Relationships among American popcorn and their links with landraces conserved in a microcenter of diversity

Abstract

This study describes the genetic diversity and the population structure of 66 popcorn landrace collections in a recently discovered microcenter of maize (Zea mays L.) diversity in southern Brazil. Furthermore, we elucidate their phylogenetic relationships with a diverse panel of 575 popcorn populations from 18 countries of American Continent. The germplasm, representing distinct landraces, was genetically characterized as population bulks using single nucleotide polymorphism markers (SNPs). Five main groups were identified for the popcorn germplasm of the southern region of Brazil. This pattern was associated with phenotypic diversity in grain shape and color. The germplasm of the American Continent was structured in nine groups associated with geographical region with significant differences in terms of genetic diversity and expansion capacity or popping expansion (the formation of large flakes after the kernels explode in response to heating). The popping expansion pattern of the American groups displayed a North-South geographical continuum, in which the average values increased with geographical distance from the center of origin in Mexico. The highest averages were obtained for the Lowland groups of South America. These results raise two hypotheses: the first one is the possibility of a continuous evolution of this characteristic, which is popcorn did disperse North - South, but interbreeding with local varieties drove up the diversity of the gene pool, and at the same time allowed more efficient selection on the trait of expansion capacity. The second is the possibility of a second domestication event of Zea mays ssp. mays L., in South America, which would assume an independent origin of popcorn, but not an independent domestication of maize. Both hypotheses would be based on popcorn populations brought from Mexico by human migrations. The germplasm collected in the microcenter of diversity in southern Brazil, most of them originated in the Lowlands of South America, a part of germplasm established phylogenetic relationships closer to the popcorn populations of Brazil collected in the last century. The study contributes to improved understanding of the origin and phylogenetics of this maize group and as such to conservation of those valuable genetic resources and future breeding efforts. This is valuable genetic research which led to better insight into grouping and dispersion of studied genotypes in the target region, but also its place vis-à-vis origin and migration of popcorn genotypes in South America in general.

Introduction

Many studies of maize (Zea mays ssp. mays L.) domestication have generated divergent theories in relation to their center of origin. The unicentric theory supports the occurrence of a single domestication event (Matsuoka et al. 2002; Vigouroux et al. 2008; Warburton et al. 2011; Bedoya et al. 2017), while the multicentric theory advocates the occurrence of multiple domestication events, with the existence of five centers of origin-domestication and four primary centers of diversification, all located in Mexico and Guatemala (Kato et al. 2009). Although the controversy over single versus multiple domestication events of the species is not fully resolved, the unicentric theory brings together a larger set of scientific evidences (anthropological, archaeological and molecular), which supports the idea that maize was domesticated in the Rio Balsas Valley (southern Mexico), from the teosinte populations of the subspecies Zea mays ssp. parviglumis (Matsuoka et al. 2002; Vigouroux et al. 2008; Bedoya et al. 2017). This process would have occurred at least 8700 years before the present—BP (Piperno et al. 2009). In fact, the only consensus regarding maize domestication is the recognition of some form of teosinte as its direct ancestor and human intervention as an indispensable condition for its transformation into the present maize as a result of a progressive evolutionary (Galinat 1988, 1992; Iltis 1972, 1983; Doebley et al. 1983; Doebley 1990; Kato 1984).

In this evolutionary scale, some authors agree that the popcorn type probably corresponds to the first and the lowest level of domestication of the species (Wellhausen et al. 1951; Contreras et al. 2006). These inferences are based on the fact that the popcorns still present some characteristics considered “wild”, such as smaller seed size, greater prolificacy, very rigid pericarp (Ziegler 2001), and, in some races, a pointed grain shape. As some of these kernel characteristics would require an extraordinary effort to grind the grain into flour, their consumption would more likely be in the popped form.

In one of the first studies on the origin of popcorn, Erwin (1950) suggests that popcorn originated from a natural mutation of flint corn, resulting in an endosperm that would expand consistently when subjected to high temperature. Later, Brunson (1955) concluded that the expansion capacity of popcorn is a characteristic controlled by many genes. Currently, a more complex genetic inheritance is the most accepted genetic basis for this feature, considering that the ability to burst is defined not only by one, but by a set of characteristics associated with the grain (Ziegler 2001).

In fact, the expansion capacity of popcorn is related to the rigidity of the pericarp, to the presence of oil and humidity in the grain, which when heated, exert strong pressure on the pericarp, causing it to rupture completely and expose at rapidly expanding endosperm, giving rise to “popcorn” (Ziegler 2001; Soylu and Tekkanat 2007). Other studies have highlighted the composition of the starch and the arrangement of the proteins in the endosperm as important components of the grain expansion (Park et al. 2000, Borras et al. 2006; Soylu and Tekkanat 2007). It was this characteristic of expanding (bursting) due to this set of attributes that made it possible to classify popcorn as a special type within the subspecies Zea mays ssp. mays L (Silva et al. 1993; Ziegler 2001).

At present, it is accepted that popcorn was the result of a more complex human construct, made from the values of grain use, and whose characteristic of expansion capacity may have even been responsible for the beginning of the process of domestication of this species, from the grain of its ancestor (teosinte), which already had the capacity to expand and form “popcorn” (Contreras et al. 2006). Knowing how or by what characteristic the process of domestication happened is precisely one of the great questions still unanswered about the origin of maize.

As far as dispersion is concerned, the consensus is that maize has been rapidly dispersed to other regions of the American Continent since its initial domestication, with archaeological evidence supporting maize cultivation for at least 7707 years BP in Central America (Dickau et al. 2007); 7150 years BP in north of South America (Pearsall and Piperno 1990); and 5200 years BP in south of South America (Hilbert et al. 2017). Many studies have inferred the genetic relationships among the maize races of the Americas, based on the geographic distributions and the dispersion patterns of the crop species and the humans who were consuming it, reconstructing and suggesting possible maize migration routes throughout the American Continent (Matsuoka et al. 2002; Vigouroux et al. 2008; Bedoya et al. 2017). However, none of these studies focused on popcorn, considering that this form of maize probably corresponds to the earliest primary stage of domestication, as previously described. Popcorn has historically received little attention in genetic diversity studies, and the dispersal of the maize on the continental geographic scale, when studied, has been based on geographically restricted diversity panels, with no representation of the popcorn germplasm from the lowlands of South America. The lowlands of South America, which includes areas with altitudes below 1500 m (72% of the South American Continent), is considered a secondary center of genetic diversity in maize (Brieger et al. 1958; Paterniani and Goodman 1977).

Studies carried out at the regional level in the lowlands of South America have concluded that popcorn races have peculiarities in terms of genetic diversity, since differences can be detected between populations that are geographically very close, without any physical barriers between them, and are likely to have been generated by special management practices and by human selection (Bracco et al. 2009, 2012). At the micro regional level, recent studies have also demonstrated the same population structure for popcorn populations in southern Brazil. In a diversity microcenter of the Zea genus (which in this study will only be called “diversity microcenter”), located in the far west region of Santa Catarina State (Fig. 1), it was demonstrated that the diversification of new popcorn races is the result of present day human sociocultural activities (Silva et al. 2015, 2016; Costa et al. 2016). Return most of the maize found in this region is popcorn, explained by the high number of popcorn landraces (71% of the mapped total maize) kept mainly by women (≈ 80%) to feed their families (Costa et al. 2016; Silva et al. 2016). The traditional use, associated with the diversity of races and the high number of landraces, constitutes a good genetic source, from which it is possible to obtain indicatives of its dispersion process, as well as to obtain information about the origin of the germplasm of that region.

Fig. 1
figure1

Distribution of 66 popcorn populations of in the municipalities of Anchieta and Guaraciaba, a diversity microcenter in Southern Brazil. Map contour constructed from spatial data retrieved from http://www.diva-gis.org/gdata

Our hypothesis is that popcorn populations in this diversity microcenter are genetically closer to the South American lowland germplasm and that the genetic variation present in the germplasm studied is influenced by geographic factors, which are reflected in the distribution of popcorn diversity and flows migration in the Americas. Therefore, the objectives of this research were (1) to study the genetic diversity and population structure of popcorn in this diversity microcenter, to make inferences about the origin of the popcorn germplasm found there, (2) to verify its phylogenetic relationships with landraces from other regions of the Americas and iii) to understand the overall evolutionary history of popcorn on the American Continent.

Materials and methods

Plant material

The popcorn populations used in this research were obtained from a collection of the genus Zea carried out in 2013 in the municipalities of Anchieta and Guaraciaba in the western most county of the Brazilian state of Santa Catarina (Fig. 1). The selection of the popcorn germplasm for this study was selected based on the results of previous studies Costa et al. (2016) and Vidal et al. (2019). The first identified and mapped 1078 popcorn landrace populations preserved in situ-on farm by farming families. Vidal et al. (2019) established a Core Collection representative of this diversity, based on morphological, agronomic, adaptive, geographic and sociocultural variables, from which a sample of 66 populations was obtained for the present study (Table S1). The popcorns were grown under greenhouse conditions to obtain young leaves for DNA extraction. In addition, a population of teosinte (T2021) from this diversity microcenter was included. This population was classified by Silva et al. (2015) as Zea luxurians, (Durieu and Ascherson) Bird. It was used as the outlier for all subsequent phylogenetic analyses.

To verify the phylogenetic relationships of popcorn populations from the diversity microcenter with other popcorn populations from the Americas and, consequently, to infer the dispersion of this type of maize to southern Brazil, molecular genetic data from 575 accessions (complete passport data are available in Table S2) from the popcorn Base Collection of the Maize Gene Bank (MGB) of the International Maize and Wheat Improvement Center (CIMMYT) were used, from a total of 715 popcorn accessions from the Americas, Asia and Africa. The criteria for choosing the 575 accessions were based on: (1) geographic origin on the American Continent; (2) information on maize race designation; (3) maize race that has the expansion capacity based on the information derived from the “The Races of Maize Booklets” (Wellhausen et al. 1951; Hatheway 1957; Roberts et al. 1957; Brieger et al. 1958; Wellhausen et al. 1958; Grobman et al. 1961; Ramírez et al. 1961; Timothy et al. 1961, 1966; Grant et al. 1963; Paterniani and Goodman 1977) and; (4) representatitive of landrace diversity and geographic range within each country. After analyzing these criteria, the geographic coverage of the selected accessions for the present study (Fig. 2) included the following countries (number of accessions in parentheses) Argentina (128), Mexico (121), Brazil (112), Chile (65), Paraguay (42), Uruguay (24), Ecuador (20), Bolivia (14), Colombia (11), Peru (10), Venezuela (9), Guatemala (8), Costa Rica (4), Guiana (2), Panama (2), Cuba (1), El Salvador (1), United States (1), which in total represent the American gene pool of popcorn for this study. The molecular data were generated by the MASAgro-Biodiversity Project (also known “Seeds of Discovery”) at developed by CIMMYT, whose methodology of DNA extraction and sequencing of the samples was used to obtain the diversity microcenter germplasm information, as described below.

Fig. 2
figure2

Geographic origins of popcorn populations of the American Continent. Map elaborated with the accesses that presented information of the geographical coordinates in the passport data. Map contour constructed from spatial data retrieved from http://www.diva-gis.org/gdata. The same coordinate can represent more than one access

Molecular analyses

For the 66 accessions from the diversity microcenter, DNA was extracted from fresh leaf tissue collected from individual 3-week-old plants grown in the green-house, using a CTAB protocol (Doyle and Doyle 1990). DNA quality and quantity were evaluated by electrophoresis in agarose 1% (w/v) gels stained with SYBR Safe DNA (Invitrogen) by comparison with phage λ molecular size standards and with nanodrop. Each accession was analyzed as a bulk of DNA from 30 individual plants, mixed in equal amounts as described in Reif et al. (2005) and Dubreuil et al. (2006). All accessions were genotyped by the genotyping by sequencing GbS method, according to the protocol developed by Diversity Arrays Technology—DArT (Jaccoud et al. 2001; Elshire et al. 2011; Wenzl et al. 2004; Sansaloni et al. 2011), the same methodology adopted by CIMMYT to genotype the accessions from the germplasm bank. The molecular data of the 575 accessions were shared with the first author by the Project “MASAgro-Biodiversidad” (Seeds of Discovery), developed by CIMMYT.

SNP filtering

In order to obtain high quality data for the statistical analysis, the following criteria were applied for filtering the Single Nucleotide Polymorphisms (SNPs) markers: (1) Call Rate = 1, the proportion of samples for which the genotype call is either ‘1’ or ‘0’, rather than ‘-’ (all markers with missing data have been deleted); (2) RepAvg ≥ 0.85, which means the proportion of replicated technical test pairs for which the marker score is consistent; (3) AvgPIC > 0, the average of the polymorphism information content (PIC) of the reference and SNP allele rows. After filtering, 5898 SNPs markers remained for the accessions of the Americas, 1587 SNPs markers for the landraces collected at the diversity microcenter and 773 SNPs markers for the combined data sets (Americas + diversity microcenter).

Data analysis

Statistical analyses examined the diversity at three geographic levels: (1) only popcorn populations within the diversity microcenter; (2) only the CIMMYT accessions from the American Continent; (3) the combination of both local (diversity microcenter) and regional (CIMMYT).

The genetic structure of molecular data was assessed by principal component discriminant analysis (DAPC). For this, the adegenet package (Jombart 2008) was used in R (R Development Core Team 2015). DAPC consists of an exploratory analysis which determines the most likely number of population groups from a set of SNP markers distributed in the genome. First, a principal component analysis (PCA) is performed and then a discriminant analysis from the estimated PCA scores. The DAPC defines a number of clusters and presents the genetic structure so that variation is minimized within groups and maximized among groups (Jombart et al. 2010). The optimal number of groups was calculated using the K-means method and the Bayesian Information Criterion (BIC), without considering the information on the number of “a priori” groups and without assuming that the groups meet the Hardy–Weinberg equilibrium assumptions or absence of link between loci (Pritchard et al. 2000). A Chi square test (X2) was performed to verify if the formed groups showed distribution pattern in relation orders variables/characteristics. This test aims to verify whether the observed absolute frequency of a variable is significantly different from the expected absolute frequency distribution. To interpret some of the results, we consulted the database of the popcorn farmer interviews from previous studies (Costa et al. 2016; Silva et al. 2016).

A neighbor-joining cluster analysis (Saitou and Nei 1987) was performed with the R statistical package ape (Paradis et al. 2004). To determine the degree of statistical support for different branch points in the phylogenies, we evaluated 1000 bootstrap samples of the data. The phylogenetic trees were formatted with the program FigTree (Rambaut 2008), without rooting. An unrooted tree specifies relationships among taxa and does not define the evolutionary path.

To estimate the genetic diversity of the groups formed by DAPC the expected heterozygosity (Hs) which corresponds to the Nei’s Index was calculated (Nei 1978). The significant differences of the diversity and the expansion capacity (only for groups formed by the 575 popcorn populations from the Americas) among groups were checked through ANOVA. The analyses were performed with the statistical program PAST, version 3.4 (Hammer et al. 2001).

Results

Genetic structure and genetic diversity of popcorn populations within the diversity microcenter in Southern Brazil

The K-means method established that based of the BIC tested the number of groups (K) from 1 to 7, and the optimal K corresponded to five groups (Fig. 3 and Table S3). The DAPC analysis identified genetic structure of the 66 popcorn landraces and the teosinte population 2021T. Considering the five genetic groups (Fig. 4a, b), Group A (GA) consisted of 33 popcorn populations (19 from Guaraciaba and 14 from Anchieta) with a grain shape and color predominantly pointed and white, respectively. Group B (GB) (round and golden grain) was composed of three populations (two from Anchieta and one from Guaraciaba). The Group C (GC) was formed by the teosinto population (2021T) and the 956A popcorn landrace. The Group D (GD) was formed by 12 popcorn populations, with predominantly round shape grain and black color. And lastly the Group E (GE) was formed by 16 popcorn populations (nine from Guaraciaba and seven from Anchieta) with predominantly round shape grain and mixed color (orange, yellow, white and black). The X2 test detected significant difference at 5% probability between grain shape and groups (p < 0.05) and grain color and groups (p < 0.05). A Neighbor-joining cluster analysis (Fig. 5) showed that the groups formed in this analysis were in agreement with the DAPC, with some dispersed occurrences of varieties in distinct groups. The results showed a clear separation between the groups and the formation of five consistent groups. The occurrence of mixtures in genotypes was very low.

Fig. 3
figure3

K optimal (K = 5) for 66 popcorn landraces and teosinte population determined by the K-means method based on the Bayesian Information Criterion (BIC) considering 1587 SNPs markers

Fig. 4
figure4

Principal component discriminant analysis (DAPC) based on 1587 SNPs markers for 66 popcorn landraces and teosinte population. a Scatter plot of the groupings formed by the K-means method. b Density graph according to the groupings established along the first discriminant function obtained in the DAPC

Fig. 5
figure5

Neighbor-joining cluster analysis of 66 popcorn landraces and teosinte population from diversity microcenter in Southern Brazil based on proportion of shared alleles from 1587 SNPs markers. The colors represent the groups formed by DAPC. (Color figure online)

The teosinte and the 956A population were genetically closer to each other and could be considered outliers. In the case of teosinte, this result was expected because it is a wild relative of maize, belonging to another species of the genus Zea, identified by Silva et al. (2015) as Zea luxurians. For the 956A population, based on a search of the “Diversity Census” database, it was discovered that the farmer who conserves this population also manages nearby teosinte populations for fodder for her livestock. The occurrence of gene flow and the formation of interspecific hybrids between maize and teosinte has already been demonstrated by several studies (Fukunaga et al. 2005; Ross-Ibarra et al. 2009; Warburton et al. 2011; Silva et al. 2015). In this way, it could explain the proximity between population 956A and 2021T, as well as the dissimilarity of the first in relation to the other popcorn populations analyzed. The same analyzes were performed excluding the GC group (2021T and 956A), considering that these could be driving so much of the variation and obscuring the relationships of interest. The results shown in Fig. S1 and Table S4 demonstrated that there was no change in the genetic structure of the previously formed groups and therefore subsequent analyzes were performed including the GC.

The genetic diversity (Hs) of the 66 popcorn populations ranged from 0.162 to 0.499, with the highest mean Hs being 0.499, found in the GC group, followed by GE (0.247), GB (0.216), GA (0.204) and GD (0.184). The GC, with the highest diversity have two populations with similar diversity and one of them is teosinte, that reinforces a possible occurrence of gene flow among them. There was a significant difference for the genetic diversity between groups.

Classification of the American Continent popcorn germplasm

The K-means method tested the number of groups from 1 to 58 and the optimal K established based on the BIC corresponded to nine conglomerates (Fig. 6 and Table S5). Thus, the DAPC allowed the identification of the formation of nine genetic clusters—g1, g2, g3, g4, g5, g6, g7, g8 and g9—and to evaluate the genetic structure of these groups, as well as their relationship (Fig. 7a, b). The predominant pattern of separation of the clusters followed the differences in the geographical origin of popcorn populations detected with the X2 test at 5% probability (p < 0.05).

Fig. 6
figure6

K optimal (K = 9) for 575 popcorn populations from American Continent determined by the K-means method based on the Bayesian Information Criterion (BIC) considering 5898 SNPs markers

Fig. 7
figure7

Principal component discriminant analysis (DAPC) based on 5898 SNPs markers for 575 popcorn populations. a Scatter plot of the groupings formed by the K-means method. b Density graph according to the groupings established along the first discriminant function obtained in the DAPC

Table 1 presents the characteristics of each group in relation to the number of popcorn populations, countries and popcorn races. The group g1 was formed almost entirely by populations of South America (with the exception of the four populations of Mexico), most of which are located at altitudes above 1500 m (Table S2). This altitude limit sets the standard highlands (over 1500 m) and lowlands of South America (below 1500 m). The g2 was predominantly made up of Chilean populations, most of them located below 1500 m. The g3 was formed by populations from Brazil, Paraguay and Argentina, with a predominance of populations from Brazil. The g4 was formed by populations of the western Sierra Madre West of Mexico, represented mainly by the Reventador race, a population of Argentina and the only population of the United States. The g5 group was predominantly formed by populations located in Mesoamerica, Central America, and the Caribbean, such as Mexico, Guatemala, El Salvador, Costa Rica, Panama, Colombia, and Venezuela. The g6 conglomerate was formed by populations of the Central Valleys and East of the Sierra Madre Occidental of Mexico, represented in greater proportion by the Arrocillo Amarillo, Arrocillo and Palomero races. The g7 was formed mainly by populations of Argentina, most of which are below 1500 m in altitude. The g8 was formed by populations from Brazil, Paraguay, Argentina and Bolivia. The g9 conglomerate was made up of populations located in the highlands and lowlands of South America, mostly from populations of Argentina.

Table 1 Composition of nine DAPC groups formed from 575 populations of popcorn from the American Continent

The nine groups defined by the DAPC followed the geographical pattern, defined by convention in this article as: Highland South America (g1), Lowland South America–Chile (g2), Lowland South America–Brazil (g3), West of the Sierra Madre Occidental of Mexico (g4), Mesoamerica, Central America and Caribbean (g5), Central Valleys and East of the Sierra Madre Occidental of Mexico (g6), Lowland South America–Argentina (g7), Lowland South America–Paraguay (g8), Intermediate South America Zone (g9).

A neighbor-joining cluster analysis (Fig. 8) showed that the groups formed in this analysis were in agreement with the DAPC, with some dispersed occurrences of varieties in distinct groups. The results showed a clear separation between the groups and the formation of nine consistent groups. The occurrence of mixtures in genotypes was very low.

Fig. 8
figure8

Neighbor-joining cluster analysis of 575 popcorn populations from American Continent and teosinte population based on proportion of shared alleles from 5898 SNPs markers. The colors represent the groups formed by DAPC. (Color figure online)

Genetic diversity and expansion capacity of popcorn populations from American Continent

The mean Hs for the 575 populations of popcorn in the Americas was 0.430, with maximum and minimum values of 0.483 and 0.355, respectively. According to the ANOVA there are significant differences between groups, the highest means Hs were found within the g6, g7 and g9 groups, the smallest were identified within the g3 and g2 groups (Table 2). For the expansion capacity, the mean values ranged from 5.8 to 14.7 (Table 2), according to the ANOVA there are significant differences between groups, all lowland populations have significantly more expansion capacity than those of Mexico and Mesoamerica. The Lowland South America–Chile (g2) and Lowland South America–Paraguay (g8) presented the highest average values, and the group Central Valleys and East of the Sierra Madre Occidental of Mexico (g4), the lowest mean value.

Table 2 Genetic diversity and expansion capacity of nine DAPC groups formed from 575 populations of popcorn from the American Continent

Phylogenetic relationships between groups from Brazilian diversity microcenter and America’s popcorn groups

Figure 9 shows the phylogenetic relationships of the five groups (GA, GB, GC, GD and GE) of diversity microcenter popcorn populations with the nine groups of the American Continent (g1, g2, g3, g4, g5, g6, g7, g8 and g9). The groups GA and GE are genetically closer to the group of Lowland South America–Brazil (g3) corroborating the initial hypothesis of this study that most of the diversity present in the diversity microcenter in Southern Brazil has originated in this part of the Continent. The GB and GD groups did not relate to any groups in the Americas. The GC group was as distant from the others as expected.

Fig. 9
figure9

Phylogenetic relationships between five groups from diversity microcenter in Southern Brazil and nine groups from American Continent

Discussion

Structure patterns and genetic diversity of popcorn landraces from Brazilian diversity microcenter in the far western Santa Catarina (FWSC)

In the latest publication about FWSC popcorn populations, Silva et al. (2016) reported the presence of at least five races (I, II, III, IV and the isolated population denominated 2279X, also analyzed in this study), classified based on 16 morphological characteristics of the grain and ear. Among the five, three were considered new races (I, II and 2279X). The race I was characterized by having predominantly purple and pointed grain, and red cob. Race II was characterized by having orange and round grain and ear length (10.0 cm) lower than the average of the other breeds. The race III was characterized by having predominantly black and round grain, predominantly black endosperm and white cob. Race IV was characterized by having predominantly white and pointed grain, predominantly white endosperm and white cob. Finally, the population 2279X was characterized by having red grain, ear length (19.0 cm), ear diameter (4.1 cm), grain length (11.4 mm), grain width (7.3 mm) and grain thickness (4.5 mm), higher than the average of the other races.

Considering the 66 populations analyzed in this study, it was verified that the populations of GA (Figs. 4, 5), whose predominant genetic pattern is pointed and white grain, could correspond to race IV. The populations of GE, whose predominant genetic pattern is round and mixed color grain, could correspond to race II (new race). The populations of GD, which also has the round grain genetic pattern, but predominant black color, would correspond to race III. The populations of GB were not analyzed in the aforementioned study and probably also correspond to a new race. They have particular characteristics such as the high number of rows and they are denominated “popcorn rice” by farmers, because they have grains similar to the rice grains. Significant differences between grain color and grain shape and GA, GB, GD and GE groups confirm that these phenotypic markers that are used by farmers to select their seeds (Silva et al. 2016) explain the genetic differences between the groups identified in the present study. Research with microsatellite markers in small areas also allowed to detect genetic differences among Argentina’s popcorn races, explained by farmers’ management or selection barriers (Bracco et al. 2009), but with smaller diversity estimates found in this study.

The association of the pattern of genetic groups by SNPs (Figs. 4, 5) with color and grain shape, related to the management and selection barriers performed by the farmers, explain the genetic structure of the popcorn populations of the diversity microcenter, proving that in small areas, the selection of women farmers establish differentiated patterns of diversity across the geographic area, and that distance isolation is not a significant component to explain this pattern. This fact becomes more evident when we rescue the results found by Silva et al. (2016). These authors demonstrated that women farmers in this diversity microcenter (FWSC) use a set of 16 characteristics to perform the selection, and 97% of the farmers’ indications were related to characteristics such as color and shape of the grain, shape and size of the ear and grain arrangement in the rows (Silva et al. 2016), coinciding with the scientific descriptors used to identify maize races.

The genetic structure by SNPs of flour, dent, semi-dent, semi-flint and flint maize populations (called “common maize”), also within the diversity microcenter region, was analyzed by Vidal (2016), but in this case, populations were mainly managed by men. In this study, the author did not identify isolation by geographical barriers, nor by the management of the farmers, since common maize is in an evolutionary process denominated by the author of convergent, in which alleles of neighboring cultures are often incorporated by gene flow, associated with the softer selection pressure made by their maintainers. In this logic, we can corroborate the work of Vidal (2016) and consider that the popcorn populations analyzed in this study are in a divergent evolutionary process, because they undergo strong selection pressure from their maintainers as well as the care to avoid undesirable crossings. This practice promotes the conservation of the genetic identity of a particular landrace and consequently maintains the main characteristic of popcorn which is the expansion capacity.

Structure and sub-structure patterns in American popcorn races

The 575 populations of popcorn from the American Continent were grouped into distinct geographical complexes (Fig. 9 and Table 1). These results are consistent with previous studies investigating the genetic structure of maize populations in the Americas (Matsuoka et al. 2002; Santacruz-Varela et al. 2004; Vigouroux et al. 2008; van Heerwaarden et al. 2011; Mir et al. 2013; Bedoya et al. 2017), in spite of the methodological differences employed in the various works and the shortcomings in relation to the geographic sampling, in general, with low representativeness of lowland in South America accessions.

From the studies cited above, the work of Santacruz-Varela et al. (2004) was the only one that studied the genetic structure and phylogenetic relationships specifically of popcorn population and, nevertheless, with the focus on the germplasm of the United States. From the evaluation of 56 populations through morphological characteristics, isoenzymes and microsatellites, Santacruz-Varela et al. (2004) identified five groups, one composed of populations from Chile, Uruguay and Mexico, which could be equivalent the g2 and g3 groups of the present study; a second group formed exclusively by populations of Brazil, Argentina and Paraguay, which would be equivalent to the group g8; a third group constituted by populations of the United States and a single access from Chile; a fourth group with populations of pointed grain from Latin America and; a fifth group composed exclusively of popcorn populations from the United States. The only United States access evaluated in this study was grouped in the subgroup g3 (Intermediate Zone/Chile), possibly corresponding to the Yellow Pearl Popcorn race derived from the Curagua race of Chile, introduced in the USA in the nineteenth century (Smith 1999) and coincident with the studies of Santacruz-Varela et al. (2004).

The first study on the relations between native races of the Americas was performed by Goodman and Bird (1977). By means of numerical taxonomy, the authors analyzed 17 characteristics of the ear, altitude, latitude and longitude, that allowed to identify 14 groups, among which four were constituted by popcorn races, being: (1) Cónico, which included the races Arrocillo Amarillo, Palomero Toluqueño, Cónico and Chalqueño from Mexico High Valleys, concordant with the representative races of the g4 group, adapted to more than 1500 m of altitude (Table S3); (2) Chapalote, which included the races Chapalote and Reventador from northwestern Mexico, which are concordant with the g5 subgroup, adapted to less than 1500 m of altitude (Table S3); (iii) Southern Popcorn, which included the races Avati Pichingá (Br, Py), Avati Pinchingá Ihú (Br, Py), Polulo (Ch) and Pinsikalla (Ar, Bo) forming a single group, differently from that found in this study which these races presented a wider geographical distribution (in more than one subgroup). In addition, the race Polulo evaluated in the study by Goodman and Bird (1977) was the only one of this group adapted to the altitude regions, belonging in this study to subgroup g1 and; iv) North South America Popcorn, contemplating the Andean and the Caribbean region, divided in three subgroups, constituted by round and yellow popcorns (Confite Morocho-Pe, Tusilla-Ec), white popcorns (Pira-Co, Clavo-Co, Chirimito-Ven, Araguito-Ven e Guarivero-Ven) and pointed popcorns (Canguil-Ec, Confite Pontiagudo-Pe) and that, in this study, the minority of the populations belonging to these races were grouped in the subgroups g1 (with altitude higher than 1500 m) and g9, with both adaptations (Table S5).

Genetic diversity and expansion capacity patterns in American germplasm: would South America be a popcorn domestication center or a popcorn origin center?

Estimates of the genetic diversity of the popcorn subgroups of the Americas found in this study (Table 2) were lower than the results of other studies that used microsatellite markers (Matsuoka et al. 2002; Vigouroux et al. 2008; van Heerwaarden et al. 2011; Bedoya et al. 2017) to analyze the diversity of genetic groups that follow geographic patterns similar to those of this research (Table 1). In addition, estimates of genetic diversity did not follow the logic “the further away from the center of origin, the less genetic diversity, reaching the lowest levels in the South American populations”, suggested by Rebourg et al. (2003) and Bedoya et al. (2017). This disagreement with these studies may be associated with the type of molecular marker used, the limited geographical sampling that, as previously commented, has a low representativeness of populations in South America, especially in the lowlands, as well as the low representative of popcorn populations. On the other hand, studies carried out at the regional level with Mexican (Reif et al. 2006) and Argentine races (Bracco et al. 2009, 2012) found that popcorn groups presented lower diversity than those characterized with other types of endosperm, which may be the result of severe bottlenecks imposed by adverse environmental conditions or the practice of stricter selection of farmers (Bracco et al. 2009, 2012).

The expansion capacity (Table 2) followed the logic of the “geographical continuum” increasing the mean values as it distances geographically from the center of origin, with the highest values found in groups g3 and g8 (Brazil and Paraguay). Thus, the expansion capacity values associated with the cluster analysis result (Fig. 9) support the hypothesis of the maize dispersal routes (by human migration) from the center of origin to other regions of America, rebuilt by several studies (Matsuoka et al. 2002; Freitas et al. 2003; Lia et al. 2007; Vigouroux et al. 2008; Bedoya et al. 2017). This means that corn would have been straggling from the Mexican highlands (g6), migrated to the tropics of Mexico (g4) and other regions of Mesoamerica, then to Central America and the Caribbean (g5), leaving Colombia for the region Andean (g1). This route is in agreement with the study of Goodman and Bird (1977), in concluding that the group North of South America Popcorn represents a relation of the popcorns of the Caribbean with those of popcorns of the Andes. The group of the Intermediate South America Zone (g9) identified in the present study would represent the contact zone between the highlands (g1) and lowlands of South America (g2, g3, g7 and g8). The studies of Dubreuil et al. (2006) and Lia et al. (2007) also found Andean signatures in lowland maize populations, the latter being based strictly on maize populations in Argentina, which corroborates the presence of the g9 group, most of them from popcorn races in this country (Table 1), adapted to the altitude above and below 1500 m (Table S5).

Considering that the center of origin of the maize is Mexico, we can suggest as the first hypothesis that as popcorn has dispersed from this country to other regions of the American Continent, there has been a selection aimed at increasing the capacity for expansion. This indicates that the human populations of South America, especially in the southern part (where the highest average values of expansion capacity were observed), appreciated and still appreciate this type of maize in the diet, like the women farmers who conserve until the present-day hundreds of popcorn landraces. In Mexico, on the other hand, the use of popcorn landraces in human nutrition was lost over time, with the main use being poultry feed (Contreras et al. 2006; Vázquez et al. 2014). Wellhausen et al. (1951), who first described the maize races of Mexico, had already mentioned the little use of popcorn to make “popcorn” because of its “little value for this purpose”. Considering these two extreme situations, if the expansion capacity is the characteristic that defines the quality of popcorn and makes this type of maize become a food for human populations, the largest and smallest values found in Table 2 were observed for groups whose use was possibly preserved and lost, respectively.

One other explanation for the decline in expansion capacity with the high genetic diversity further from the center of domestication in Mexico: perhaps popcorn dispersed from North America to South America, but interbreeding with local varieties drove up the diversity of the gene pool, and at the same time allowed more efficient selection on the trait of expansion capacity.

We also do not rule out the possibility that a second popcorn maize domestication event occurred in South America. Brunson (1955) had already suggested, but without much evidence, that South America and Central America were probably the center of origin of popcorn. Contreras et al. (2006) point out that for every four primitive popcorn originating in Mexico, at least another four were found in South America. In fact, the earliest archaeological remains of popcorn were discovered in Peru, with over 6000 years of AP (Grobman et al. 2012), being considered contemporaneous to the remains of corn macrofossils recorded at Guila Naquiz Cave in Mexico (Piperno and Flannery 2001), one of the oldest, but curiously different in some respects. This suggests that maize may have undergone important developments when it left Mexico (Benz 2001; Piperno and Flannery 2001; Grobman et al. 2012). Archaeological remains of popcorn in Ecuador (Zarrillo et al. 2008), Chile (Rivera 2006) and Argentina (Lia et al. 2007) have been found, showing that popcorn probably was already present in the diet of these pre-historical. In Brazil and Uruguay, the oldest archaeological records of maize date from 5200 years BP (Hilbert et al. 2017) and 4190 years BP (Iriarte et al. 2004) respectively, but without the inference if the traces found related to the popcorn. This evidence suggests that maize may have undergone important developments when it left Mexico (Benz 2001; Piperno and Flannery 2001; Grobman et al. 2012) how to recently demonstrated by Kistler et al. (2018) that suggested from genomic, linguistic, archaeological, and paleoecological data that the southwestern Amazon was a secondary improvement center for maize.

A “secondary domestication” of popcorn implies a wild gene pool in South America, and a completely independent origin of domesticated maize. We are not implying this idea, because it is not ecologically or genomically plausible, or supported by any previous evidence. We are suggesting a South American origin for popcorn specifically, out of an existing domesticated or semi-domesticated gene pool. This is different from an independent domestication. In order words this is an independent origin of popcorn, but not an independent domestication of maize.

The findings presented by archeology, the new evidence pointed out in the study by Kistler et al. (2018) and the assumptions we make based on the results of our study support the hypothesis that popcorn populations evolved in the north–south direction, whose domestication processes provided an increase in the expansion capacity. The fact that the highest mean values were found in southern South America (g3 and g8) suggest an association with the indigenous Guarani culture. This is because this territory (which includes part of Brazil, Paraguay, part of Bolivia, part of Argentina and Uruguay) was the area of occupation of Guaranis (and continues to be). Moreover, in the literature about the maize races of lowland of South America it was already stated that “apparently only the Guaranis grew popcorn”. The Guarani expansion to southern South America, including for the diversity microcenter, would need to be better investigated, in order to understand if the Guarani culture was indeed associated with the dispersal of popcorn and even with its process of domestication in this part of the continent. These are clues that can certainly contribute to the reconstruction of the migratory routes of popcorn and also to understand in more depth the “geographical continuum” of the expansion capacity.

Genetic origin of popcorn from a microcenter of diversity in southern Brazil

Considering the popcorn populations of the diversity microcenter these were structured in five groups (Figs. 3, 4), with groups GA and GE being phylogenetically related (Fig. 9) to America g8 group (Lowland South America- Brazil) approving our initial hypothesis. The genetic origin of groups GA and GE can be explained by the fact that this diversity microcenter was also the area of Guarani occupation. Brieger et al. (1958) and Paterniani and Goodman (1977) described two Brazilian popcorn races: Avati Pichingá/Pichingá Aristado (pointed grain) and Avati Pichingá Ihú/Pichingá Redondo (round grain), both with many colors. The populations of GB, GC and GD group were not structured with any of the groups in the Americas. The GC was to be expected because it was formed by the teosinte population and the teosinto x popcorn hybrid (956A). The GB and GD probably they originate in Guarani popcorn and have either undergone a process of differentiation through human selection or come from more recent introductions. In other words, we can say that it is a diversity originated in the region itself.

The five groups identified for DAPC analyze brought together possibly descended from the germplasm cultivated by the Guaranis associated with the conservation process carried out by the women farmers, which on the one hand maintain the genetic identity of the races (conservationist selection) and, on the other, enables the formation of new races (through intervarieties crossing and selection for diversification). This aspect is in agreement with the studies by Silva et al. (2016) that identified old and new popcorn races in this Brazilian diversity microcenter. This result makes it possible to recognize these varieties as cultural patrimony, indigenous and typical of the region, and has been maintained in recent times by the practice of conservative selection of women farmers. Both origins—from the region itself and from women farmer diversification processes—demonstrate the importance of in situ-on farm conservation, in this microcenter of diversity in southern Brazil.

Summary conclusion and perspectives

At the continental level, we identified nine genetic groups of a set of 575 populations of popcorn from the Americas, which were structured according to the geographical pattern but did not follow the logic of “the farther from the center of origin, the lower the genetic diversity”. However, for the expansion capacity the results showed a “geographical continuum”, that is, the more geographically distant from the center of origin of the maize, the greater the expansion capacity. The fact that the populations of the South American groups, especially in the lowlands, presented the highest average values for this characteristic raised the three hypotheses previously discussed. All issues need to be thoroughly investigated, bringing together genetic, geographic, historical, archaeological, anthropological, genomic and archaeological data, and analyses that can detect selection genes by identifying loci that have signatures of selection. All this information will undoubtedly contribute to the reconstruction of the history of popcorn, the dispersal routes and its evolutionary process, especially in the lowlands of South America.

At the diversity microcenter in Southern Brazil we identified the phylogenetic relationships of the popcorn populations, with two distinct origins: one from lowland germplasm of South America (Brazil), possibly descended from Guarani popcorn races, and the other resulting from women farmer diversification processes, which shows that this region is indeed a microcenter of accumulation of popcorn diversity, and that even can provide clues to the issues raised above. This conclusion connects with the result of the genetic structure identified for the set of 66 analyzed populations that is maintained not by geographic isolation, but by the isolation related to the conservation by women farmer. This makes the breed standard maintained phenotypically and, as demonstrated by our results, also genetically reinforcing the particularities of this type of maize within the subspecies Zea mays ssp. mays L., in this diversity microcenter.

From our results, we reinforce the importance of South American popcorn germplasm, providing clues about its evolution and generating findings about its diversity. The South American Continent encompasses gene pools distinct from those found in other regions, whether continental or micro regional. For this reason, the measures of conservation of the species must be priority as much as they occur in its center of origin. The human action that was the key to the domestication of the species by the prehistoric peoples must be seen as an ongoing process that reaches the present.

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Acknowledgements

The authors would like to thank the farmers and their organizations for the information provided about the FWSC germoplasm. This research was supported by the Research Support Foundation of Santa Catarina (FAPESC), and National Council for Scientific and Technological Development (CNPq), whereas the scholarship was granted to Natália Carolina de Almeida Silva by the Coordination of Personal Perfectioning of Superior Level (CAPES) and the “Ciência sem Fronteiras” Program (CNPq).

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Conceptualization: NS. Data curation: JO, DC. Formal analysis: NS, RV, JC. Funding acquisition: JO, NS, DC. Investigation: NS. Methodology: NS, RV, JC. Project administration: NS, JO, DC. Supervision: JO, DC. Writing—original draft: NS. Writing—review and editing: NS, RV, JO, DC, JC.

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Correspondence to Juliana Bernardi Ogliari.

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De Almeida Silva, N.C., Vidal, R., Bernardi Ogliari, J. et al. Relationships among American popcorn and their links with landraces conserved in a microcenter of diversity. Genet Resour Crop Evol (2020). https://doi.org/10.1007/s10722-020-00935-2

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Keywords

  • Domestication
  • Expansion capacity
  • Genetic diversity
  • Landraces
  • Single nucleotide polymorphism markers
  • Zea mays ssp. mays L.