Wild Progenitor and Landraces Led Genetic Gain in the Modern-Day Maize (Zea mays L.)

1. Introduction

Maize (Zea mays ssp. mays) is a member of the Maydae tribe of the Poaceae family, originated in Mexico and Central America. Maize with somatic chromosome 2n = 20, 2.3 gigabase of genome size and more than 60000 genes [1]. After Columbus entered the New World and introduced maize to Europe, it gradually spread worldwide [2]. Its production exceeds wheat (Triticum aestivum) and rice (Oryza sativa) nowadays (http://www.fao.org). It has emerged as a crop of global importance due to its use as human food, livestock feed and various industrial products. A significant portion of maize production is utilized as animal consumption as it serves as important source of calories and protein in the developing countries [3]. A debate emerged at the beginning of the last century concerning the origin of maize. Maize ought to be derived from the cross between a close relative of maize and Tripsacumor the oldest wild maize is the progenitor of maize [4]. Subsequent archeological and genetical evidences indicated that teosinte (Z. maysssp. parviglumis) is the only ancestor of maize and is widely accepted [5, 6]. The discrepancy between teosinte and modern day maize were found around the Balsas River in southwestern Mexico around 9000 years ago [7].

The ancestor teosinte originated from Mexico, the selection by Native Americans for improved plant types and seed types become corn. According to modern breeding, different generations of selection turned teosinte into landraces and ultimately to the modern-day maize. The modern day maize differs from teosinte in the key traits; for example, teosinte is characterized by multi-branched, tiny reproductive parts and two rows of seed. In comparison, the modern-day maize possesses 20–22 kernel rows. The reproductive separation is not complete in primitive strains. The modern-day maize reproductive separation is complete, i.e., ear and tassels, taller plant height, erect stature, more light interception and more photosynthesis [4]. Domestication leads to the evolution of wild progenitor species to early domesticated landraces and ultimately to modern cultivars. The loss of genetic diversity often accompanies domestication. Typically landraces are heterogeneous (non-uniform) and, therefore, a good source of genetic diversity. Landraces are usually less diverse than wild relatives but more diverse than modern-day cultivars [8].

Typically, domesticated plant species’ wild relatives do not have all the desirable characteristics for normal agricultural production and use. Only a small portion of the genome’s selection and the key genes/QTLs/transcription factors involved under domestication have been identified and cloned [1]. In transforming teosinte into modern maize, genetic loci such as teosinte branched 1(tb1) and teosinte glume architecture 1(tga1) has played a pivotal role [9, 10]. The loci involved in transforming plant architecture and morphology were shown to have a pleiotropic effect on other traits. This lead to the development of convergent phenotype of the modern-day maize. Maize later spread from the centre of origin to various parts of the globe, including America, Europe, Africa and Asia. Genetic resources, especially wild relatives and landraces, harbor novel alleles/genes to impart resistance/tolerance to various biotic/abiotic stresses and boost productivity and nutrition quality. Teosintes and Tripsacumare native to Mexico and Central America among wild families, while in Southeast Asia, Coix, Chionachne, Sclerachne, Trilobachneand Polytocaoriginated. Landrace accessions with unexplored alleles/genes function as important donors with substantial characteristics.

This chapter summarizes the early crop domestication process from thousands of years ago to modern-day plant breeders’ success in plant improvement. Understanding the domestication of crops and plant breeding provides a background for the importance, significance and usage of wild relatives of crops maintained either in situ or in gene banks. The importance of landrace accessions and wild relatives of maize in supplying useful genes for different essential traits has been addressed.

2. Evolution of maize

Maize (Zea mays ssp. mays, Taino: mahiz, Spanish: maíz), also known as corn (North American English), is a cereal grain that was first domesticated by indigenous people around 10,000 years ago in southern Mexico. The ancient farmers from Mexico took the initiative to domesticate the maize by only looking at their kernels. They observed that all plants are not the same; some kernels look better, taste better or easier to grind. They saved the kernels based on the beneficial characteristics and used them to plant in the next season for their harvest. This forms artificial selection or selective breeding. Over time, with more rows of kernels, maize cobs grew bigger, gradually taking the form of modern maize. The identity of maize’s progenitor or wild ancestor remained a mystery for a while compared to other crops. Although there are apparent wild relatives of other grains such as wheat and rice, there is no wild plant that looks like maize, with smooth, starchy kernels arranged along the cob. To explain the origin of maize, various researchers explained several theories/hypotheses: tripartite hypothesis, catastrophic theory of sexual transmutation, Tripsacum-Zea diploperennishypothesis, and teosinte hypothesis were discussed and discussed in depth by various scientists.

The tripartite hypothesis stated that the progenitor of maize was the extinct popcorn. The crosses between corn and related genera Tripsacumlead to teosinte formation, with further crosses giving rise to the diversity of maize we observe today [11]. Among the theories, the teosinte hypothesis is the most accepted one. Teosinte does not look much like maize, particularly when its kernels are compared to maize kernels. But at the DNA level, the two are surprisingly alike. Both possess the same number of chromosomes and similar gene arrangements. The hybrids between teosinte and maize are fertile and can reproduce naturally. Beadle [4, 12, 13] was one of the first scientists to establish the close relationship between maize and teosinte. He proposed that ancient people cultivated teosinte for food. During the cultivation of teosinte, mutations arose and being selected by the people. A set of five major mutations transformed teosinte into maize. Beadle [4] has studied the advanced generations of teosinte × maize derived hybrids. In the F₂ population of 5000 plants, the frequency of parental types was 1 in 500 plants. He concluded that 5 major loci/genes are responsible for maize domestication based on simple Mendelian genetics. Later five major quantitative trait loci (QTLs) and QTLs with minor effect for the key traits differ for maize and teosinte [9]. Wright et al. [14] reported 2–4% of genes had been selected during evolution/domestication by investigating around 774 genes. Out of a total of 3900–42000 protein-coding genes, only 800–1700 (2–4%) protein-coding genes underwent selection during the process of domestication. With the advent of next-generation sequencing (NGS) techniques, Hoffard et al. [15] identified 484 domesticated loci, of which 107 loci were further selected during improvement. The evidence mentioned above suggests that only a small portion of the genome was selected during maize domestication and improvement.

Genetic studies have provided firm evidence that maize was domesticated from Balsas teosinte (Zea mayssubspecies parviglumis). This wild relative is endemic to the mid-to lowland regions of southwestern Mexico. Thus, genetic data point to the primary diffusion of domesticated maize from the highlands rather than from the region of initial domestication. The gene flow between maize and its wild relatives meaningfully impacts geographic origins [16].

3. Genes selected under domestication

Selection during evolution, whether natural or artificial, acts through the phenotype. For multifaceted phenotypes such as plant and inflorescence architecture, the underlying genetic architecture comprises a complex network of interacting genes rather than single genes that act independently to determine the trait. As such, selection acts on entire gene networks [17]. A set of genes/loci were selected during domestication knowingly or unknowingly by farmers then breeders. The earlier selection mainly focused on plant morphology, ear size, seed type and single stalk etc., for transforming its wild progenitor to the modern-day maize. Only a few genes, i.e., 2% genes (1200 genes) of the 60000 genes of maize, have been selected during the process of domestication. Those genes that have experienced artificial selection have greatly reduced genetic diversity in modern germplasm. Therefore cannot contribute to the variation for agronomically important traits. Artificial selection has impacted maize diversity during its domestication from teosinte (Zea mays ssp. parvglumis) to landraces and plant breeding from landraces to modern inbred lines. Artificial selection has impacted protein, oil, starch and amino acid content.

Maize domestication started around 10000 years ago. Early farmers selected and planted seeds from plants with beneficial traits while eliminating the undesirable ones. As a result of good alleles, i.e., alleles of genes controlling the favored traits, the frequency has been increased within the population. At the same time, bad/deleterious alleles frequency decreased. Such selection is made possible due to the tremendous availability of natural genetic variability in the teosintes. Over time, with current agricultural practices, certain combinations of genes have been selected. This includes major and minor gene mutations distinguishing from wild ancestors. That’s why only few genes are responsible for the transformation. Beadle and Doebley revealed that only five genes might be responsible for the dramatic morphological changes. The “one gene-one trait” model for such genes is still questionable. Although a small number of genes has striking effects, on-ear and plant morphology resulted in the maize evolution. However, the vast majority of genes have an only a modest effect. Thousand of genes were likely necessary to contribute to the transformation like, increase in the size of the ear, adapting maize to the modern agricultural practices and an increase in the maize kernel’s nutrient status.

3.1 Traits modified under domestication

3.1.1 Glume

Teosinte was characterized by hard glumes, the seed, which were passed through the digestive tract of the ruminants and not get digested. This ultimately serves as propagating material for the next generation under natural conditions. The locus tga1, teosinte glume architectureleads to a decrease in the size of glumes (Figure 1). It encodes the squamosa-promoter binding protein (SBP) transcription factor. This QTL has been mapped on chromosome 4 [18] and cloned [19]. Interestingly, in the tga1promoter region, tga1is regulated by tb1 viadirect binding of tb1to two GGNCCC motifs [20].

3.1.2 Plant architecture

The loci teosinte branched 1 (tb1) responsible for the transformation from many tillers, many inflorescence to the single stalk with single inflorescence in the modern day maize. Concentrating the energy resources in a single ear and stalk made it possible to increase the ear size. The tb1encodes the TCP family transcription factor, i.e., TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL NUCLEAR ANTIGEN FACTOR, which is mapped for apical dominance and inflorescence development [10]. The tb1was mapped by transposon tagging, which leads to the inhibition of axillary bud formation and transformation to female inflorescence [21, 22]. The causal variant of this phenotype was transposable element (TE) in the upstream of tb1suggests the role of long range chromatin insertions in the maize domestication [23]. The ortholog tb1locus also has been reported in the other crops suggesting its conserved nature in other plant species. In rice OsTB1with negative regulation [24], BRC1in Arabidopsis thaliana[25], HvTB1for higher tiller number in barley [26]; TaTB1along with FLOWERING LOCUS T1regulates inflorescence architecture in wheat [27]. These conserved loci of tb1explained the evidence for its role during domestication.

3.1.3 Others

QTLs at genes responsible for shattering vs. solid cobs, single vs. paired spikelets and distichous (two rank ear) vs. polystichous (> four ranks ear). The gene Zea floricaula leafy2(zfl2) primarily regulates the teosinte ear’s two ranks [9, 28]. Sweet maize and popcorn retain tillering growth habit during maize diversification. However, the underlying molecular genetic mechanism remains unknown. The retention of maize tillering is controlled by a major quantitative trait locus (QTL), tin1, which encodes a C2H2-zinc-finger transcription factor that acts independently of tb1. tin1is involved in multiple pathways, directly represses two tiller-related genes, gt1and Laba1/An-2, and interacts with three TOPLESS proteins to regulate the tiller buds’ outgrowth. Therefore maize tin1, derived from a standing variation in wild progenitor teosinte population, determines tillering retention during maize diversification [29].

Characterization of variations in the Four-row Wax landrace of China reported kernel row number (KRN) related genes and KRN QTL regions revealed potential causal mutations in fea2, td1, kn1, and te1[30].

3.1.4 Starch

In the initial phase of domestication, the focus was mainly on the plant shape and ear morphology. Many additional traits were acts as the targets from recent years. Grain yield, ear size (increased from 2 cm to 30 cm), quality and starch. Starch is the major byproduct of maize, constitutes ~73% of kernels’ total weight. The three loci, i.e., Su1, bt2and ae2,are targets of selection during maize domestication and improvement. Tassel, seed2and dwarf8as the targets of selection based on a screen of genes on chromosome1 [31, 32].

4. Pleiotropic gene interactions during smaize domestication and improvement

Pleiotropy generally describes the effect of an allele of a gene for producing an unrelated phenotype. It affects the path of evolution as it facilitates if a directional selection of a phenotype affects other beneficial phenotypes’ fitness or restricts if the allele has the deleterious effect on another phenotype. Generally, the developmental traits reveal pleiotropy by explaining the association among flowering time in male and female flowers [47], ear and tassel developmental traits [48], leaf length and flower length [49]. Apart from these, QTLs responsible for tassel and ear development are also responsible for flowering time [50].

Understanding pleiotropy and the association between phenotypes will help to explain the selection outcome constraints. For example, the maize allele at zfl2is responsible for spiral ear phyllotaxy that increases the kernel number and is involved in other traits like early flowering [51]. So in a well-adapted environment stabilizing selection for flowering might limit directional selection for kernel number. Therefore such pleiotropy may limit domestication alleles when selection disallows variation.

Various researchers have reported that domestication alleles were pleiotropic [11, 12, 52, 53]. The teosinte branched1 (tb1)is pleiotropic across many traits; apical dominance, growth of leaves on the lateral branches, length of lateral branches, ear and root architecture [54]. tb1, as a transcription factor, binds to many locations in the genome. It directly regulates gt1by binding to its promoter. Still, it directly affects the cell cycle by suppressing many cell cycle genes (proliferating cell nuclear antigen2 (pcna2)and minichromosome maintenance2/prolifera (mcm2/prl) [20]. zga1is a MADS-box transcription factor associated with ear size and has a pleiotropic effect on flowering time [36]. tga1, a glume architecture allele shown to have pleiotropic effect on lateral branch lengthy, ear phyllotaxy and ear disarticulation [55].

5. Effect of maize domestication on genetic diversity (Domestication Bottleneck)

Both domestication and artificial selection during crop improvement led to selecting only desirable/beneficial traits, resulting in the reduced genetic diversity of the unselected genes. During the process of domestication, nearly all crop species experience “Domestication Syndrome” or “Domestication Bottleneck” [22, 56]. These effects happen in two stages; i) initial bottleneck effect, when a subset of crop wild species population brought under cultivation and ii) subsequent reduction in the genetic diversity through selective breeding for the desirable traits during crop improvement is improvement bottleneck. Among crop species, maize experiences a relatively mild genetic bottleneck, as domesticated maize retains around ~81% of the genetic diversity of teosinte [15]. Approximately 2–4% of genes were the target during the initial domestication and crop improvement stage [14, 15]. It is established that genetic diversity generally declines with the domestication of teosinte to the landraces. Subsequently, modern plant breeding reduces the genetic diversity of modern-day maize inbred lines relative to the landraces (Figure 2). Therefore such genes strongly influenced by domestication or improvement are enriched in modern improved varieties in the subset of genes that show low nucleotide diversity [14]. Yamasaki et al. [57] proposed a model containing three types of genes: ‘neutral genes that demonstrate diversity reduction by general bottleneck effects, domestication genes in which diversity by selection between the teosintes and landraces is significantly reduced, and improvement genes in which diversity by selection between landraces and inbreds is significantly reduced (Figure 2).’

The genes that experienced artificial selection during domestication and crop improvement have significantly reduced genetic diversity in the modern germplasm and cannot contribute to the agro morphological traits. Therefore the selected genes are difficult to identify in the genetic screens and may not be useful in traditional breeding programmes. If we need to utilize the selected genes fully, the new variation must be reintroduced from teosintes. Additionally, for the 98% of genes, which do not experience selection during domestication and crop improvement, there are huge genetic variations in the diverse inbred lines that could be utilized by identifying the genetic loci/QTLs and improvement through plant breeding.

6. Wild relatives of maize

Wild relatives of crops are the species of wild plants that are genetically linked to cultivated crops. Unattended by humans, they continue to grow in the wild, developing traits that farmers and breeders can cross with domesticated crops to produce new varieties, such as drought tolerance or pest resistance. The Zeagenus of grass consists of seven genera with different chromosome numbers divided into two groups: viz. old-world and new world groups. Chionachne, Coix, Polytoca, Sclerachneand Trilobachneoriginated in Southeast Asia and belonged to the old-world group. The new world group consists of Zeaand Tripsacumand originated in Mexico and Central America. Zea mays ssp. maysis the only species of economic importance and other species referred to as teosintes.

7. Landraces of maize

A landrace is defined as ‘dynamic population(s) of a cultivated plant that has a historical origin, distinct identity, and lacks formal crop improvement and often being genetically diverse, locally adapted, and associated with traditional farming systems’ [58]. Compared to other crops, maize has tremendous genetic diversity, which offers potential for crop improvement for biotic/abiotic stresses, nutritional quality and grain yield. In landraces, the diversity/genetic variations lie within-population rather than among populations. Worldwide, the landraces have been characterized both morphologically and molecularly. The genetic variability present in the available landraces has been utilized to improve agro morphological traits, biotic/abiotic stresses and specialty traits. In crop centers of origin and diversity, often biotic and abiotic conditions vary across the landscape, creating the possibility of local adaptation of crops. Local landraces perform better than non-local ones under local conditions. Some of the examples of their utilization are given below:

8. Conclusions

The domestication and crop improvement processes lead to converting teosinte into landraces and subsequently to the modern-day maize inbred. During domestication, based on genetic evidence, it is clear that selection was mainly focused on five genes. This leads to the change in the architecture and morphology of teosinte into maize. Maize has evolved distinct genetic solution towards domestication: domestication of maize has involved distinct genetic and regulatory networks have been used to acquire convergent phenotypes. During domestication and artificial selection, only a small part of the genome underwent selection, which ultimately led to the modern-day maize. So, wild relatives and landraces encompassing the unselected genes possess enormous potential as the donor for beneficial genes/alleles. The derived inbred lines from such material could not be directly utilized in the breeding programme. They must be utilized as a donor for the specific traits, i.e., tolerance to biotic/abiotic stresses and nutritional quality traits. The utilization of wild relatives and landraces in the breeding programmes is not that easy; utilization of bridging species and embryo rescue provides the solution to this problem. The pre-breeding programme helps to utilize wild relatives and landraces to enrich the ongoing crop improvement programmes. The availability of the genome sequence of ‘B 73’ and ‘Palmoreo’ landrace and strong pre-breeding programme can potentially enhance unexplored germplasm in the maize breeding programme.