1 IMPROVEMENT OF ( quinoa Wild.) AND QAÑAWA 2 (Chenopdium pallidicaule Aellen) IN A CONTEXT OF CLIMATE CHANGE IN 3 THE HIGH 4 5 Alejandro Bonifacio1 6 7 1 Fundación PROINPA, La Paz, Bolivia. [email protected] 8 9 Abstract 10 Quinoa and qañawa are the only native crops that produce food in the high Andes. 11 The improvement of quinoa has been addressed by government institutions, universities 12 and NGOs, obtaining improved varieties. However, qañawa has received little or no 13 attention in development of varieties and only has native varieties and revalued varieties. 14 The native and improved varieties of quinoa have contributed to food production for rural 15 families and also for export, generating significant economic income. In recent decades, 16 the production of these is being negatively affected by effects of climate change. 17 In the high Andes, climatic variability together with climate change is disturbing the 18 regime of climatic factors with evident changes represented by drought, frost, hail and 19 wind. The objective of this paper is to describe the context under climate change, followed 20 by a review of the progress in the improvement of quinoa and qañawa and then propose 21 some adjustments to improvement methods for the high Andes. The genetic methods and 22 materials used in the improvement of quinoa have allowed to obtain varieties with 23 characters prioritized for the last decades, which met and continue to fulfill their role in 24 food production and income generation for producers. However, in the face of the effects 25 of climate change, some varieties are becoming unfitted, especially those of long cycle. 26 Therefore, it has been proposed to include new breeding objectives as well as new genetic 27 materials for improvement, new sources of characters and suggesting some improvement 28 methods in the context of climate change. 29 30 Keywords: Improvement, quinoa, qañawa, climate change 31 32 33 34

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35 1. Introduction 36 37 The Andes is an area where crops that produce grains, tubers and food roots have been 38 domesticated and developed for the inhabitants of this area. In the high part of the Andes 39 (high Andes), that is to say between 3800 and 4500 m.s.l, the main producing grain crops 40 are quinoa and qañawa. These crops were domesticated, conserved and used by men and 41 women of the predecessor civilizations such as Tiahauancota and Incaica. Subsequently, 42 these genetic resources were taken advantage of by contemporary generations. 43 44 Until the 1980s, quinoa and qañawa were produced for the subsistence of rural families 45 and for local market. Since the 90s, thanks to the discovery of its outstanding nutritional 46 properties and the promotion of its consumption, quinoa has entered the national and 47 export markets, reaching the highest demand between 2013 and 2014. According to 48 Montero and Romero (2017), in 1998 the world production of quinoa was 49,400 t, of 49 which 20,921 t produced Bolivia and 28,171 t ; for 2016 world production reached 50 148,720 t where Bolivia participated with 65,548 t and Peru with 79,269 t. The reports 51 show an increase in quinoa production by 200% over a period of 15 years. 52 53 The demand for quinoa in the market has led to increased production mainly based on the 54 expansion of the area under cultivation, reaching in some areas to become a monoculture 55 of quinoa with the negative consequences for the sustainable production of quinoa (Risi, 56 Rojas & Pacheco, 2015). 57 58 The qañawa has not had the same demand in the market, so production continues to be 59 on a smaller scale, although there is some increase in the acceptance of the product in the 60 local market and in the export market. 61 62 As the international market for quinoa increased, the consequences of climate change 63 became more evident with adverse effects on the quinoa and qañawa production. 64 According to Risi, Rojas and Pacheco (2015), yields of quinoa show a decrease, which 65 they attributed to monoculture and low soil fertility. However, it is very likely that the 66 factors derived from climate change are contributing to the decline in yield. 67

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68 On climate change, various concepts have been raised. According to Useros (2013), the 69 generally accepted concepts are two, "that of the IPCC and that of the UN Framework 70 Convention. The first focuses on the identifiable change in climate, regardless of whether 71 it is due to natural variability or that resulting from human activity, and the second, refers 72 to the change induced by human activity, either directly or indirectly and that adds to the 73 natural climatic variability " 74 75 The adverse climatic phenomena in the high Andes are drought, frost, hail and wind. 76 These adverse factors affect quinoa and qañawa, but the effects are differentiated for 77 species and within varieties of the same species. 78 79 In this context, the genetic improvement of quinoa and qañawa must play an important 80 role in obtaining varieties adapted to the new context and satisfying the quality 81 requirements of the product demanded in the local and export markets. 82 83 With the described background, in the present work a brief description of the context is 84 made, the revision of the advances in the improvement of quinoa and qañawa in the high 85 Andes, the methods used and varieties generated to date. Then, propose some adjustments 86 in the methods of improvement of quinoa and qañawa in a context of climate change. 87 88 2. The adverse effects of climate change in the high Andes 89 90 The agriculture of the high Andes, has always been developed in an environment of 91 climatic variability, the phenomena of drought and frost were present in a range of 92 variation that the farmers managed based on local technologies and management of 93 agroecosystems. However, with the effects of climate change, the varietal component 94 requires adjustments so that the production of quinoa and qañawa can adapt to climate 95 change. 96 97 In much of South America, the episodes of El Niño and La Niña are those that affect the 98 temporal and spatial distributions of rain, with episodes of El Niño with below-normal 99 rainfall and La Niña episodes with rainfall more than of the normal (Herzog et al., 201d 100 and Vuille, 2013).

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101 According to projections, until the middle of the 21st century or until the end of the 102 century, in the high plains and the subtropical Andes, the tendency is to decrease 103 precipitation by up to 10% with evidence of severe impacts of the climatic extremes that 104 are occurring or that may occur in the region (Herzog et al., 2012). 105 106 In the Bolivian highlands, the adverse factors related to climate change are drought, frost, 107 hail, and wind among others. These factors negatively affect the production of crops at 108 different stages of their development. 109 110 2.1. Drought 111 112 In the highlands, the drought occurs at the beginning and at the end of the rainy season 113 (García et al., 2015). In the rain fed agriculture system, drought may occur at sowing 114 time, in the stage of vegetative development and in the reproductive phase of quinoa and 115 qañawa. 116 117 The drought in the sowing season leads to postpone sowing. If it causes failures in the 118 emergence of seedlings, it leads to repeat sowing or cancel the sowing. In the vegetative 119 phase, drought causes growth retardation, with the consequent lengthening of the 120 productive cycle; while in reproductive phase drought accelerates maturation. Quinoa has 121 outstanding capacity for adaptation to drought and other adverse conditions, thus, it has 122 valuable potential for future challenges of climate change (Zurita et al., 2014). 123 124 In relative terms, quinoa tolerates drought better than qañawa, however, the precocity of 125 the qañawa and the low sensitivity to photoperiod allow the qañawa to reach its 126 productive cycle even if the planting date is delayed. 127 128 2.2. Frost 129 130 In general, when frost occurs on fields with quinoa and qañawa cultivation, quinoa is 131 more affected than qañawa. Qañawa is frost-tolerant species and can report high yields in 132 marginal soil conditions (Rojas et al., 2010). On the other hand, in both crops, the 133 sensitivity to frost differs according to the phenological phase in which the is at the 134 time of the occurrence of frost. In the seedling phase, both quinoa and qañawa are highly

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135 tolerant to frost, the susceptibility increases as their development proceeds, being more 136 sensitive in the flowering stage. 137 138 In quinoa, the damage by frost is the freezing of leaf tissue that are immediate and visible 139 effects. However, the frost also causes the death of the epidermal tissue of the stem, its 140 damage is evident in subsequent stages to the occurrence of frost. These damages are 141 considered as the sequels of the frost, since these are observed after the occurrence of 142 frost. The sequels of the frost in the quinoa are longitudinal cracking of the stem, 143 superficial necrosis of the stem tissue and finally the fall of the . 144 145 According to Jacobsen et al. (2007), the quinoa possesses the capacity of overcooling 146 which prevents the damage by avoiding ice formation by means of a moderate 147 overcooling; in addition they report that the quinoa has high levels of sugar that could 148 reduce the freezing point. 149 150 2.3. Hail 151 152 The damages caused by hail in the crops are determined by their characteristics such as 153 the size, amount of hail that falls in a unit of area and the strength of the winds during the 154 occurrence of hail (Bal et al., 2014). 155 156 The crop resistance to hail depends on the physiological state of the plant and soil 157 moisture conditions, since plants that grow with good moisture have greater elasticity and 158 resistance to hail is increased (Sanchez et al., 1996). 159 160 According to the local knowledge of the farmers of the highlands, for decades, the hail 161 had occurred in well-located areas and for a very short period of time. The occurrence of 162 hail was likely at the beginning and at the end of the rainy season. However, in recent 163 years, hail is likely throughout the rainy season, which causes serious damage to crops 164 since in that period the plants are in the development phase. 165 166 The damage caused by hail varies according to growth stages of quinoa. The most 167 sensitive stage is the flowering and beginning of grain filling (García et al., 2015). At 168 sowing, the hail causes soil compaction preventing seedling emergence. In the stage of

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169 juvenile plants, the hail causes breakage of leaves and stem, meanwhile in the flowering 170 phase it leads to the floral abortion and in a mature state causes the fall of the grain. 171 172 The hail leaves sequels in the quinoa plant. The punctual lesions by the hail blow become 173 necrotic over time and become fungal infection sites. The injured and necrotic stem 174 sectors become fragile and break when the wind shakes those causing plants to fall. 175 176 Hail tolerance varies with variety (García et al., 2015). However, there are few records 177 on the characterization of quinoa germplasm due to tolerance to hail damage. 178 179 2.4. Wind 180 181 The wind is another factor whose occurrence has increased in frequency and speed. Until 182 about 30 years ago, the wind had a well-defined seasonal occurrence. In the Bolivian 183 highlands, the month of August was known as the month of winds and the wind speed 184 was not so erosive. Currently, the occurrence of the wind has been extended to the sowing 185 season, plant growth and even at harvest time. The adverse consequences of wind are 186 more damaging in fields with sandy soils. 187 188 In the cotyledonal phases up to the two opposite leaves, the seedlings are buried by the 189 sand carried by the wind. In the vegetative stage, the sand transported by the wind causes 190 injuries to the leaves and stem due to abrasion by the sand transported by wind. In mature 191 (dry) plants, the wind causes grain falling by friction between plants shaken by the wind. 192 In the drying and threshing stage, the wind drags the harvested material causing shattering 193 and mixing the grain with sand. 194 195 3. Advances in the improvement of quinoa and qañawa 196 197 3.1. Improvement of quinoa 198 199 The improvement of quinoa in the Andean highlands began in the 1960s and 1970s, when 200 methods of mass selection, individual selection, panicle-furrow selection, pedigree 201 selection and the backcross method were proposed (Gandarillas cited by Bonifacio, 202 Gomez-Pando and Rojas, 2014). Subsequently, Bonifacio, Gómez-Pando and Rojas

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203 (2014) included other methods such as stratified mass selection, combined individual- 204 mass selection, single descent and the massive method. At that time, the objectives 205 of the improvement were the yield, large grain and free of saponin (Bonifacio, Gómez- 206 Pando and Rojas, 2014 and Gómez-Pando, 2015). Since the 1990s, efforts have been 207 made to obtain early maturing and mildew disease resistant varieties (Bonifacio, Vargas 208 and Aroni, 2014, Bonifacio, Gomez-Pando and Rojas, 2014). Since 2000, hail tolerance 209 has been considered as a selection criterion in quinoa. Gomez-Pando and Aguilar (2016), 210 among selection criteria in quinoa for the highlands indicate tolerance to adverse climatic 211 factors such as frost, drought and hail. 212 213 Initially, the methods to combine characters and the segregation of characters in the 214 process of quinoa improvement, was artificial hybridization (Bonifacio, Gómez-Pando 215 and Rojas, 2014, Gomez-Pando, 2015). Subsequently, induced mutation technique to 216 generate the variation in quinoa was suggested (Gomez-Pando and Eguiluz, 2013, 217 Bonifacio, Gómez-Pando and Rojas, 2014, Gomez-Pando, 2015). On the other hand, the 218 participatory evaluation of genetic materials has been adopted in a scheme of pre- 219 breeding and direct use of germplasm (Rojas et al., 2010). 220 221 The of the plants was carried out since prehistory and with very long 222 processes, where the first domesticated forms were cultivated together with their wild 223 relatives facilitating a genetic flow to maintain the genetic diversity (Prohens et al., 2017). 224 With advances in molecular biology, modern tools are recently being developed for the 225 molecular characterization of genetic diversity and for molecular marker assisted 226 selection (Mason et al., 2005, Jarvis et al., 2008). 227 228 Yassui et al. (2016) worked to obtain a pure line of quinoa (Kd) that allowed them to 229 perform a rigorous molecular analysis and they assembled the genome sequence of Kd 230 line, which provided an important basis for determining the precise roles and numbers of 231 candidate genes and pathways that regulate tolerance to abiotic stress in quinoa. On the 232 other hand, Jarvis et al. (2017) assembled the reference genome sequence for quinoa, this 233 sequence allowed them to identify the transcription factor that probably controls saponin 234 production in quinoa , as well as a mutation in lines of sweet quinoa, stating that 235 these advances in developing modern tools is the first step to accelerate the improvement 236 of quinoa.

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237 The application of the methods of improvement of quinoa in the programs of Bolivia and 238 Peru has allowed obtaining improved varieties. Tables 1, 2, 3 and 4 show the list of quinoa 239 varieties from Peru and Bolivia for highland conditions. 240 241 The improved varieties of quinoa in Peru are sweet, semi-sweet and small to large in seed 242 size (Table 1). The productive cycle of early varieties is in the range of 140 to 150 days, 243 while those of late cycle are 190 days. From the above, it can be deduced that the long- 244 cycle varieties are unsuited to the effects of climate change. 245 246 The varieties obtained by the program of improvement of the former IBTA are of sweet 247 grain and medium sized (Table 2), which coincides with the objectives of the 248 improvement which was to encourage local consumption. On the other hand, it is 249 observed that the improved varieties are adapted to the Central Highlands of Bolivia with 250 a precocious production cycle in relation to Peruvian varieties. 251 252 In recent years, the genetic improvement of quinoa in Bolivia has given greater emphasis 253 to precocity maintaining large grain size with and without the presence of saponin (Table 254 3). It could be said that the varieties of Bolivia have greater options of adaptation to the 255 conditions imposed by climate change due to their escaping characteristics to the adverse 256 climate factors. 257 258 According to Bonifacio, Vargas and Aroni (2014) and Bonifacio, Gómez-Pando and 259 Rojas (2014), most of the varieties recently released in Bolivia are of short growing cycle, 260 resistant to mildew (Jacha Grano, Kurmi and Blanquita) and tolerant to hail (Blanquita). 261 These varieties have greater options to adapt to the conditions generated by climate 262 change. However, it is advisable to have a greater diversity of varieties with these 263 characteristics. 264 265 Real quinoa is composed of 54 native varieties or ecotypes, of which at least 12 are the 266 most important ones (Bonifacio et al., 2012). As it is seen, all the varieties are large 267 seeded and bitter (Table 4). Real quinoa includes early and semi-precocious varieties, so 268 its options for adapting to climate change are high. The method of obtaining it is assumed 269 that it was the mass selection and the conservation of the variety was through the varietal 270 purification by the producers.

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271 According to Apaza et al. (2013), quinoa is very versatile to adapt to different ecological 272 environments, it can grow in desert climate even in hot and dry weather, as it can also 273 withstand temperatures from -8 ° C to 38 ° C thanks to the diversity and genetic 274 variability. 275 276 4.2. Improvement of qañawa 277 278 Qañawa is a relegated crop even in its own center of origin, its distribution outside the 279 high Andes is unknown. The qañawa belongs to the group of so-called forgotten and 280 underutilized crops (Rojas et al., 2010). The cultivation of qañawa occurs exclusively in 281 rural communities located at high altitudes of Bolivia and Peru (3800 to 4500 masl). 282 283 The production of qañawa is on a smaller scale due to a series of technological, 284 biophysical and social limiting factors. However, it has some advantages that can be used 285 in production and consumption. According to Woods and Eizaguierre (2004), the qañawa 286 has an advantage over quinoa, since its seed contain low saponin, which means that it is 287 faster and cheaper to obtain edible flour from the qañawa, while in the quinoa removing 288 saponin is expensive. 289 290 Researchers in Andean crops, agree in qualifying the qañawa as a semi-domesticated 291 species due to the small size of the plant, branched habit and dehiscent grain before and 292 during the harvest. These characteristics of the plant are coincident with the wild complex. 293 Despite the knowledge of the factors that limit the increase in qañawa production, the 294 process of genetic improvement has not been implemented to overcome wild type 295 characters. 296 297 Qañawa plant has very small flower (1.5 mm), being difficult artificial crossing. So the 298 methods of improvement are limited to mass selection and individual selection (Apaza, 299 2010). According to Apaza (2010), the improvement of the qañawa is focused to obtain 300 greater yields and to achieve uniformity in seed maturation. 301 302 Bonifacio (2018), proposed adjusted methods for qañawa improvement, among these 303 mass selection, individual selection, plant-furrow selection, massive conduction of 304 descendants and adjusted single seed decent method.

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305 The improvement of the qañawa was concentrated on evaluation of yield performance of 306 materials conserved in germplasm banks (Pinto et al., 2008). This means the direct use of 307 germplasm genetic material, using the method of mass selection to revalue germplasm 308 accessions. Paucara (2016) and Bonifacio (2017), have reported the results of evaluation 309 of mutant qañawa lines whose grain yield and lower pre-harvest shattering were 310 encouraging to obtain new varieties. 311 312 The list of improved varieties in Bolivia is presented in table 5, which are scarcely 313 disseminated, so it is cultivated on a smaller scale. 314 315 In addition to the varieties detailed in table 5, in the municipality of Toledo, Oruro, three 316 new varieties have been selected: Janco, Samiri and Wila, which have characteristics of 317 tolerance to drought and frost. 318 319 The varieties selected in Peru are Cupi, Ramis and Illpa INIA-406 and a series of 320 multilinear varieties are in the process of being formed (Apaza, 2010). 321 322 On the other hand, in Bolivia there are native varieties such as Last'a, Saiwa or Chilliwa, 323 Wila, Q'illu, Ch'uxña among others (Bonifacio, 2018). In Peru the local varieties are 324 Akcallapi, Chilliwa, Konacota, Lambrana, Pantila, Kello, Condor saya, Chusilla, Pacco 325 chilliwa, Kello huitil, Chusilla, Paco chiliwa, Huanacuri among others (Tapia & Fries, 326 2007). These varieties generally have the productive cycle between 130 and 200 days. 327 328 4. Methods of improving quinoa and qañawa for the context of climate change 329 330 Under climate change, the scenario to work on plant improvement will be given by high 331 temperatures, high CO2 concentration, higher frequency of drought, increase in areas 332 affected by salinity and higher frequency of biotic stress; where conventional breeding 333 and biotechnology can help by developing new varieties that can adapt to stress 334 (Ciccareli, 2008). 335 336 In the highlands of Bolivia, climatic variability together with climate change has 337 disturbing effects on environmental factors, with changes in the regime of climate factors 338 being more evident. To this is added the anthropic effects of the expansion of the

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339 agricultural frontier of cash crops. Therefore, it is necessary to introduce some 340 adjustments in the approach of the genetic improvement of quinoa and qañawa to 341 contribute to adaptation under climate change context. The genetic improvement 342 approach must change because the environmental conditions have changed. It is 343 reasonable to assume that crops domesticated 7000 years ago are being unsuited in the 344 current context, which implies strong improvement work. 345 346 The objectives of genetic improvement should be properly prioritized to develop varieties 347 superior to those already existing, these may include performance, adaptation, resistance 348 to stress and quality; among these, abiotic stress is the biggest factor limiting productivity, 349 so the search for resistance to abiotic factors is the priority (García et al., 2018). 350 351 4.1. Quinoa 352 353 The varieties of quinoa for the context of variability and climate change in the high Andes, 354 should include characteristics of precocity, resistance to drought and tolerance to frost 355 and hail. For this, the use of the genetic diversity present in local varieties as well as 356 application of conventional and modern breeding tools should be considered. 357 358 In the resistance to drought, it is necessary to identify the mechanisms involved, such as 359 escape or tolerance. Escape to drought tends to minimize the interaction of this with the 360 growth of the crop and its yield, while tolerance provides a productive capacity despite 361 the loss of moisture from the plant (García et al., 2018). 362 363 For precocity and escape to drought should be chosen current varieties of shortest growing 364 cycle as possible, then cross these progenitors and favor segregation in F2 and subsequent 365 generations in which it can accumulate favorable genes for superior precocity. The 366 selection methods suggested in order of priority are the mass method, single seed descent, 367 pedigree selection, individual selection and mass selection. Preliminary observations lead 368 to assume that quinoa growing under stress conditions undergoes epigenetic changes that 369 lead to natural segregation as observed in the Real Pandela variety and in others. 370 371 For precocity, it is important to consider wild relatives known as ajara (Chenopodium 372 quinoa var melanospermum). The suggested method for incorporating the genes of

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373 precocity is backcrossing. The domestication of the plants was carried out since 374 prehistory and with very long processes, where the first domesticated forms were 375 cultivated together with their wild relatives facilitating a genetic flow to maintain the 376 genetic diversity (Prohens et al., 2017). 377 378 An ambitious objective is the perenialization of quinoa that can allow consecutive 379 harvests with the least degree of soil disturbance. In Bolivia, wild quinoa with a multi- 380 year growing cycle is being multiplied. The suggested method to incorporate this 381 character to quinoa is backcrossing under the introgressiomics approach (Prohens et al., 382 2017). 383 384 Another option to address the improvement for the context of climate change is the 385 cultivation of wild relatives and implements selection plans in the ajara as well as the 386 crossing with these genotypes, then perform selection for precocity and resistance to 387 drought. 388 389 The sources for hail tolerance are found in the local varieties of the Central and Northern 390 Highlands. Obtaining a variety with tolerance to hail (Blanquita), is encouraging to 391 continue in the search for tolerance to hail. Therefore, improvement for hail tolerance 392 should begin with the evaluation of the genetic material of the germplasm bank. 393 394 For the tolerance of quinoa to abrasion by sand carried by the wind, there are no promising 395 materials identified, but it is assumed that the genetic sources may be found in the 396 ecotypes of the Southern highlands. Local varieties are those that have evolved during 397 decades under particular environmental conditions, so they are well adapted to the context 398 and are capable of absorbing the usual environmental variations of the area (Ruiz de 399 Galarreta et al. (2016). 400 401 4.2. Qañawa 402 403 The characters of interest for selection in qañawa are the precocity and less dehiscence of 404 the grain. This last character is a priority, since the dehiscence of the grain is magnified 405 with the occurrence of hail and wind, and this constitutes the main cause of loss of yield.

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406 The high precocity is found in the wild relative of qañawa. Preliminary evaluations 407 reported maturation between 75 to 100 days. The difficulty of conducting artificial 408 hybridization prevents the combination of characters for precocity from the wild species. 409 Given this, the induced mutation is the appropriate method to generate variation, then 410 implement selection in segregating progenies. The applicable methods are the selection 411 by single seed descent and the massive conduction of segregants. 412 413 The selection of mutant qañawa lines with the lowest degree of shattering by hail was 414 reported by Paucara (2016) and Bonifacio (2017). The reduced grain dehiscence is these 415 lines, is attributed to the deformation of inter glomerular leaves that embrace the group 416 of flowers, which makes lower the fall of mature grain. The deformation of the leaf blade 417 and the petiole is a mutant character. 418 419 Another option is the selection in ethno-varieties or landraces and I accessions of the 420 germplasm bank. The selection methods available are mass selection, stratified mass 421 selection, individual selection and combined individual-mass selection. 422 423 References 424 Apaza V. 2010. Manejo y mejoramiento de kañiwa. Instituto Nacional de Innovación 425 Agraria (INIA-Puno), Centro de Investigación de Recursos Naturales y Medio 426 Ambiente (CIRNMA), Bioversity International, International Fund for 427 Agricultural Development (IFAD). Puno, Perú. 75 p. 428 Apaza V., G. Cáceres, R. Estrada and R. Pinedo. 2013. Catálogo de variedades 429 comerciales de quinua en el Perú. Organización de las Naciones Unidas para la 430 Alimentación y la Agricultura (FAO), Instituto Nacional de Innovación Agraria 431 (INIA). Lima, Perú. 79 p. 432 Bal S.K., S. Saha, B.B. Fand, N.P. Singh, J. Rane and P.S. Minhas. 2014. Hailstorms: 433 Causes, Damage and Post-hail Management in Agriculture. National Institute of 434 abiotic Stress Management, Pune, Maharashtra, India. Technical Bulletin No.5. 435 44 p. 436 Bonifacio A., G. Aroni, and M. Villca. 2012. Catálogo etnobotánico de la quinua real. 437 Fundación PROINPA, Poligraf, Cochabamba, Bolivia. 122 p. 438 Bonifacio A., L. Gomez-Pando and W. Rojas. 2014. Mejoramiento genético de quinua y 439 el desarrollo de variedades modernas. In: Bazile et al. (Editores), Estado del arte

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473 Investigación del Cambio Global (IAI) Sao Jose dos Campos, y Comité Científico 474 sobre Problemas del Medio Ambiente (SCOPE), Paris, Francia. 426 p. 475 Jacobsen S.E., C Monteros, L.J. Corcuera, L.A. Bravo, J.L. Christiansen and A. Mujica. 476 2007. Frost resistance mechanisms in quinoa (Chenopodium quinoa Willd.). 477 European Journal of Agronomy. 26(4): 471- 475. 478 Jarvis D.E., O.R. Kopp, E.N. Jellen, M.A. Mallory, J. Pattee, A. Bonifacio, C.E. 479 Coleman, M.R. Stevens. D.J. Fairbanks and P.J. Maughan. 2008. Simple 480 sequence repeat marker development and genetic mapping in quinoa 481 (Chenopodium quinoa Willd.). Journal of Genetics 87:39–51. 482 Jarvis D.E., Yung Shwen H. […] & Tester M. 2017. The genome of Chenopodium 483 quinoa. Nature 542: 307–312. doi.org/10.1038/nature21370 484 Montero C.V. and C.A. Romero. 2017. Análisis Económico de la Producción Nacional 485 de la Quinua. Ministerio de Agricultura y Riego, Lima, Perú. 11 p. 486 Mamani F. 2017. Cultivo de cañahua (Chenopodium pallidicaule Aellen) para la 487 seguridad alimentaria. Proyecto Conservación de la biodiversidad genética de 488 quinua y cañahua en el altiplano norte y centro del departamento de La Paz. 489 DIPGIS-UMSA. La Paz – Bolivia. 34 p. 490 Mason S.L., R.R. Stevens, E.n. Jellen, A. Bonifacio, D.J. Fairbanks, C.E. Coleman, 491 R.R. McCarty, A.G. Rasmussen and P.J. Maughan. 2005. Development and use 492 of microsatellite markers for germplasm characterization in quinoa 493 (Chenopodium quinoa Willd.). Crop Science. 45:1618–1630. 494 Paucara L. 2016. Comportamiento agronómico de quince líneas de cañahua 495 (Chenopodium pallidicaule Aellen), en la Estación Experimental de Quipaquipani 496 del departamento de La Paz, Tesis Ing. Agr. Facultad de Agronomía, Universidad 497 Mayor de San Andrés, La Paz, Bolivia. 108 p. 498 Pinto M., Rojas W. y Soto J.L. 2008. Variedad de cañahua Illimani. Fundación 499 PROINPA-SINARGEA-MDRAyMA, IFAD-BIOVERSITY, La Paz, Bolivia. 4 500 p. 501 Prohens J.; Gramazio P.; Plazas M.; Dempewolf B.; Kilian B.; Díez M.J.; Fita A.; Herraiz 502 F.J.; Rodríguez-Burruezo A.; Soler S.; Knapp S.y Vilanova S. 2018. 503 Introgressiomics: a new approach for using crop wild relatives in breeding for 504 adaptation to climate change, Euphytica 213:

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505 Risi, J., W. Rojas and M. Pacheco. 2015. Producción y mercado de la quinua en Bolivia. 506 Instituto Interamericano de Cooperación para la Agricultura (IICA), Gráfica Real, 507 La Paz, Bolivia. 315 p. 508 Rojas W, J.L. Soto, M. Pinto, M. Jäger and S. Padulosi (eds). 2010. Granos Andinos. 509 Avances, logros y experiencias desarrolladas en quinua, cañahua y amaranto en 510 Bolivia. Bioversity International, Roma, Italia. 178 p. 511 Ruiz de Galarreta J. I., J, Prohens and R. Tierno. 2016. Las variedades locales en la mejora 512 genética de plantas. Sociedad Española de Ciencias Hortícolas Sociedad Española 513 de Genética, Gobierno Vasco, España. 480 p. 514 Tapia, M. E. and A.M. Fríes. 2007. Guía de campo de los cultivos andinos. FAO y ANPE. 515 Lima, Perú. 209 p. 516 Sanchez J.L., R. Fraile, J.L. De la Madrid, M.T. De la Fuente, P. Rodriguez P and A. 517 Castro. 1996. Crop damage: The hail size factor. American Meteorological 518 Society: 1535-1541 519 Useros J.L. 2013. El cambio climático: sus causas y efectos medioambientales. Anales de 520 la Real Academia de Medicina y Cirugía de Valladolid 50:71-98. 521 Vuille M. 2013. El Cambio Climático y los Recursos Hídricos en los Andes Tropicales 522 Unidad de Salvaguardia Ambientales, Banco Interamericano de Desarrollo. Nota 523 Técnica IDB-TN-517 524 Yasui Y., Hirakawa H, Oikawa […] and Y. Fujita. 2016. Draft genome sequence of an 525 inbred line of Chenopodium quinoa, an allotetraploid crop with great 526 environmental adaptability and outstanding nutritional properties. DNA Research, 527 23(6): 535–546, https://doi.org/10.1093/dnares/dsw037 528 Woods A. y P. Eizaguirre. 2004. La cañahua merece regresar. LEISA Revista de 529 Agroecología 20(1):32-34. 530 Zurita-Silva A., Jacobsen S-E., Razzaghi F., Alvarez-Flores R., Ruiz K.B., Morales A. y 531 Silva H. 20114. Respuestas a la sequía y adaptación de la Quinua. In: Bazile et al. 532 (Editores), Estado del arte de la quinua en el mundo en 2013: FAO (Santiago 533 de Chile) y CIRAD (Montpellier, Francia): 187-202. 534 535 536 537 538

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539 Table 1. Quinoa varieties selected for the Peruvian altiplano. 540 Variety Saponin Grain Grain Days to Adaptation color size maturity INIA 431 Sweet Cream Large --- Altiplano, Costal Altiplano INIA 420 - Negra Sweet Gray Small 136 a 140 Altiplano, Valley, Collana Cost INIA 415 – Sweet Gray Medium 140 Altiplano Valley Pasankalla Costal Illpa INIA Sweet Cream Large 150 Altiplano Salcedo INIA Sweet Cream Large 160 Altiplano, Valley Costal Blanca de Juli Sweet Cream Small 160 a 170 Altiplano Cheweca Semi sweet Cream Medium 180 a 190 Altiplano Kankolla Semi sweet Cream Average 160-180 Altiplano Rosada Taraco Biter Cream Small --- Altiplano Tahauaco Semi sweet White --- 170 a 190 Altiplano 541 Source: Prepared based on Apaza et al., 2013. Gomez-Pando and Aguilar, 2016. 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571 572 573

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574 Table 2. Quinoa improved varieties released by the former IBTA in Bolivia (1967 - 575 1996). 576 Variety Saponin Grain Seed size Days to Adaptation color maturity Sajama Sweet White Medium 150 Central altiplano Samaranti Sweet White Medium 160 Central altiplano Huaranga Sweet White Medium 160 Central altiplano Chucapaca Sweet White Medium 160 Central altiplano Kamiri Sweet White Medium 140 Central altiplano Sayaña Sweet Yellow Medium 145 Central altiplano Ratuqui Sweet White Medium 140 Central altiplano Robura Sweet White Medium 170 Central altiplano Jiskitu Sweet White Medium 140 Central altiplano Amilda Sweet White Medium 160 Central altiplano Santa María Sweet White Large 170 Central altiplano Intinayra Sweet White Large 160 Central altiplano Surumi Sweet White Medium 160 Central altiplano Jilata Sweet White Large 170 Central altiplano Jumataki Sweet White Large 160 Central altiplano Patacamaya Sweet White Large 145 Central altiplano 577 Source: Prepared based on Risi, Rojas y Pacheco (2010). 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606

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607 Table 3. Varieties obtained by the PROINPA Foundation (1999 -2010). 608 Variety Saponin Seed Grain Days to Adaptation size color maturity Jach’a Grano Bitter White Large 145 Altiplano Central y norte. Kurmi Sweet White Large 160 Altiplano Central y norte Aynuqa White Large 145 Altiplano Central Horizontes Bitter White Large 145 Altiplano Sur y Central Qosuña Sweet White Large 150 Altiplano Sur y Central Blanquita Sweet White Medium 160 to Altiplano Norte, Valles 170 609 Prepared based on: Bonifacio and Vargas (2005), and y Risi, Rojas y Pacheco (2015). 610 611 612 613 614 615 616 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648

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649 Table 4. Principal native varieties of Quinoa Real (Bolivia). 650 Variety Saponi Seed Seed size Days to Adaptation n color maturity Real Blanca Bitter Large White 170 Southern and Central altiplano Pandela Bitter Large 175 Southern and Central altiplano Toledo Bitter Large Orange 173 Southern altiplano Otusaya Bitter Large White 165 Southern altiplano Qanchis Blanco Bitter Large White 145 Southern altiplano Maniqueña Bitter Large White 143 Southern and Central altiplano Pisanqalla Bitter Large Brown/red 170 Southern altiplano Ch’aku Bitter Large White 172 Southern altiplano Q’illu Bitter Large Amarillo 172 Southern altiplano Rosa Blanca Bitter Large White 178 Southern altiplano Achachino Bitter Large White 176 Southern altiplano Ch’ullpi Bitter Large Cream/ 156 Southern altiplano 651 Source: Prepared based on Bonifacio et al., 2012. 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685

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686 Table 5. Characteristics of qañawa varieties in Bolivia. 687 Variedad Tipo Days to Plant colo Grain Commercial Potencial maturity color yield yiel kg/hectare kg/hectare Illimani Last’a 160 Pink/Orange White/gray 800 kg/ha 2000 Kullaca Last’a 140 Purple White/gray 700 kg/ha 1200 Condornayra Last’a Red Red 1350 Warikunka Saiwa Beige Brown 2250 Ak’apuya Last’a Purple Orange 1600 Pukaya Saiwa Orange Brown 1950 Kullpara Last’a Pink Grey 1200 UMSA 2006 Last’a Yellow Grey 1650 AGRO 2006 Last’a Yellow Grey 1250 688 Source: Prepared based on Pinto et al., 2008 and Pinto et al., S.f., Giménez et al., 2017. 689

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