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Review

Lupinus mutabilis Breeding in the Andes of Ecuador, Peru, and Bolivia: A Review

by
Diego Rodríguez-Ortega
1,*,
José Luis Zambrano
1,
Santiago Pereira-Lorenzo
2,
Andrés Torres
2,3 and
Ángel Murillo
1
1
Instituto Nacional de Investigaciones Agropecuarias (INIAP), Estacion Experimental Santa Catalina, Cutuglahua 171108, Ecuador
2
Department of Crop Production and Engineering Projects, Campus Terra, University of Santiago de Compostela, 27002 Lugo, Spain
3
Plant Biotechnology Laboratory, Universidad San Francisco de Quito, Quito 170901, Ecuador
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(1), 94; https://doi.org/10.3390/agronomy14010094
Submission received: 21 August 2023 / Revised: 4 October 2023 / Accepted: 9 October 2023 / Published: 30 December 2023
(This article belongs to the Topic Vegetable Breeding, Genetics and Genomics)
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Abstract

:
Lupinus mutabilis, also known as tarwi or chocho, is an important agricultural species that has been cultivated in South America since ancient times. Tarwi is native to the Andean regions of Peru, Bolivia, and Ecuador and has very high protein content. Despite its high nutritional value and promotion efforts by regional researchers and breeders, tarwi is not a widely cultivated crop in its center of origin. In this review, we present the work carried out by public breeding programs of L. mutabilis at national agricultural research institutes, universities, and other institutions in Ecuador, Peru, and Bolivia. The main breeding method used in the Andes to improve local landraces has been mass selection to adapt lines to specific environments. At least 25 cultivars or ecotypes have been selected and released over the last 40 years using this breeding system. Nevertheless, breeders are currently struggling to develop new varieties that are high yielding, suitable for mechanized harvesting, have a low content of alkaloids or other anti-nutritional properties, and resistant to anthracnose (Colletotrichum acutatum). Therefore, it is necessary to reassess the potential of this crop and invest in its research to incorporate new techniques and breeding strategies to optimize the development of new varieties in the Andes which address the current cultivation challenges of the species.

1. Introduction

Tarwi (Lupinus mutabilis Sweet), also known by other common names such as tauri or chocho [1], is a species native to the Andean region of Peru, Bolivia, and Ecuador that has been cultivated since pre-Incan times [2,3]. The indigenous populations of this region used tarwi as one of their main sources of food and income. The ancestral knowledge about its cultivation, conservation, and various forms of utilization are still maintained by indigenous people in the Andean culture. L. mutabilis is the only species of the genus Lupinus that has been domesticated and cultivated in South America [4]. At present, it is mainly planted in the Andean region of Ecuador, Peru, and Bolivia, and is it used for human consumption in several methods of food preparation [5].
The cultivation of tarwi is essential for conserving the agroecological systems in the highlands. Through the nodules formed in their roots by the bacteria Rhizobium, the plant has the capacity to fix between 120 and 160 kg ha−1 of Nitrogen (N) in the soil per year [6], even fixing up to 500 kg ha−1 of N per year [7]. In addition, the plant has adapted to grow under poor soil conditions (low nutrient content) and low-input agricultural systems [8]. In the “chakra” (Andean name for a typical farmer plot), tarwi is typically cultivated as a monoculture or in association with other crops like maize (Zea mayz), quinoa (Chenopodium quinua), potatoes (Solanum tuberosum), and cereals [9].
Tarwi is considered to be of paramount importance for food security in the Andean region [10]. The seed has a high protein content of 41–51%, which exceeds that of any other Lupinus species [11]; additionally, it has an oil content of 14–24% [12], a high content of calcium, fiber, iron, and zinc, and does not contain gluten [13]. Therefore, its cultivation and consumption are considered strategic, especially for nursing mothers and growing children as one of the alternatives to combating child malnutrition [14]. The consumption of L. mutabilis, as part of a healthy diet for humans, prevents and treats metabolic diseases such as obesity, diabetes, and cardiovascular diseases [14].
Tarwi grains are raw materials with great industrial potential in the production of processed or semi-processed foods [14]. The commercialization of proteins of vegetable origin and their derivatives has increased significantly in recent years: in 2012 they moved about 1.7 million metric tons, and it is expected that there will be an increase of 5.5% in the coming years; North America and Europe are the markets with the highest consumption [15]. Tarwi paste is useful in making beverages, yogurts, and jams; meanwhile, the flour is mainly used in the preparation of protein-rich and gluten-free bread, cakes, cookies, cakes, noodles, chips, instant soups, and sausages [16]—making it an excellent option for people with gluten intolerance (celiac disease).
Although tarwi has been considered an ideal food for its nutritional value, industrial potential, and environmental benefits, the study and genetic improvement of the crop is still limited, lacking high-yielding, early-maturing varieties, and a consistent breeding history [17]. This review describes the breeding methods used in L. mutabilis and the released cultivars during 40 years of research in Ecuador, Bolivia, and Peru—countries recognized as centers of origin of the crop. Additionally, the future of tarwi breeding is analyzed.
Much of the information contained in this review referring to the genetic improvement carried out in the Andean region has not been widely disseminated in the international scientific community. The publication of the progress obtained in the improvement of tarwi will be used by breeders in the Andean Region and breeders from other parts of the world who have already shown interest in generating new varieties of L mutabilis.

2. Tarwi Plant Characteristics

L. mutabilis (2n = 48) [17] taxonomically belongs to the Fabaceae Family [2] and is primarily an autogamous species with hermaphroditic flowers; however, a certain level of cross-pollination can occur (5 to 10%), the level of which can increase depending on the genotype and the ecological conditions where it is planted [18]. The most important characteristic of tarwi is its high nutritional value; its seeds have high protein, fat, and fiber contents (50%, 20%, 7%) that can surpass other grains that are commonly used in the food industry, such as soybeans (Glycine max) (40%, 18%, 4%), beans (Phaseolus vulgaris) (22%, 1.6%, 4%), and peanuts (Arachis hypogaea) (27%, 42%, 2%) [2].
L. mutabilis is generally an annual plant that varies in height from 0.50 m to more than 2 m depending on the genotype and the environment in which it is grown [19]. The root is taper, vigorous, and deep, and can extend up to 45–50 cm deep [4].
The secondary roots have symbiotic nodules with bacteria of the genus Rhizobium [20].
The stems are erect, cylindrical, and have a main axis that can be prominent or not prominent with ramifications [2] (Figure 1a). The stem of the tarwi is generally very woody, with a high content in fiber and cellulose. The number of branches varies from a few to 52 branches. The number of pods and fruitful branches has a positive correlation with high production [4]. The stem and its ramifications determine the architecture of the plant [18].
The branching of the tarwi is sympodial, typically alternate. Axillary buds are born on the central stem sides, forming the first order branches; in turn, they form second-order sub-branches, and these branches give rise to third-order branches [4] (Figure 1b).
Tarwi has terminal inflorescences of flowers arranged vertically (Figure 1c) [2]. The variation in the number of clusters depends on the number of branches, and each cluster can develop up to 20 flowers, which bloom at different times.
The flowers are bilaterally symmetrical, each flower has a corolla with five petals: one for the standard, two for the keel, and two for the wings (Figure 1d). The keel surrounds the pistil and the ten stamens [21]. The color of the corolla can be blue, white, pink, or violet [22] (Figure 2a). The flower color intensity varies from the beginning of its formation to maturation, starting from a light color to very intense (Figure 2b).
The fruit is an elliptical pod. The seeds are accommodated in the pod in a row in a size that varies from 4 to 15 mm (Figure 2c). The young pods are very pubescent, and as it matures, there is considerable loss of pubescence. The shape of the seeds can be ellipsoidal, lenticular, rounded, and others in a semi-square shape. The seed color varies, especially due to their distribution, which can be like an eyebrow, mustache, crescent, marbled [21]. The grain color is regulated by several genes: in some cases, the dark colors are dominant over the light ones; however, the white color has a double recessive behavior [4].

3. The Cultivation of Tarwi in Ecuador, Peru, and Bolivia

Bolivia has an approximate area of 1895 ha of tarwi [19,23], with an average yield of 637 kg ha−1 [23]. It is grown in the cold areas of the Altiplano and in the inter-Andean valleys at altitudes between 2500 and 4000 masl, specifically in the Departments of Cochabamba, La Paz, Potosí, and Chuquisaca [24] (Figure 3).
In Ecuador, the approximate area of tarwi cultivation is 6000 ha, and the average yield is 400 kg ha−1 [25]; however, improved varieties with a potential yield of 1500 kg ha−1 are currently being introduced [3]. Tarwi cultivation is concentrated in the inter-Andean region, especially in the provinces of Cotopaxi (Juan Montalvo and Alaquez) and Chimborazo (Palmira and Riobamba). Although to a lower extent, it is also cultivated in other agroecological zones of the highlands, such as Pichincha (Cayambe), Bolivar (Guaranda), Imbabura (Cotacachi), Tungurahua (Quero), and Carchi (Bolívar) [3]. The tarwi-producing areas in these provinces are located between 2700 and 3800 masl, mainly in areas with low rainfall [22]. A potential area of 140,712 ha for the cultivation of tarwi has been estimated for the highlands of Ecuador [9].
In Peru, tarwi is cultivated in the Sierra (highland) of Cajamarca, La Libertad, Amazonas, Huanuco, Huancavelica, Ancash, Ayacucho, Junin, Pasco, Apurimac, Cusco, and Puno [6]. The approximate area is 10,628 ha, with an average yield of 1335 kg ha−1, a maximum yield of 2232 kg ha−1 in Apurímac, and a minimum yield of 657 kg ha−1 in Amazonas [3].
The annual per capita consumption in Ecuador is 4 kg per year−1, being the highest in the region. In Bolivia and Peru, consumption does not exceed 0.2 kg per year−1 and 0.5 kg per year−1, respectively [3].

4. Genetic Diversity of L. mutabilis in the Andean Region

L. mutabilis was domesticated in the highlands of northern Peru, most likely in the Department of Cajamarca, with L. piurensis being the most likely wild progenitor of tarwi. L. piurensis is a wild Lupinus species endemic to the western edges of the Andes, from Cajamarca through Piura in Peru to the southern Loja in Ecuador, between 1650 and 3300 masl [26]. The Andes has the greatest genetic diversity of L. mutabilis [19], with a wide variety in plant morphology and ecological adaptation, differentiating three subspecies [18]:
  • L. mutabilis, chocho common name (northern Peru and Ecuador), with a high degree of branching, very late maturing, greater hairiness in leaves and stems; some ecotypes behave as biennials, tolerant to anthracnose.
  • L. mutabilis, tarwi common name (central and southern Peru), with few branches, medium late maturing, somewhat tolerant to anthracnose.
  • L. mutabilis, tauri common name (altiplano of Peru and Bolivia), with few branches, smaller plant (1–1.40 m), with a developed main stem, susceptible to anthracnose.
Additionally, in Bolivia, according to the vegetative cycle, the geographical region of adaptation, and diversity, the cultivated tarwi is divided into three races [20]:
  • Early Titicaca, late Titicaca, Cochabamba.
  • Early South (Chuquisaca-Potosí).
  • Late South (Potosí).
Germplasm collections of L. mutabilis were initiated in 1974 by Dr. Oscar Blanco at the University of Cusco (Peru), and shortly thereafter, collections were conducted in Bolivia and Ecuador. In addition to the Germplasm Banks of Peru, Ecuador, and Bolivia, there are smaller collections in Chile, Argentina, Colombia, Australia, Russia, Poland, Germany, Spain, Hungary, the United Kingdom, and Portugal [17]. However, the number of accessions conserved in these centers mainly represents the varieties and/or species collected by researchers in the area, and not the total existing agro-biodiversity [2].
In South America, the main centers for the conservation of the germplasm of L. mutabilis are the PROINPA Foundation (Toralapa and Pairumani) in Bolivia; the Instituto Nacional de Innovación Agraria (INIA) in Peru, with locations in Kayra (Cusco), Santa Ana (Huancayo), Camacani (Puno), Canaan (Ayacucho), and Baños del Inca (Cajamarca); the Gorbea Experimental Station (Temuco) in Chile; and Instituto Nacional de Investigaciones Agropecuarias (INIAP) in Mejía (Santa Catalina Experimental Station), Ecuador [2,27].
The largest collection of germplasm of L. mutabilis is in Peru, with more than 2000 collected accessions [6]. The Santa Catalina Experimental Station of INIAP-Ecuador has a collection of 529 accessions of 17 species of Lupinus. Among them, 257 accessions were collected in Ecuador and 272 in other countries. In a preliminary characterization of 120 accessions of L. mutabilis, wide variability in earliness, reaction to diseases, and flower color was found [28]. In Bolivia, 595 accessions are maintained in germplasm banks located in La Paz and Cochabamba [6,29] (Table 1).
The tarwi diversity identified in the gene banks is wide, as is shown by several phenotypic traits, such as the growth periods, branching patterns (branches from 0 to 52), color and shape of grains and flowers, and flowering times [28,31,32]. This wide diversity has also been revealed by molecular markers. The genetic variability of 30 accessions of Peruvian origin was evaluated using 65 ISRR (Inter Simple Sequence Repeat) primers, of which the ISSR primers (AG)8YT and (AG)8YC were the most polymorphic, both within each accession and between accessions; of the remaining ISSR primers showed a high content of intra-accession polymorphic information (Table 2). The average percentage of polymorphism was 58.82 [32].
Similar results were obtained when using six ISSR primers (Table 2) to characterize the genetic variability of 23 accessions of L. mutabilis. These primers revealed an average polymorphism of 30.55%. In this study, the (AG)8YG, (AG)8YC, and HVH(TG)7 primers were the most suitable for distinguishing accessions. Additionally, they verified that genetic variability did not correlate with phenotypic variability, indicating the need to incorporate more molecular markers [33]. In the same study, the genome size of L. mutabilis ranged between 1.94 pg/2C and 2.13 pg/2C and, according to the authors, it was the first intraspecific analysis of the genome size of L. mutabilis, which represented an overall average size of 2.05 pg (2001.2 Mbp) [33].
Two recent studies evaluated accessions from the Ecuadorian germplasm bank on four environments (Portugal, Ecuador, and two locations in The Netherlands), and high phenotypic variability has been reported for some characteristics, such as the flowering time, plant height, number of branch orders, vegetative yield, pods and seeds on the central axis, total number of pods and seeds per plant, and seed weight. High heritability values were reported for flowering (0.88), plant height (0.82), and production of pods and seeds on the main stem (0.6), as well as a strong correlation between plant height, flowering time, and seed yield [34,35]. In addition, using a genome wide association study (GWAS), 10 markers linked to flowering time, plant height, vegetative yield, and number of pods and seeds on the main stem were identified (Table 3). Most of the reported SNPs were identified as single location markers. The reference genome used in this study was L. angistifolius [35].
L. mutabilis shows wide diversity in its plant architecture, plant height, grain and flower color [13,32]; likewise, it varies in crop cycle, protein, oil and alkaloid content, yield, and tolerance to insect pests and diseases [1]. This variability has been detected within and between populations. This species exhibits 5 to 10% of intra-specific cross-pollination and inter-specific crosses with wild Lupinus species [21]. This event is interesting from the point of view of plant breeding as genes of interest from wild species could be introduced into the tarwi; however, this complicates the development of uniform and stable genotypes.

5. Breeding Methods Used in the Region

The genetic variability that has been found in the germplasm of L. mutabilis collected in Ecuador, Peru, and Bolivia has allowed a wide margin of selection for identifying materials with good agronomic characteristics [21,36]. Therefore, the genetic improvement of L. mutabilis in the Andes was mainly based on selection within native ecotypes to adapt lines to specific conditions. In this way, several cultivars have been obtained through selection within heterogeneous populations and not properly as a result of hybridization programs [37].
Mass selection has been employed as the main breeding method for the development of new tarwi cultivars in Ecuador, Peru, and Bolivia. The method consisted of evaluating landraces or accessions from the germplasm bank in farmers’ fields and experimental stations, selecting the best individual plants. In the following cycle, the seeds of the selected plants were sown in individual rows (plant-row), and the best plants were selected again. This evaluation and selection process was carried out for several cycles until promising lines were obtained. Subsequently, these lines were evaluated in yield trials in several locations or environments to identify the best genotype [13,38,39,40,41].
In 2008, breeders of INIAP (Ecuador) began the improvement of tarwi through hybridization, making the first crosses among accessions from the germplasm bank to generate new cultivars that could improve the performance of the widely used commercial cultivar, “INIAP 450 Andino” [22,41]. At present, two promising lines have been generated using the Genealogical or Pedigree Method [42], and they have been tested in several locations. However, to the best of our knowledge, no improved varieties of L. mutabilis have been released through hybridization in the Andean Region. Additionally, molecular tools and mapping populations for studying the genetic basis of L. mutabilis are not available. Molecular studies with tarwi have focused on understanding the phylogeny [26,43] and characterizing the genetic variability of this species [32,33].

6. Breeding Targets in the Region

The most important traits evaluated in tarwi have been the earliness, plant architecture, yield, protein and oil content, tolerance to anthracnose, plant height, and alkaloid content [3,38,41,44,45,46].

6.1. Breeding for Low Content Alkaloid

The selection of tarwi genotypes with a low alkaloid content has been an important objective since the beginning of the breeding programs in Bolivia and Peru [4,13,36,38]; meanwhile, in Ecuador, the breeding (by crossing) for low alkaloid content began in 2018 [10] (Figure 4). The presence of alkaloids in the grains of tarwi has been a key limiting factor to the wide-scale expansion of this crop [21,47,48]. The content and composition of alkaloids in grains depend on many factors, including the genotype, biotic/abiotic stress, and edaphoclimatic conditions [49,50]. The content of alkaloids in the Peruvian germplasm showed great variation and presented quantitative inheritance [4]. Later, it was discovered that the inheritance of the trait was recessive, as only 12% of the F2 plants had low alkaloid content [4]. The main alkaloids reported in L. mutabilis are lupanine, sparteine, 3-hydroxylupanine, 13-hydroxylupanine, and 4-hydroxylupanine [47]. Although the chemistry of quinolizidine alkaloids has been extensively studied, information concerning the genetic basis and the proteins involved in the production of the alkaloids in L. mutabilis remains unknown [49].

6.2. Breeding for Resistance to Anthracnose

Anthracnose is the most important disease in L. mutabilis, causing significant yield losses [36,51,52]. Anthracnose was previously reported to be caused by the fungus Colletotrichum gloeosporioides [53], but more recent research claimed that the disease is caused by C. acutatum [51,53,54]. The environmental conditions that favor the development of the disease are high precipitation and high temperature [55].
Typical symptoms of the disease include twisting of stems, petioles, and pods with necrosis. When mature, the acervuli produce aggregates of conidia in orange mucilaginous masses. Tissues above the infection area could collapse [52] (Figure 5). The pathogen can enter the interior of the infected pod and affects the seed—this is the main way of spreading the disease [55]. Contaminated seeds appear thin (sucked). Plants that are born from infected seeds show symptoms in the cotyledons and stems, sometimes killing the plant [21].
One of the objectives of the breeding program of tarwi in the Andean region has been the development of cultivars with resistance to anthracnose [3,22,41,46]; however, to date, only one variety has been reported with tolerance to anthracnose: the Peruvian variety ‘Huamachuco’ [2].
In Ecuador, studies have been carried out using artificial inoculations in the field and greenhouse since 2007 to identify plants with resistance or tolerance to anthracnose in several accessions from the INIAP Germplasm Bank (Table 4).
As a result of several studies using accessions from the germplasm bank of Ecuador and isolates of C. acutatum, an inoculation methodology has been defined to allow the selection of genotypes with resistance or tolerance to anthracnose. In addition, a series of steps has been described for the development of a breeding program to obtain varieties that are resistant to anthracnose in Ecuador [51] (Figure 6).

7. Improved Varieties of L. mutabilis Obtained in the Andean Region

7.1. Bolivia

All commercial varieties have been generated from the selection of the best local ecotypes or landraces; however, many of these have not been used extensively [13]. In Potosí, local varieties known as ‘Chumpi tarwi’ are planted, which have a dark brown grain color and are widespread in the region. Other varieties, such as ‘Tarwi Ñawi’ (dark-colored in the embryo part) and ‘Blanca’ (large white seed), are not widely used [58]. In 2013, the Foundation PROINPA began the genetic improvement of tarwi, evaluating local genotypes collected in different parts of the country [3]. Among the limitations of tarwi cultivation, it was identified that in conditions of fertile soil and high humidity, the plants grew too tall (up to 2.5 m), their cycle was quite long, and they produced non-uniform maturation, which made mechanized cultivation impossible. Therefore, among the main improvement objectives, the PROINPA Foundation considered obtaining plants for an early cycle, with uniform maturation and a high yield [13], managing to generate two cultivars that are in the process of being officially registered with the names ‘Jayata’ [3,38] and ‘Candela’ [13] (Table 5).

7.2. Peru

Between the years 1980 and 1991, the National Institute of Agrarian Research (INIA) and the National Universities released white and other colored grain varieties [61]; however, these varieties have not been adequately disseminated and it is difficult to find pure materials [21]. Furthermore, they have rarely resulted in the official registration of cultivars [20]. In later years, a series of varieties with outstanding characteristics in terms of yield, crop cycle, and lower alkaloid content were released, but with enormous susceptibility to insect pests, diseases, and adverse weather conditions [62]. At present, there are few varieties from Cusco, Huancayo, and La Libertad that have reached yields of over 3000 kg ha−1 [21] (Table 5). Despite the numbers of new cultivars released in Peru, tarwi cultivation is still carried out using local ecotypes, typical of each region, which are characterized as being heterogeneous populations, very late, and very susceptible to anthracnose, rust, Ascochyta, and insect pests [61].

7.3. Ecuador

The history of plant breeding for L. mutabilis began in 1983, with the collection and formation of the germplasm bank at the INIAP-Santa Catalina Experimental Station. Between 1987 and 1996, promising materials were characterized and selected. In 1999, the first improved variety (through mass selection)—‘INIAP 450 Andino’—was released, coming from an accession of Peruvian origin. This is an early variety (6 to 7 months of cultivation), of wide adaptability, with a large grain size, white grain color, and high yield. Today, it is estimated that more than 70% of the planted area in the country is grown with this variety (5000 ha approx.).
In 2010, in a joint effort with the University of Bolívar, using mass selection, the second improved variety—“INIAP 451 Guranguito”—was released in the province of Bolívar [41] (Table 5). This variety has tolerance to foliar diseases, a large grain size, white grain color, intermediate cycle, and market acceptance [60].
It is important to highlight the importance of the ‘Inti’ variety, which is the first variety of L. mutabilis with a low alkaloid content (0.0075%), generated at the Gorbea Experimental Station in Chile. The ‘Inti’ cultivar was evaluated in the Peruvian Andes, where the obtained yields were in the range of 121 to 1216 kg ha−1 [12]. In addition, ‘Inti’ showed an enormous susceptibility to insect pest, diseases, and adverse weather conditions [45].

8. Brief Overview of Tarwi Breeding Progress in Europe

There is growing interest for L. mutabilis in Europe to generate cultivars that adapt to Mediterranean environmental conditions. In the 1990s, two European research projects took place: “Lupinus mutabilis: Its adaptation and production under European pedoclimatic conditions” and “Adaptation of L. mutabilis to European soil and climate conditions”. The interest of Europe continued in 2020 with the LIBBIO European project (No 720726, Horizon 2020), entitled “Lupinus mutabilis for Increased Biomass from marginal lands and value for BIOrefineries” “http://www.libbio.net” (accessed on 12 July 2023). In these projects, several ecotypes of L. mutabilis have been phenotypically and genetically characterized in Germany, the United Kingdom, Poland, France, Portugal, Greece, Spain, Austria, Iceland, the Netherlands, and Romania. After some years of experimentation and research, some L. mutabilis accessions have finally been identified; as a result, they are partially adapted to the European agroecological conditions [59].
The investment that European countries have made into research on the cultivation of tarwi shows that it has great commercial potential; however, in the Andean region—the center of origin—its cultivation is still undervalued, lacking significant investment in research. Lupinus species of Mediterranean origin, such as L. albus and L. angustifolius, are better studied, and they have a wide selection of genomic tools and molecular markers available for traits such as the alkaloid content, flowering time, and resistance to anthracnose disease [63]. These resources could be applied to L. mutabilis to significantly accelerate the improvement of tarwi in the Andean Region.

9. Breeding Perspectives

The high content of quinolizidine alkaloids in the seed is one of the most important factors that have slowed down the potential use of this crop. Before consumption or processing, an alkaloid elimination process is necessary, which involves time (about 3 to 7 days), use of natural resources such as water, and additional financial resources for adequate equipment and infrastructure. This process makes the final product more expensive. Additionally, the susceptibility to biotic and abiotic factors, the indeterminate growth, and non-uniform maturation of the central axis and lateral branches (which complicates the mechanization of the crop) are other aspects that prevent the further commercial development of the crop [36]. These limitations could be overcome through diverse breeding strategies. The wide genetic variability preserved in the germplasm of L. mutabilis and in the wild species of Lupinus that grow in the Andes offers the opportunity to carry out intra- and inter-specific crosses to generate promising materials with great potential for the region.
Within the collections of L. mutabilis conserved in the germplasm banks of the Andean region, there are accessions and/or varieties with a low content of alkaloids, earliness, high yield, and plant architecture. These genotypes are important in breeding programs to generate “sweet” varieties. However, before starting crosses, homozygous materials must be obtained (for the characteristics of interest) to ensure the self-fertilization of the selected plants during several reproductive cycles. Thanks to the degree of cross-pollination, it is very likely that some plants of tarwi present characteristics of interest, even if they show recessive inheritance, as is presumably the case for the content of alkaloids in tarwi; therefore, they will segregate, and after a few production cycles, the number of plants with these characteristics could decrease drastically.
On the other hand, the importance of wild species lies in the wide geographic variability of adaptation so that they are asources of genes for resistance to biotic and abiotic factors. At present, preliminary characterization studies of these species are already available in Bolivia [64], Peru [65], and Ecuador [66]. Wild species from the Andean region are presumed to share the same chromosome number as L. mutabilis [21,67]. With wild species, evaluations must be carried out for resistance to diseases and pests of economic importance. In the case of anthracnose (the most important disease), specific inoculation methodologies are already available that would allow the evaluation and selection of resistant genotypes. Otherwise, the information related to the study of insect pests, evaluation methodologies, and the selection of resistant cultivars is almost nil, despite the fact that insect pests are important limiting factors in some tarwi production areas.
Another important aspect will be to evaluate the behavior of sweet varieties or accessions in terms of their susceptibility to pests and diseases, for which standardized evaluation methodologies will be important. This will better guide the selection of parents in the breeding program and agronomic management in the field for future varieties with a low alkaloid content.
To optimize this genetic improvement process, it is necessary to include molecular tools and generate genomic information, which is still very scarce for L. mutabilis. At present, the new generation sequencing technologies allow the generation of a large amount of genomic information at a lower cost compared to the previous technologies; for example, they enable genome-wide association studies (GWAS) to identify and establish genetic markers [17]. In addition, it is necessary to initiate crosses between homozygous plants for the characteristics of interest, to generate mapping populations, and, together with the use of molecular tools, obtain genomic information that allows for accelerating genetic improvement. It is also important to mention that genomic information is available for L. angustifloius and L. albus, which can be applied to the improvement of L. mutabilis.
One of the breeding methods that has been widely used in L. mutabilis is mutation induction [10,68,69,70], through which materials with a low content of alkaloids and plants without branching have been obtained. The use of this method is feasible for further expanding the variability of L. mutabilis for these and other characteristics of interest. Branchless plants provide the opportunity to obtain new varieties for mechanized harvesting.
At present, the availability of molecular resources for the breeding of L. mutabilis remains limited, without a reference genome, without genetics map, and without reported genes. However, the use of new technologies, such as gene editing, offers the opportunity to generate commercial varieties in the short- and medium-term. In the Andean region, adapted and highly productive but bitter varieties are cultivated. With gene editing, it is possible to optimize the generation of sweet varieties that commercially promote the cultivation of tarwi, not only regionally, but globally. For this, it is essential to advance with genomic information of this crop.

10. Conclusions

At least 25 varieties of L. mutabilis have been generated in the highlands of Ecuador, Peru, and Bolivia in the last 40 years. These varieties were primarily developed using mass selection breeding methods. Some of the ecotypes or varieties generated using these breeding methods are not officially registered or released. To date, no varieties that come from crosses or hybridization have been released; however, in Ecuador, there are already two promising lines developed by crosses using the Pedigree breeding method.
Despite the achievements shown in terms of the number of varieties released, there are still some limitations to the cultivation of tarwi: no varieties resistant to anthracnose have been obtained; the vast majority of the varieties grown in the Andean region have a high alkaloid content. There is a variety with a low alkaloid content, but it is susceptible to diseases and pests. No breeding studies for pest resistance have been conducted; the use of molecular tools for the breeding of L. mutabilis in the Andean region is almost null.
Due to the multiple advantages in agriculture and the benefits in nutrition and medicine, L. mutabilis is gaining global importance; however, it will be necessary to implement new breeding strategies and start studies at the molecular level—for example, GWAS and gene editing—which will optimize genetic gains and reduce the time to obtain new varieties.

Author Contributions

Conceptualization, D.R.-O., J.L.Z., A.T. and S.P.-L.; methodology and search of literature, D.R.-O.; writing—original draft preparation, D.R.-O.; writing—review and editing, D.R.-O., J.L.Z., A.T. and S.P.-L.; supervision, J.L.Z., S.P.-L. and Á.M. All authors have read and agreed to the published version of the manuscript.

Funding

Radicle Crops, The Netherlands and Universidad San Francisco de Quito, Instituto Nacional de Investigaciones Agropecuarias (INIAP), and Fondo de Investigación en Agrobiodiversidad, Semillas y Agricultura Sustainable (FIASA), Ecuador.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 14 00094 g001
Figure 1. (a) Prominent (main axis rises above the branch) and no prominent stem (central axis similar height or smaller than the branches) of tarwi; (b) Prominent and no prominent stem of tarwi; (c) Terminal inflorescences in tarwi; (d) Corolla with five petals in the flower of tarwi, one petal for the standard, two for the keel and two for the wings.
Figure 1. (a) Prominent (main axis rises above the branch) and no prominent stem (central axis similar height or smaller than the branches) of tarwi; (b) Prominent and no prominent stem of tarwi; (c) Terminal inflorescences in tarwi; (d) Corolla with five petals in the flower of tarwi, one petal for the standard, two for the keel and two for the wings.
Agronomy 14 00094 g001
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Figure 2. (a) White, blue, pink, and violet colors of the tarwi flowers; (b) flower color intensity varies from the beginning of its formation (upper part of the inflorescence) to maturation (lower part of the inflorescence) in tarwi; (c) main stem pods of tarwi.
Figure 2. (a) White, blue, pink, and violet colors of the tarwi flowers; (b) flower color intensity varies from the beginning of its formation (upper part of the inflorescence) to maturation (lower part of the inflorescence) in tarwi; (c) main stem pods of tarwi.
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Figure 3. Production areas of tarwi in Ecuador, Peru and Bolivia.
Figure 3. Production areas of tarwi in Ecuador, Peru and Bolivia.
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Figure 4. Scheme used in the INIAP-Ecuador breeding program to generate varieties of tarwi with low content of alkaloids in the seeds.
Figure 4. Scheme used in the INIAP-Ecuador breeding program to generate varieties of tarwi with low content of alkaloids in the seeds.
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Figure 5. Anthracnose typical symptoms: (a) mature infection on the stem; (b) twisting of stems; (c) collapse tissues above the infection; (d) mature infection on the pod.
Figure 5. Anthracnose typical symptoms: (a) mature infection on the stem; (b) twisting of stems; (c) collapse tissues above the infection; (d) mature infection on the pod.
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Figure 6. Scheme of a tarwi breeding program for resistance to anthracnose [51].
Figure 6. Scheme of a tarwi breeding program for resistance to anthracnose [51].
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Table 1. Number of accessions of L. mutabilis conserved in germplasm banks in the Andes [6,28,29,30].
Table 1. Number of accessions of L. mutabilis conserved in germplasm banks in the Andes [6,28,29,30].
Germplasm BankCountryNumber of Accessions ConservedReference
Experimental Station La Molina, INIA, LimaPeru50[30]
Experimental Station Andenes, INIA, CuscoPeru20[30]
Experimental Station Baños del Inca, INIA, CajamarcaPeru347[30]
Experimental Station Canaan-Huamanga, INIA, CajamarcaPeru11[30]
Universidad Nacional del Altiplano (UNAP)Peru319[30]
Centro de Investigación de Cultivos Andinos (CICA), CuscoPeru1800[6]
Centro de Investigación y Producción,
Camacani-UNA, Puno		Peru260[6]
Experimental Station Santa Ana, INIA, HuancayoPeru1725[30]
Instituto Nacional de Investigaciones
Agropecuarias, Mejía		Ecuador381[28]
Universidad Tecnica de Ambato (UTA),
Ambato		Ecuador50[30]
Fundación para la Promoción e Investigación de Productos Andinos, La PazBolivia20[6]
Centro de Investigaciones Fitoecogenéticas (CIFP), Pairumani, CochabambaBolivia114[6,30]
Universidad Mayor de San Andrés (UMSA), La PazBolivia340[6]
Instituto Nacional de Innovación
Agropecuaria y Forestal (INIAF)		Bolivia123[29,30]
Universidad Nacional de Colombia (UNC), Bogotá.Colombia20[6]
Instituto Colombiano Agropecuario (ICA), BogotáColombia40[6]
Cenrtro Regional de Investigacion Carillanca, INIA, TemucoChile1[6,30]
Universidad Astral de Chile, ValdiviaChile3[6,30]
Universidad de TemucoChile180[6]
Instituto Nacional de Tecnología
Agropecuaria (INTA), Buenos Aires		Argentina180[6]
Total 5984
Table 2. Sequences of the most polymorphic ISSR primers in accessions of L. mutabilis.
Table 2. Sequences of the most polymorphic ISSR primers in accessions of L. mutabilis.
PrimerSequenceReference
(AG)8YTAGAGAGAGAGAGAGAGYT[32,33]
(AG)8YCAGAGAGAGAGAGAGAGYC[32,33]
(AG)8AGAGAGAGAGAGAGAG[32]
(AG)8YGAGAGAGAGAGAGAGAGYG[33]
(GA)8YCGAGAGAGAGAGAGAGAYC[32]
(GA)8YGGAGAGAGAGAGAGAGAYG[32]
(GA)8YTGAGAGAGAGAGAGAGAYT[33]
(GA)8CGAGAGAGAGAGAGAGAC[32]
(GT)8YCGTGTGTGTGTGTGTGTYC[33]
DBD(AC)7DBDACACACACACACAC[32]
HVH(TG)9HVHTGTGTGTGTGTGTGTGTG[32]
HVH(TG)7HVHTGTGTGTGTGTGTG[33]
Table 3. SNPs markers reported for time flowering, pods on the main stem, plant height, and vegetative [35].
Table 3. SNPs markers reported for time flowering, pods on the main stem, plant height, and vegetative [35].
MarkersTraitsChrPositionEnvironment
M11034Flowering time (days), Pods on the main stem (number)LG135,615,305All Env, PT, NL-Sc
M7399Flowering time (days)LG087,668,768All Env, NL-Wi
M7412Flowering time (days)LG087,670,152All Env
M7413Flowering time (days)LG087,680,541All Env
M7670Flowering time (days)LG0816,132,804All Env
M396Plant height (cm)LG0115,690,000EC
M10925Vegetative yield (g)LG1218,150,269NL-Sc
M14832Pods on the main stem
(number)		LG183,860,231EC
M14675Pods on the main stem
(number)		LG1720,841,361NL-Wi
M7272Pods on the main stem
(number)		LG084,062,540All Env
Table 4. Studies carried out to identify accessions with resistance to C. acutatum through inoculations using germplasm of the National Bank, Ecuador.
Table 4. Studies carried out to identify accessions with resistance to C. acutatum through inoculations using germplasm of the National Bank, Ecuador.
YearNo. of Accessions EvaluatedStudy ConditionsInoculation MethodTolerant GenotypesReference
2007126GreenhouseSpraying with an inoculum concentration 106 UFC/mLNeither[41]
201370GreenhouseSpraying 3 months after sowing with an inoculum concentration of 105 UFC/mLECU-674, ECU-701, ECU-702, ECU-2332 ECU-713[56]
20147FieldSpraying at 2 and 3 months after sowing with an inoculum concentration of 105 UFC/mLECU-2658, ECU-2700[57]
Table 5. Origin and characteristics of the Varieties and Ecotypes of L. mutabilis generated in Ecuador, Peru and Bolivia (1980–2020).
Table 5. Origin and characteristics of the Varieties and Ecotypes of L. mutabilis generated in Ecuador, Peru and Bolivia (1980–2020).
Country of OriginName of the VarietyLocality of SelectionInstitutionsCharacteristicsReference
Peru“Alta gracia”E. E. Santa AnaINIA-HuancayoHigh yield[2,21]
Peru“Andenes-80”E. E. Andenes-CuscoINIA-CUSCOHigh yield[2,21]
Peru“Carlos Ochoa”Kayra-CuscoCICA-UNSAACHigh yield[2]
Peru“Cajamarca”CajamarcaUniversidad Nacional de Cajamarca---[21]
Peru“Cholo fuerte”ÁncashCEDEPGrain white[21,27]
Peru“Cusco”Kayra-CuscoCICA-Universidad Nacional San Antonio Abad del Cusco (UNSAAC)White flower[2]
Peru“Cusco 1”CuscoUNSAACMedium grain and white[21,27]
Peru“Cusco 2”CuscoUNSAACLow content of alkaloids[21]
Peru“Fortunato” “Herrera”Kayra-CuscoCICA-UNSAACHigh yield[2]
Peru“H6”E. E. HuancayoUniversidad NacionalHigh yield[2,21]
Peru“Huamachuco”E. E. Baños del IncaINIA-CAJAMARCAAnthracnose tolerant, late[2]
Peru“Kayra”E. E. AndenesINIA-CUSCOHigh yield[2]
Peru“Puno”E. E. IlpaINIA-PUNOEarly, small plant[2,36]
Peru“SacacataniE. E. CamacaniUNA-PunoHigh yield, late[2]
Peru“SCG-1 al SCG-4”E. E. CamacaniUNA-PunoEarly[2]
Peru“SCG-25”Kayra-CuscoCICA-UNSAACHigh yield, White and black seed[2,36]
Peru“SCG-9”Kayra-CuscoCICA-UNSAACHigh yield, white seed[2,36]
Peru“Yunguyo”E. E. IlpaINIA-PUNOHigh yield[2,21]
Bolivia“Chumpi tarwi”Potosí---Local dark brown grain ecotypes[19]
Bolivia“Tarwi Ñawi”Potosí---Local grain ecotypes of white color and dark color in the part of the embryo[19]
Bolivia“Toralapa”E. E. PayrumaniINIAP-CochabambaHigh yield, late[2,59]
Bolivia“Carabuco”E. E. PayrumaniINIAP-CochabambaHigh yield, late[2,19]
Bolivia“Jayata”CochabambaPROINPA-CochabambaUniform maturation, white seed[13,38]
Bolivia“Candela”CochabambaPROINPA-CochabambaLow content of alkaloids[13]
Ecuador“INIAP-450 Andino”E. E. Santa CatalinaINIAP-EcuadorHigh yield[39]
Ecuador“INIAP-451 Guaranguito”E. E. Santa CatalinaINIAP-EcuadorFoliar disease tolerant[60]
Chile“Inti”E. E. GorbeaSemillas BaerFree of alkaloids[2]
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Rodríguez-Ortega, D.; Zambrano, J.L.; Pereira-Lorenzo, S.; Torres, A.; Murillo, Á. Lupinus mutabilis Breeding in the Andes of Ecuador, Peru, and Bolivia: A Review. Agronomy 2024, 14, 94. https://doi.org/10.3390/agronomy14010094

AMA Style

Rodríguez-Ortega D, Zambrano JL, Pereira-Lorenzo S, Torres A, Murillo Á. Lupinus mutabilis Breeding in the Andes of Ecuador, Peru, and Bolivia: A Review. Agronomy. 2024; 14(1):94. https://doi.org/10.3390/agronomy14010094

Chicago/Turabian Style

Rodríguez-Ortega, Diego, José Luis Zambrano, Santiago Pereira-Lorenzo, Andrés Torres, and Ángel Murillo. 2024. "Lupinus mutabilis Breeding in the Andes of Ecuador, Peru, and Bolivia: A Review" Agronomy 14, no. 1: 94. https://doi.org/10.3390/agronomy14010094

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