano amarillo Penjamillo 20°4’ 26.01" 101°56’ 16.43" 1795
111 M58 Zamorano amarillo Penjamillo 20°4’ 25.64" 101°56’ 18.32" 1800
112 M59 Zamorano amarillo Penjamillo 20°4’ 22.27" 101°56’ 19.08" 1792
113 M60 Zamorano amarillo Penjamillo 20°4’ 25.92" 101°56’ 21.25" 1806
114 M61 Tabloncillo San Juanito 19°40’ 28.27" 101°15’ 5.32" 1895
115 M62 Tabloncillo Tumbiscatio 18°31’ 7.35" 102°22’ 28.58" 919
116 M63 Tabloncillo Chinicuila 18°1’ 53.26" 102°12’ 49.82" 34
117 M64 Tsiri charapiti Patzcuaro 19°30’ 42.45" 101°35’ 26.32" 2285
118 M65 Tsiri charapiti Tingambato 19°29’ 59.91" 101°51’ 33.40" 1945
119 M66 Elotes conicos Tingambato 19°30’ 19.65" 101°51’ 38.13" 1955
120 M67 Elotes conicos Tingambato 19°30’ 6.30" 101°51’ 36.04" 1949
121 M68 Elotes conicos Tingambato 19°29’ 33.01" 101°50’ 58.55" 1968
122 M69 Elotero sinaloa Buenavista 19°12’ 11.08" 102°35’ 51.87" 453
123 M70 Elotero sinaloa Aguililla 18°44’ 9.44" 102°46’ 24.09" 909
124 M71 Elotero sinaloa Arteaga 18°21’ 17.52" 102°16’ 43.37" 856
125 M72 Elotero sinaloa Tacambaro 19°13’ 25.94" 101°27’ 20.50" 1569
126 M73 Elotero sinaloa Aquila 18°36’ 3.48" 103°29’ 48.02" 273
127 M74 Elotero sinaloa Coahayana 18°51’ 1.77" 103°37’ 12.58" 46
128 M75 Elotero sinaloa Chinicuila 18°2’ 6.06" 102°13’ 4.91" 63
129 M76 Elotero sinaloa Tamazula 19°34’ 51.97" 102°27’ 6.88" 1367
130 M77 Elotero sinaloa Tecatitlan 19°21’ 48.78" 103°1’ 6.03" 801
131 M78 Elotero sinaloa Jilotlan 19°22’ 15.71" 103°0’ 44.48" 754
132 M79 Elotero sinaloa Paramo 19°22’ 43.12" 102°1’ 38.35" 1589
133 M80 Reventador Aquila 18°36’ 8.32" 103°30’ 18.21" 197
134 M81 Reventador Aquila 18°35’ 50.92" 103°30’ 28.31" 233
135 M82 Reventador Aquila 18°35’ 33.14" 103°30’ 29.07" 190
136 M83 Reventador Aquila 18°35’ 38.66" 103°30’ 0.93" 242
137 M84 Reventador Aquila 18°36’ 14.80" 103°29’ 59.85" 276
138 M85 Arrocillo Aporo 19°39’ 53.63" 100°24’ 33.59" 2292
139 M86 Arrocillo Angangueo 19°36’ 35.63" 100°17’ 30.43" 2616
140 M87 Arrocillo Zitacuaro 19°26’ 55.95" 100°19’ 59.13" 2132
141 M88 Arrocillo Ocampo 19°35’ 38.35" 100°20’ 26.80" 2320
142 M89 Arrocillo Ocampo 19°35’ 31.45" 100°20’ 48.17" 2304
143 M90 Perepecha Ocampo 19°35’ 14.77" 100°20’ 43.80" 2300
144 M91 Perepecha Ocampo 19°34’ 59.68" 100°20’ 47.52" 2287
145 M92 Dulce Ocampo 19°34’ 48.96" 100°20’ 58.47" 2275
146 M93 Dulce Ocampo 19°34’ 34.88" 100°21’ 5.35" 2278
147 M94 Dulce Ocampo 19°34’ 36.47" 100°20’ 43.99" 2292
148 M95 Dulce Ocampo 19°34’ 31.59" 100°20’ 28.88" 2326
149 M96 Dulce Ocampo 19°34’ 25.16" 100°20’ 19.39" 2340
150 O1 tuxpen San Jose Chiltepec 17°57’ 17.68" 96°9’ 18.15" 51
151 O1 tuxpen. . .olotil San Jose Chiltepec 17°57’ 14.59" 96°9’ 30.96" 53
152 O3 tuxpen. . .tepeci Valle Nacional 17°45’ 44.92" 96°13’ 12.70" 61
153 O4 tepeci. . .dzitba Valle Nacional 17°48’ 37.49" 96°13’ 26.59" 50
154 O5 tepeci San Juan Lalana 17°27’ 10.45" 95°45’ 59.76" 249
155 O6 olotil San Juan Lalana 17°27’ 0.35" 95°46’ 2.01" 208
156 O7 hibrido tuxpen Santiago Yaveo 17°19’ 49.25" 95°41’ 57.85" 339
157 O8 olotil 8 Santiago Yaveo 17°19’ 46.67" 95°42’ 55.07" 218
158 O9 tepeci. . .zapagr San Juan Guichicovi 16°59’ 22.77" 95°1’ 15.84" 108
159 O10 zapagr. . .olotil San Juan Guichicovi 16°58’ 40.64" 95°1’ 5.03" 121
160 O11 tepeci. . .tuxpen San Juan Cotzocon 17°9’ 36.23" 95°46’ 40.41" 1408
161 O12 tepeci Santiago Yaveo 17°19’ 47.81" 95°40’ 9.59" 339
162 O13 olotil. . .zapagr Santiago Yaveo 17°20’ 8.96" 95°40’ 41.55" 346
163 O14 chalou. . .bolita Nochistlan 17°28’ 12.90" 97°16’ 23.45" 2052
164 O15 chalou Nochistlan 17°27’ 40.46" 97°16’ 2.89" 2046
165 O16 bolita Nochistlan 17°26’ 55.85" 97°14’ 51.77" 2055
166 O17 bolita conico Nochistlan 17°31’ 19.09" 97°16’ 44.99" 2090
167 O18 connor. . .pepiti Nochistlan 17°30’ 32.38" 97°16’ 46.06" 2082
168 O19 bolita San Andres Andua 17°26’ 52.71" 97°18’ 11.45" 2055
169 O20 bolita San Andres Andua 17°26’ 9.44" 97°17’ 36.60" 2048
170 O21 bolita San Andres Andua 17°27’ 10.80" 97°16’ 2.49" 2039
171 O22 chalou La Paz 17°16’ 51.35" 97°20’ 25.23" 2221
172 O23 chalou La Paz 17°17’ 0.92" 97°20’ 14.93" 2178
173 O24 chalou. . .bolita San Juan Diuxi 17°17’ 6.84" 97°22’ 31.82" 2316
174 O25 chalou 9 San Juan Diuxi 17°17’ 0.14" 97°22’ 49.39" 2472
175 O26 bolita San Pedro Topiltepec 16°39’ 46.52" 96°17’ 16.90" 922
176 O27 chalou Santo Domingo Yanhuitlan 17°31’ 20.43" 97°20’ 13.34" 2143
177 O28 bolita. . .chalou Santo Domingo Yanhuitlan 17°32’ 16.36" 97°20’ 53.48" 2182
178 O29 tepeci. . .tuxpen Pinotepa de Don Luis 16°25’ 23.51" 97°59’ 11.91" 435
179 O30 tepeci. . .olitill San Juan Colorado 16°27’ 22.17" 97°57’ 29.96" 447
180 O31 tuxpen. . .olotill Pinotepa de Don Luis 16°25’ 37.07" 97°57’ 43.71" 427
181 O32 olotil 9 San Pedro Jicayan 16°26’ 51.50" 98°1’ 26.79" 336
182 O33 tepeci. . .olotill San Pedro Jicayan 16°27’ 15.94" 98°1’ 19.89" 348
183 O34 tepeci. . .tuxpen San Pedro Jicayan 16°26’ 36.04" 98°1’ 8.91" 287
184 O35 olotil 7 San Pedro Jicayan 16°27’ 40.02" 98°0’ 45.03" 394
185 O36 olotil 8 San Miguel Tlacamama 16°25’ 10.33" 98°3’ 36.81" 276
186 O37 tuxpen San Miguel Tlacamama 16°24’ 38.92" 98°3’ 35.07" 306
187 O38 tuxpen. . .fasciado Santiago Pinotepa Nacional 16°11’ 1.35" 97°58’ 6.80" 16
188 O39 tuxpen. . .olotill Santa Maria Tonameca 15°44’ 38.05" 96°33’ 9.85" 31
189 O40 olotill 7 Santa Maria Tonameca 15°44’ 30.90" 96°33’ 1.71" 28
190 O41 tuxpen. . .tepeci Santa Maria Tonameca 15°44’ 58.27" 96°32’ 27.13" 32
191 O42 tuxpen. . .olotill San Pedro Mixtepec 15°59’ 37.02" 97°5’ 30.37" 310
192 O43 olotil 9 Pinotepa de Don Luis 16°25’ 11.27" 97°58’ 31.62" 442
193 O44 tuxpeño San Meteo Sindihui 16°59’ 58.07" 97°20’ 55.73" 1484
194 O45 tuxpeño San Meteo Sindihui 17°0’ 26.56" 97°21’ 8.24" 1461
195 O46 tuxpeño San Meteo Sindihui 17°0’ 1.51" 97°21’ 9.48" 1471
196 P1 Cacahuacintle Chignahuapan 19°50’ 44.87" 98°1’ 25.64" 2268
197 P2 Conico Amarillo Zacatlan 19°56’ 9.52" 97°56’ 39.16" 2032
198 P3 Arrocillo San Nicolas Buenos Aires 18°29’ 43.52" 97°25’ 42.18" 1687
199 P4 Conico Amarillo San Martin Texmelucan 19°17’ 42.29" 98°26’ 24.18" 2263
200 P5 Palomero Blanco Tetela de Ocampo 19°48’ 46.58" 97°48’ 16.33" 1759
201 P6 Chalqueño Aljojuca 19°5’ 55.26" 97°32’ 20.83" 2444
202 P7 Elotes Conicos Tlachichuca 19°6’ 46.89" 97°24’ 39.80" 2639
203 P8 Conico Blanco San Juan Tianguismanalco 18°56’ 5.44" 98°27’ 38.26" 1951
204 P9 Chalqueño Tepatlaxco 19°4’ 16.79" 97°58’ 11.54" 2370
205 P10 Elotes Conicos Chalchicomula de Sesma 18°57’ 2.17" 98°12’ 44.96" 2071
206 P11 Cacahuacintle Tlachichuca 19°7’ 35.00" 97°25’ 18.39" 2588
207 P12 Olotillo Xicotepec 18°56’ 53.77" 98°15’ 36.60" 2098
208 P13 Tuxpeño Francisco Z. Mena 18°32’ 9.70" 98°30’ 10.43" 1210
209 P14 Amilaceo Tetela de Ocampo 19°49’ 24.79" 97°48’ 41.60" 1698
210 P15 Conico Amarillo Tepatlaxco 19°4’ 49.67" 97°57’ 38.96" 2390
211 P16 Pepitilla Morado Atlixco 18°54’ 4.80" 98°25’ 49.97" 1826
212 P17 Ancho Atlixco 18°53’ 58.65" 98°27’ 6.57" 1862
213 P18 Ancho Cohuecan 18°46’ 56.70" 98°42’ 58.81" 1706
214 P19 Vandeño Albino Zertuche 18°1’ 3.30" 98°32’ 3.45" 1313
215 P20 Pepitilla Blanco Tochimilco 18°53’ 7.39" 98°34’ 34.34" 2075

DNA extraction, PCR amplification and detection of transgenes in vegetal material

Seeds from each collected variety were planted and germinated to obtain foliar tissue for GMO-DNA analyses. Polystyrene trays were filled with sterile forest soil and substrate (peat-moos) in a 6:4 ratio. After, a group of 10 seeds of each maize variety were planted. At 14 days after plantlet emergence, leaf tissue from 10 germinated seeds was cutting in mass and stored at 4 °C. For DNA isolation was used the method proposed by Graham et al. (1995). DNA integrity was determined by electrophoresis in 1.5% agarose gel and DNA quality was estimated in an Epoch Microplate Spectrophotometer with the Gen5 1.11 software. A Polymerase Chain Reaction (PCR) was performed with each DNA sample composite to amplify eight accompanying sequences (Table 2) and nine transgenic events (Table 3), in this case, specific primers and specific amplification temperatures for each of these sequences were used. Most of the published studies analyzed one or a few transgenic sequences and, in some cases, only a few samples of maize varieties and most of the studies were concentrated in Oaxaca (Mercer and Wainwright 2008). The PCR amplified segments were visualized using agarose gel electrophoresis (1.5%). The molecular markers of 50bp and 100bp DNA ladder (Invitrogen) were used as reference for determination of amplified segments size. In addition, the different amplified segments were sequenced to corroborate the identity of the amplified sequence.

Table 2 Target sequence, primer sequence, sequence size, and annealing temperature used during PCR, for detection of accompanying transgenic sequences. 

Target sequence Primer sequence Sequence size (bp) Annealing temperature (°C)
ubi [25] F-5’-gctaacttgccagtgtttctctttgg-3’ 220 55
R-5’-ggctggcattatctactcgaaacaag-3’
35 s [24] F-5’-gctcctacaaatgccatca-3’ 238 60
R-5’-actgcgtgttagggtgatag-3’
bar [26] F-5’-gcacagggcttcaagagcgtggtc-3’ 177 55
R-5’-gggcggtaccggcaggctgaa-3’
ntpII [26] F-5’-gaggctattcggctatgact-3’ 271 64
R-5’-aaggtgagatgacaggagat-3’
uidA [27] F-5’-ggtgggaaagcgcgttacaag-3’ 150 55
R-5’-accgccttcgttgcgcatttg-3’
luc [28] F-5’-cgccaaaaacataaagaaaggc-3’ 450 64
R-5’-tgtccctatcgaaggactctgg-3’
ocs [27] F-5’-ctcgagctgctttaatgagatatgcg-3’ 120 55
R-5’-tctagactgctgagcctcgacatgttg-3’
nos [26] F-5’-gaatcctgttgccggtcttg-3’ 125 57
R-5’-gcgggactctaatcataaaaacc-3’

Table 3 Target gene, primer sequence, sequence size, and annealing temperature used during PCR for detection of transgenic events. 

Gene Primer sequence Sequence size (bp) Annealing temperature (°C)
cry 3a F-5’-acatgcatgcattaactagaaagtaaagaagtag-3’ 479 62.6
R-5’-acatgcatgcaagcttacagagaaatacacgaggg-3’
cry2a F-5’-gctctagaataggaggaaaagattttatgctaaaa-3’ 850 62.6
R-5’-acgcgtcgacaaatatctagttttatattaa-3’
cry 1e F-5’-ggatcccatatggagatagtg-3’ 756 64
R-5’-cgcggatcctatctagaatcgtaatt-3’
ec F-5’-ccagtctgttgacctggttgt-3’ 239 64.7
R-5’-tttctgcagatgtcaacgtattctatacc-3’
cry11a F-5’-acatgcatgcagtcatgttagcacaagagga-3’ 850 62.6
R-5’-acatgcatgctttaggtctttaaaaattaga-3’
Accasa F-5’taggactggtaccgtaaagcagagtaacacaaggtcag-3’ 514 64.7
R-taggactctcgagagtctttcggaacctcacaccataagg-3’
Als F-5’-gggttacgcacgcgccaccgg-3’ 397 64
R-5’-ggctgatcccagtcaggtatc-3’
cry 1ab F-5’-accatcaacagccgctacaacgacc-3’ 184 70
R-5’-tggggaacaggctcacgatgtccag-3’
Epsps F-5’-tggcgcccaaagcttgcatggc-3’ 356 62
R-5’-ccccaagttcctaaatcttcaagt-3’

Determination the level of introgression of transgenes into maize varieties

The level of introgression of transgenic event and accompanying sequence into local maize varieties which were planted as not biotech crops was determined in percent, in respect to varieties with presence of GMO into its genome vs total number of analyzed maize varieties in each Mexican State.

Statistical analysis

The PCR amplified bands of transgenic inserts were coded as absent (0) and present (1), then these values were summarized and employed for all percentage calculations. In addition, categorical analyses (tables SxR) were performed using the SAS software (9.0 version).

Results

Collection of maize seed

Each collection site of maize varieties was georeferenced on a map (Figure 1). From 215 maize seed samples, 24.65% were from Jalisco, 44.65% from Michoacán, 21.39% from Oaxaca and 9.3% from Puebla.

Figure 1 Geo-referential distribution for the collection sites of maize varieties in the Jalisco, Michoacán, Oaxaca and Puebla States. 

Detection of transgenic sequences in plant tissue

In this study, it was only detected the presence of the cry1Ab transgenic event in all the maize varieties collected in the Mexican Central Region, and the ntpII accompanying sequence only was detected in Michoacan and Jalisco; which suggest that local maize varieties from these Mexican States are contaminated with transgene insert.

Estimate of maize contamination frequencies

Only the number of varieties positive for the transgenes cry1Ab and ntpII presence were included in the statistical analysis. In this analysis about frequency of these transgenic sequences present in the maize varieties were detected highly significant differences (P < = 0.01) (Table 4), the frequency rate for the cry1Ab gene was 41%, while the frequency rate for the ntpII sequence was 9.7%, in this analysis Q value was 56.2661 which was strongly significant and indicated that both frequencies are different. One explanation may be that during transformation of plants with the cry1Ab gene, different marker genes are utilized which may be different to ntpII.

Table 4 Statistical values of the categorical analysis in SxR tables for the presence of transgenic sequences in maize varieties in Mexico. 

Statistic df Value Probability
Chi-square 1 56.3966 <0.0001
Likelihood Ratio chi-square 1 59.7029 <0.0001
Continuity Adj. chi-square 1 54.7501 <0.0001
Mantel-Haenszel Chi-square 1 56.2661 <0.0001
Phi Coefficient -0.3613
Contingency Coefficient 0.3398
Cramer’s V -0.3613

The frequency of transgenic events presents in to the maize varieties from Puebla, Oaxaca, Jalisco and Michoacán, are shown in Table 5. The present study focused on detect transgenic events and accompanying sequences into maize varieties by PCR and using seeds collected of local maize varieties from Puebla, Jalisco, Michoacán and Oaxaca States, allowed to detecting the presence of the cry1Ab transgenic gene and the presence of the ntpII accompanying sequence in the maize varieties (Table 5). The localities with presence of the cry1Ab transgenic event and accompanying sequence ntpII in the maize populations are described in Table 6.

Table 5 Frequency (%) of transgenic events transferred to the maize varieties collected in Puebla, Oaxaca, Jalisco and Michoacán States. 

Transgenic sequence non- introgressed Genotypes Percent Introgressed Genotypes Percent Total
cry1Ab 127 58.80 89 41.20 216
ntpII 195 90.28 21 9.72 216

Table 6 Localities with presence transgenic event (cry1Ab) and accompanying sequence (ntpII) in maize varieties collected from Jalisco, Michoacán, Oaxaca and Puebla States. 

Varieties corn Varieties corn
Key Name Locality Cry1Ab ntpII Key Name Locality Cry1Ab ntpII
J11 Celaya 2010(15) San Juan de los Lagos 1 0 M91 Perepecha Ocampo 1 0
J13 Celaya 2010(17) Lagos de Moreno 1 1 M92 Dulce Ocampo 1 0
J14 Celaya 2010(18) Lagos de Moreno 1 1 M93 Dulce Ocampo 1 0
J21 Celaya 2010(26) Mazamitla 1 0 M94 Dulce Ocampo 1 0
J24 Celaya 2010(29) Tala 1 0 M95 Dulce Ocampo 1 0
J28 Celaya 2010(35) Sayula 1 0 M96 Dulce Ocampo 1 0
J29 Celaya 2010(37) Sayula 1 0 O1 Tuxpen San Jose Chitepec 1 0
J30 Celaya 2010(38) Gomez Farias 1 0 O10 zapagro-olotillo San Juan Guichicovi 1 0
M13 Celaya Huaniqueo 1 1 O11 tepeci..tuxpen San Juan Cotzocon 1 0
M14 Chalqueño Epitacio Huerta 1 1 O12 tepeci Santiago Yaveo 1 0
M15 Chalqueño Angangueo 1 1 O13 olotil. . .zapagr Santiago Yaveo 1 0
M16 Chalqueño Ocampo 1 1 O15 Chalou Nochistlan 1 0
M17 Conico Morelos 1 1 O16 Bolita Nochistlan 1 0
M18 Conico Morelos 1 1 O17 Bolita conico Nochistlan 1 0
M19 Conico Morelos 1 0 O18 connor. . .pepiti Nochistlan 1 0
M21 Conico Patzcuaro 1 1 O19 Bolita San Andres Andua 1 0
M40 Ratontamaulipas Huetamo 1 1 O2 Tuxpen. . .olotil San Juan Chitepec 1 0
M48 Tuxpeño Churumuco 1 0 O20 Bolita San Juan Andua 1 0
M49 Tuxpeño Aguililla 1 0 O26 Bolita San Pedro Topiltepec 1 0
M51 Tuxpeño Tiquicheo 1 0 O27 Chalou Santo Domingo Yanhuitlan 1 0
M52 Tuxpeño1 0Tepalcatepec 1 0 O29 tepeci. . .tuxpen Pinotepa de Don Luis 1 0
M53 Tuxpeño Tepalcatepec 1 0 O4 tepeci. . .dzitba Valle Nacional 1 0
M66 Elotes Conicos Tingambato 1 1 O41 Tuxpen. . .tepeci Santa maria Tonameca 1 0
M67 Elotes Conicos Tingambato 1 0 O42 Tuxpen. . .olotil San Pedro Mixtepec 1 0
M68 Elotes Conicos Tingambato 1 1 O43 Olotil9 Pinotepa de Don Luis 1 0
M69 Elotero Sinaloa Buenavista 1 1 O45 Tuxpeño San Meteo Sindihui 1 0
M70 Elotero Sinaloa Agulilla 1 0 O46 Tuxpeño San Meteo Sindihui 1 0
M72 Elotero Sinaloa Tacambaro 1 0 O7 Hibrid Tuxpen Santiago Yaveo 1 0
M74 Elotero Sinaloa Coahayana 1 0 O8 Olotil 8 Santiago Yaveo 1 0
M75 Elotero Sinaloa Chinicuila 1 0 O9 Tepeci. . .zapagr San Juan Guichicovi 1 0
M76 Elotero Sinaloa Tamazula 1 1 P1 Cacahuacintle Chingnahuapan 1 0
M77 Elotero Sinaloa Tecatitlan 1 1 P2 Conico Amarillo Zacatla 1 0
M78 Elotero Sinaloa Jilotlan 1 1 P3 Arrocillo San Nicolas Buenos Aires 1 0
M79 Elotero Sinaloa Paramo 1 1 P4 Conico Amarillo San Martin Texxmelucan 1 0
M80 Reventador Aquila 1 1 P6 Chalqueño Aljojuca 1 0
M81 Reventador Aquila 1 0 P7 Elotes Conicos Tlachichuca 1 0
M82 Reventador Aquila 1 0 P8 Conico Blanco San Juan Tiangusmanalco 1 0
M83 Reventador Aquila 1 0 P10 Elotes Conicos Chalchicomula de Sesma 1 0
M84 Reventador Aquila 1 0 P12 Olotillo Xicotepec 1 0
M85 Arrocillo Aporo 1 0 P14 Amilaceo Tetela de Ocampo 1 0
M86 Arrocillo Zitacuaro 1 0 P18 Ancho Cohuecan 1 0
M88 Arrocillo Ocampo 1 0 P19 Vandeño Albino Zertuche 1 0
M89 Arrocillo Ocampo 1 0 P20 Pepetilla Blanco Tochimilco 1 0
M90 Perepecha Ocampo 1 1

Introgression of transgenes into maize varieties

According to the presence of cry1Ab into the genome of the sampled maize varieties from these four Mexican states, it was observed that maize varieties grown as non-biotech crops from Puebla State have the highest levels (70%) of contamination o introgression of transgenes inserts into their genomes, followed by maize variety samples from Oaxaca with 52.17%, Michoacán maize samples with 44.79% and Jalisco maize samples with 15.09%, respectively. While, the presence of accompanying sequence ntpII was only detected in the Michoacán and Jalisco maize samples in 89.47 and 10.52%, respectively (Figure 2).

Figure 2 Level of introgression (Percentage) of the transgene event cry1Ab in Mexican maize varieties from Puebla, Oaxaca, Jalisco and Michoacán states. 

Discussion

Collection of maize seed

Although some studies have confirmed the contamination of native maize by transgenic events, these studies considered a low number of samples, for example, De-Ita (2012) indicates the use of samples from 22 localities, while The National Commission for the Knowledge and Use of Biodiversity (Conabio) confirmed the presence of transgenes from 3 to 10% in 15 locations. Another study for the determination of transgenes carried out by Serratos-Hernández et al. 2007 is based on a sample of 25 communities. The present study considered a greater number of localities (215) from 4 Mexican States, which allows to have a better perspective of the contamination of native maize by transgenic segments.

Detection of transgenic sequences in plant tissue

These results confirm the introgression of transgenes into maize varieties as indicated by (Quist and Chapela 2001, Cleveland et al. 2005, Serratos-Hernández et al. 2007, Mercer and Wainwright 2008, Piñeyro et al. 2009, Orozco-Ramírez et al. 2016, Rendón-Aguilar et al 2019) who reported the presence of transgenic DNA in native varieties of maize grown in remote mountains of Oaxaca, this place is part of the center of origin and diversification of the crop in Mexico.

Estimate of maize contamination frequencies

The high detection rate of the cry1Ab transgenic event in the maize varieties populations implies that protective measures must be taken in the short term to produce maize varieties seeds free of these transgenic segments. This detection is controversial because in Mexico, it is not allowed to grow commercially maize transgenic cultivars, only at an experimental level (García and Toscana 2016, Ortega-Villegas et al. 2018, Lopez-Hernandez 2020), precisely, for preservation of biodiversity of the native maize, because Mexico is considered a center of origin and diversity of this commodity (Lohn et al. 2021).

Introgression of transgenes into maize varieties

This level of introgression of transgenes into the tested maize varieties could be considered very high, as it is determined in a specific way, what was found for each state (Figure 2), and assuming that the states with the lowest experimental seeding (Puebla and Oaxaca) are those with the greater genetic contamination, having thus that 70% of the varieties collected in Puebla state presented residues of the cry1Ab gene; while, 52% of the maize collected in Oaxaca were positive for the cry1Ab gene. On the other hand, in these states, not varieties were detected contaminated with accompanying sequences.

The cry1Ab gene was detected in 15% of the maize varieties collected in Jalisco, and 4 out of 53 samples collected were found to be introgressed with the accompanying ntpII sequence. While 44% of the varieties collected in Michoacán were observed to have the cry1Ab gene, and 17.7% of the samples collected in this state showed the accompanying ntpII sequence. The presence of transgenic events in maize varieties could have an cultural, economic, and social impact, on continuity of indigenous and peasant peoples as refer (Sánchez and Romero 2018, Ibarrola-Rivas et al. 2020), who point out the importance of this area on maize conservation, it is in this territory where the milpa takes place, and at the same time, the milpa is part of the territory; and with the cultural and natural characteristics of the territory, particular milpa are configured. Therefore, the contamination of maize or its substitution by transgenic varieties is not limited to changes in maize as a source of food, but also implies negative repercussions for farmers in the milpa and in the territory, increasing the risk to their cultural continuity. Milpa is defined as agroecosystem conformed by polyculture, which is a dynamic space of genetic resources (Ortiz et al. 2014, González and Reyes 2014, Fonteyne et al. 2023). CCA (2004) mentioned that in Mexico, maize is not only a commercial commodity, it is the base of Mexican diet and constitutes an integral expression of the relation between nature and culture, from this relation depends the subsistence of a great part of the Mexican rural population, and through this relation, the social tissue and people of these communities and diversity conservation are fortified.

Milpa is not only the space where maize, and other plant species are sown, but it is also a space for linguistic, cultural, symbolic, spiritual, social, and economical activities and food (Agapito-Tenfen et al. 2017, Ibarrola-Rivas et al. 2020), is more than a farming technique, it is an agroecosystem in which farmers of Mesoamerican origin cultivate dozens of comestible and medicinal herbs, along with fruit and timber trees. For these communities, the most important thing is that the diversity of the maize germplasm can be lost. Year after year, the farmers keep the best seeds for planting in the following season, passing the knowledge of selection of them, the preparation of the land and the accumulation of information on the weather, among other elements, to the next generation (Sánchez and Romero 2018). Maize varieties genetic diversity offers specialized genotypes which have demonstrated capacity of adaptation to different environments, pest and disease resistance, and satisfy divers demands for culinary, artisanal or industrial uses; this diversity is a key factor for the Mexican food security (WHO 2015).

It is considered that maize is a continuous process of domestication, since it depends completely on the farmer, who through selection has favored the survival, and reproduction of phenotypes that have advantageous characteristics to be used mainly as food for humans, and to date represent a total of 64 native maize races reported for Mexico (Santillán-Fernández et al. 2021). It is also convenient to clarify that natural selection operates during the process of domestication. The domestication process results in Mexico being a center of maize genetic diversity (Santillán-Fernández et al. 2021), and is the Mexicans’ responsibility to preserve this great maize genetic diversity, in addition to conducting selection programs to gather more, and better characters in the plants that will serve as progenitors to the next generation. Agricultural and cultural practices have been very important during the whole process of maize domestication, since each variety have adapted to the specific environment that includes the cultivation method (Guzzon et al. 2021).

Maize is currently important in the diet of Mexicans and for many of them, it is their main source of protein and energy, which can be considered as cheap diet (Erenstein et al. 2022); with an average consumption of 350 g per capita per day in 600 different presentations of maize. Therefore, it has been pointed out that maize requires a special protection regime for genetically modified organisms that can negatively modify the nutritional qualities of this cereal (Brookes and Barfoot, 2016). The genetic contamination by transgenes of the natural ecosystems of Mexico has been documented. Since 2001, there have been isolated reports that indicate the unintentional presence of GM maize (Quist and Chapela 2001, Serratos-Hernández et al. 2007, Mercer and Wainwright 2008, Piñeyro et al. 2009) and there is only low work in Mexico in which the absence of GMOs was reported in maize (Cleveland et al. 2005, Rendón-Aguilar et al 2019). Most of the published studies analyzed one or a few transgenic sequences and, in some cases, only a few samples of maize varieties and most of the studies were concentrated in Oaxaca (Mercer and Wainwright 2008). On the other hand, there are reports that maize shipments imported for consumption have a large percentage of transgenic residues, in addition, the grain is viable. From 29 imported shipments of maize for consumption were analyzed for presence of transgenic residues, all the samples presented at least one transgenic sequence, either an event or an accompanying sequence (Carvajal et al. 2017). So, there is a risk that grains fall during transport, germinate on the sides of roads or railroads, or that farmers take these grains as seed and when they are planted in regions with high genetic diversity of maize, pollen can transfer transgenic genes to the native maize. It is proposed that the information obtained in this work be integrated into the National Program for the Monitoring of Genetically Modified Organisms, which will allow a diagnosis of the current situation in Mexico on the introgression of transgenes to the native maize and will serve as the basis for taking the actions necessary in matters of Biosafety.

Conclusions

The present study reports presence of transgenic events (cry1Ab), and sequences associated with the gene (ntpII) into maize varieties from Puebla, Michoacán, Oaxaca and Jalisco states in about 45% of the sampled localities. Corrective measures must be taken to prevent the contamination of Mexican maize varieties, and to train the varieties producers to clean the out-of-type phenotypes that could be sources of contamination of transgenic genes within the contaminated maize varieties with transgenes.

Acknowledgements

JNSA and MACG thank to the National Council of Science and Technology of Mexico (CONACyT) for the financial support provided during their BSc. studies. Financial support was received from CONACyT through the project “Introgression of transgenes into maize landrace varieties and wild relatives SEMARNAT 2008-01-C01-108421”.

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Received: November 16, 2022; Accepted: July 08, 2023

Corresponding author: raul.rodriguez@uadec.edu.mx

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