QuinoaImprovement and Sustainable

Production

QuinoaImprovement and Sustainable

Production

Edited by

Kevin Murphy and Janet Matanguihan

Copyright © 2015 by Wiley-Blackwell. All rights reserved

Published by John Wiley & Sons, Inc., Hoboken, NewJerseyPublished simultaneously in Canada

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Library of Congress Cataloging-in-Publication Data:

Quinoa : improvement and sustainable production /edited by Kevin Murphy and Glafera Janet Matanguihan.

pages cmIncludes bibliographical references and index.ISBN 978-1-118-62805-8 (cloth)1. Quinoa. 2. Crop improvement. 3. Sustainable

agriculture. I. Murphy, Kevin (Kevin Matthew), 1972-editor. II. Matanguihan, Glafera Janet, editor.

SB177.Q55Q56 2015664′.7–dc23

2015006917

Printed in the United States of America

10 9 8 7 6 5 4 3 2 1

Contents

List of Contributors ix

Preface xi

1 Quinoa: An Incan Crop to FaceGlobal Changes in Agriculture 1Juan Antonio González, Sayed S. S.Eisa, Sayed A. E. S. Hussin, andFernando Eduardo Prado

Introduction 1A Brief History of Quinoa Cultivation 2Nutritional Value of Quinoa Seed 2Botanical and Genetic Characteristics of

the Quinoa Plant 5Quinoa and Environmental Stresses:

Drought and Salinity 7Conclusion 12References 12

2 History of Quinoa: Its Origin,Domestication, Diversification,and Cultivation with ParticularReference to the ChileanContext 19Enrique A. Martınez, Francisco F.Fuentes, and Didier Bazile

Quinoa Origins in the Central Andes 19Ancient Expansion to Southern Latitudes

in Chile 20Reintroduction of Quinoa in Arid Chile

after Local Extinction 20

Final Remarks 23References 23

3 Agroecological and AgronomicCultural Practices of Quinoa inSouth America 25Magali Garcia, Bruno Condori, andCarmen Del Castillo

Introduction 25Andean Domestication 26Botanical and Taxonomical Description 27Genetic Background and Research on

Quinoa Genetics 28Ecology and Phytogeography 30Cultivation and Agronomic Practices

in South America 30Quinoa Production 31

Soil conditions 31Climate 32

Drought resistance 32Temperature and photoperiod 33Hail 34

Cultivation 34Sowing 34Fertilization of quinoa 36Cultural practices 37Crop water requirements and

irrigation 37Biotic threats: pests and diseases 38Seed harvest and postharvest

technology 39References 41

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vi Contents

4 Trends in Quinoa Yield over theSouthern Bolivian Altiplano:Lessons from Climate andLand-Use Projections 47Serge Rambal, Jean-Pierre Ratte,Florent Mouillot, and Thierry Winkel

Summary 47Introduction 48Materials and Methods 49

The study area 49Recent past and present climate 49Source of climate scenarios 50Simulating the yield index at local

or plot scale 50The soil water balance model 50Scenarios of land-use/land-cover

changes 51Scaling local yield index up to the region 51

Results 52Drought history over the area 52Climate projections and soil drought

limitation 52Time variation of yield at local or

plot scale 54Model results at landscape level 56

Discussion 57Acknowledgments 60References 60

5 The Potential of Using NaturalEnemies and ChemicalCompounds in Quinoa forBiological Control of InsectPests 63Mariana Valoy, Carmen Reguilón,and Griselda Podazza

Introduction 63Insects in Quinoa 64

Insect pests of quinoa 65Beneficial insects in quinoa 65Chemical responses of quinoa

to insect herbivory 72Quinoa secondary metabolites 74

Potential of Biological Control in Quinoa 76

Potential for Ecological Management ofQuinoa 77

References 80

6 Quinoa Breeding 87Luz Gomez-Pando

History – Domestication Process 87Collection of Genetic Resources 88Goals and Methods of Quinoa Breeding 92

Requirement of the farmers 92Requirements of the industry and

consumers 95Methods in genetic improvement 96

Quinoa Breeding Methods 98Selection 98Participatory plant breeding (PPB) 98Introduction of foreign germplasm 99Hybridization 99Interspecific and intergeneric crosses 102Backcross method 102Using heterosis in quinoa 102Mutagenesis 103Marker-assisted selection (MAS) 103

Conclusion 103References 103

7 Quinoa Cytogenetics, MolecularGenetics, and Diversity 109Janet B. Matanguihan, Peter J.Maughan, Eric N. Jellen, and BozenaKolano

Introduction 109Cytogenetics and Genome Structure of

Chenopodium Quinoa 109Crossability of Quinoa and Allied

Tetraploid Taxa 111DNA Sequence Evidence for Quinoa’s

Genomic Origins 112Quinoa Genetic Markers and Linkage

Maps 113Quinoa Diversity 115

Phenotypic diversity 115Genetic diversity 117

Summary 118References 120

Contents vii

8 Ex Situ Conservation of Quinoa:The Bolivian Experience 125Wilfredo Rojas and Milton Pinto

Introduction 125Centers of Origin and Diversity

of Quinoa 126Geographical Distribution of Quinoa 127Genebanks of the Andean Region 128Bolivian Collection of Quinoa

Germplasm 130History and management of the

quinoa germplasm 130Current status of quinoa germplasm 132

Steps for Ex Situ Management andConservation of Quinoa 132Collection of quinoa germplasm 133Technical procedure for quinoa

germplasm collection 133History and evolution of quinoa

germplasm collections 134Distribution of quinoa germplasm

collection 136Preliminary multiplication of quinoa

germplasm 136Storage and conservation of quinoa

germplasm 138Short- and medium-term storage

(1 to 20 years) 138Long-term storage (80 to 100 years) 138Characterization and evaluation

of the quinoa germplasm 140Stages of germplasm characterization

and evaluation 140Agromorphological variables 141Agro-food and nutritional value

variables 143Molecular characterization 144Multiplication and regeneration

of quinoa germplasm 144Monitoring of seed quantity and

percentage of seedgermination 145

Technical procedure for multiplicationand/or regeneration 145

Regeneration schedule 146Documentation and information

on quinoa germplasm 147

Utilization of quinoa germplasm 148Conclusions 155References 158

9 Quinoa Breeding in Africa:History, Goals, and Progress 161Moses F.A. Maliro and Veronica Guwela

Introduction 161Origin of quinoa 161Introducing quinoa in Africa 161Ecological adaptation of quinoa 163

Goals of Quinoa Breeding in Africa 164Quinoa studies under Malawi

conditions 164Quinoa studies in Kenya 166

Challenges and Considerations forFuture Research 169Plant lodging 169Acceptability 169Agronomic practices 170Rain-fed versus irrigated cropping

systems 170Conclusion 170References 170

10 Quinoa Cultivation forTemperate North America:Considerations and Areasfor Investigation 173Adam J. Peterson and Kevin M. Murphy

Introduction 173Tolerance to Abiotic Stresses 173

Heat tolerance 173Drought tolerance 174Cold tolerance 175Salinity tolerance 176

Production Aspects 177Variety selection 177Fertilization 178Planting/spacing 179Maturity and harvesting 181

Challenges to Quinoa Production 182Waterlogging and preharvest sprouting 182Disease 183Insect pests 184

viii Contents

Weed control 185Saponins 186

Alternative Uses of Quinoa 186Forage 186Feed 187

Conclusion 187Acknowledgments 188References 188

11 Nutritional Properties of Quinoa 193Geyang Wu

Introduction 193Protein 193Carbohydrates 196

Starch 196Sugar 198Dietary fiber 198

Lipids 199Vitamins 200Minerals 201Anti-Nutritional Factors of Quinoa 202Bioactive Compounds 204

Phenolic compounds 204Phenolic acid 204Flavonoids 204Carotenoids 205

Summary 205References 205

12 Quinoa’s Calling 211Sergio Núnez de Arco

Introduction 211A Snapshot of the Economics of a

Smallholder Farmer in Bolivia andthe International Market 212

The Quinoa Market: Supply andDemand 213

Bolivia, Peru, and Ecuadorincrease quinoa acreage 213

Evolution of quinoa,(Figs. 12.7–12.10and Fig. 12.3) acreage inBolivia 213

The US quinoa market and evolutionof prices 215

Quinoa in the eye of a market storm 215The quinoa grower rises out

of poverty 217Current Production Practices, Increased

Acreage, and Thoughts onSustainability 221

Living Well, Reversed Migration, andCultural Identity 224

Opportunities for the Bolivian Farmer 225

Index 227

List of Contributors

Sergio Núñez de ArcoAndean Naturals, Inc.,Foster City, CA, USA

Didier BazileUPR47, GREEN, Centre de CoopérationInternationale en Recherche Agronomiquepour le DéveloppementCampus International de BaillarguetMontpellier, France

Carmen Del CastilloFaculty of AgronomyUniversidad Mayor de San AndresLa Paz, Bolivia

Bruno CondoriConsultative Group on InternationalAgricultural Research – International PotatoCenter, La Paz, Bolivia

Sayed S.S. EisaAgricultural Botany Department, Faculty ofAgriculture, Ain Shams University, Cairo, Egypt

Francisco F. FuentesFacultad de Agronomía e Ingeniería Forestal,Pontificia Universidad Católica de Chile, Casilla306–22, Santiago, Chile

Magali GarciaFaculty of Agronomy,Universidad Mayor de San AndresLa Paz, Bolivia

Juan Antonio GonzálezInstituto de Ecologia – Area de BotánicaFundación Miguel Lillo TucumánTucumán, Argentina

Veronica GuwelaInternational Crops Research Institute for theSemi-Arid Tropics, Lilongwe, Malawi

Sayed Abd Elmonim Sayed HussinAgricultural Botany Department, Faculty ofAgriculture, Ain Shams UniversityCairo, Egypt

Eric N. JellenPlant and Wildlife SciencesBrigham Young UniversityProvo, UT, USA

Bozena KolanoDepartment of Plant Anatomy and CytologyUniversity of Silesia, Poland

Moses F.A. MaliroDepartment of Crop and Soil Sciences, BundaCollege Campus, Lilongwe University ofAgriculture and Natural ResourcesLilongwe, Malawi

Enrique A. MartínezCentro de Estudios Avanzados en Zonas ÁridasLa Serena and Facultad de Ciencias del MarUniversidad Católica del NorteCoquimbo, Chile

ix

x List of Contributors

Janet B. MatanguihanDepartment of Crop and Soil SciencesWashington State UniversityPullman, WA, USA

Peter J. MaughanPlant and Wildlife SciencesBrigham Young UniversityProvo, UT, USA

Florent MouillotIRD, UMR 5175 CEFEMontpellier, France

Kevin M. MurphyDepartment of Crop and Soil SciencesWashington State UniversityPullman, WA, USA

Luz Gomez-PandoUniversidad Nacional Agraria La MolinaAgronomy FacultyLima, Peru

Adam J. PetersonDepartment of Crop and Soil SciencesWashington State UniversityPullman, WA, USA

Milton PintoPROINPA Foundation538 Americo Vespucio St., P.O. Box 1078,La Paz, Bolivia

Griselda PodazzaInstituto de Ecología, Fundación Miguel LilloTucumán, Argentina

Fernando Eduardo PradoFacultad de Ciencias Naturales e IMLFisiología VegetalTucumán, Argentina

Serge RambalCNRS, UMR 5175 CEFEMontpellier, FranceDepartamento de BiologiaUniversidade Federal de LavrasLavras, MG, Brazil

Jean-Pierre RatteCNRS, UMR 5175 CEFEMontpellier, France

Carmen ReguilónInstituto de Entomología, Fundación MiguelLillo Tucumán, Argentina

Wilfredo RojasPROINPA FoundationAv. Elias Meneces km 4El Paso, Cochabamba, Bolivia

Mariana ValoyInstituto de Ecología, Fundación Miguel LilloTucumán, Argentina

Thierry WinkelIRD, UMR 5175 CEFEMontpellier, France

Geyang WuSchool of Food ScienceWashington State UniversityPullman, WA, USA

Preface

The seeds of this book took root in the summerof 2010, during the first year of our multilocationquinoa trials across three major climatic regionsof Washington State. We began growing andevaluating quinoa thanks to generous fundingfrom the Organic Farming Research Foundation,and growers around the state looked on with keeninterest. In that first year we tested 44 varieties ofquinoa sourced from almost as many diverse geo-graphical locations and we were mildly surprisedwhen only 12 of these actually produced seed inour northern latitude. That first year we wereintroduced to many of the ongoing challenges wecontinue to face 5 years later, including suscepti-bility to preharvest sprouting and downy mildew,photoperiod insensitivity, pollen sterilizationresulting from high summer temperatures withlittle to no rainfall or supplemental irrigation,and the negative effects of aphid and lyguspredation. We quickly realized that if quinoa wereto become a successfully grown crop in the PacificNorthwest region of the United States, it wouldrequire a concerted effort of a transdisciplinarycadre of scientists with a range of expertise,a forward-thinking and risk-taking group ofinnovative farmers, and a strong supporting castof distributors, processors, and consumers. Fromthat first year, with only one junior faculty and oneundergraduate research intern collaborating withthree farmers, the quinoa group at WashingtonState University has grown into diverse team ofover 10 faculty and 10 graduate students, eachaddressing a key component of quinoa breeding,agronomy, sociology, entomology, or food science.This book is intended to lay the groundwork forthe latest quinoa research worldwide and to assistfaculty and students new to the crop to gain a

foothold of understanding into quinoa genomicsand breeding, global agronomy and production,and marketing.

In August 2013, Washington State Univer-sity hosted the International Quinoa ResearchSymposium (IQRS). One hundred and sixtyenthusiastic participants from 24 countriesdescended on Pullman, Washington and sharedknowledge, questions, obstacles, observations,and ideas on the path forward during an intense,vibrant and thought-provoking 3 days of talks,field visits, poster sessions, and quinoa vodkainfused social exploration. Many of the co-authorsof the various chapters in this book were atten-dees and/or presenters at the IQRS, and thesymposium provided a safe forum for the opendiscussion of ideas that have found their way intothe chapters of this book. Symposium attendeeswho have contributed to this book include DidierBazille, Juan Antonio Gonzalez, Luz GomezPando, Rick Jellen, Moses Maliro, EnriqueMartinez (in absentia), Jeff Maughan, SergioNúñez de Arco, Adam Peterson, Wilfredo Rojas,Geyang Wu, and co-editors Janet Matanguihanand Kevin Murphy.

Keynote speakers at the IQRS includedSven-Erik Jacobsen, renowned quinoa researcherfrom University of Copenhagen, Tania San-tivanez from the United Nations Food andAgriculture Organization, and John McCamant,a long-time quinoa farmer and researcher fromWhite Mountain Farms in Colorado, USA. Otheresteemed presenters not mentioned includedDaniel Bertero from the University of BuenosAires, Argentina, Morgan Gardner of WashingtonState University, Frank Morton of Wild GardenSeeds in Oregon, and Hassan Munir of the

xi

xii Preface

University of Agriculture Faisalabad, Pakistan,as well as numerous poster presentations. Finally,the highlight of the symposium for many atten-dees was the eloquent thoughts delivered by agroup of five Bolivian farmers, who traveled tothe United States for the first time to join in theinternational discussion on the many social andpolitical aspects of quinoa cultivation.

This book reflects the many presentations anddiscussions that took place at the IQRS, and isintended to provide the reader with a compre-hensive base knowledge of the current body ofknowledge of the ever-expanding, global scientificresearch of quinoa. In Chapter 1, Gonzalez et al.provide a solid overview of quinoa as an Incancrop, primarily in Peru and Bolivia, now facing adiversity of global challenges. Chapter 2 followsup on this introduction by discussing the origin,domestication, diversification, and cultivation ofquinoa from a Chilean perspective.

Chapter 3 by Garcia et al. encapsulates many ofthe wide-ranging agronomic and agroecologicalcultural practices of quinoa throughout the majorgrowing regions of South America as a whole.This broad chapter provides a botanical andtaxonomical description of quinoa, ecology andphytogeography of quinoa, and many tangibleproduction practices across a wide range ofclimates, soils, and growing conditions that canbe emulated in nontraditional growing regionsaround the world. Rambal et al. follow this witha description of the historical trends in quinoayield in the southern Bolivian altiplano, includingimportant lessons from climate and land-use pro-jections in Chapter 4. Valoy et al. then discuss inChapter 5 the potential of using natural enemiesand chemical compounds in quinoa for biologicalcontrol of pests. This chapter follows up on theagroecological themes discussed in Chapter 3, andcompiles and elucidates a vast array of knowledgegained through previous research in this realmof quinoa science, and provides the thoughtfulreader many potential ideas for new research inthis direction.

In Chapter 6, Peruvian plant breederGomez-Pando describes the historical andmodern context of quinoa breeding in the Andeanregions. Beginning with the effect of farmer

selection on seed color, dormancy, seed sizeand seed coat thickness, salt and drought toler-ance, and adaptation to multiple and countlessmicroclimates, Gomez-Pando then moves on tohighlight the rise of modern quinoa breedingin the 1960s, the collection of quinoa geneticresources and in situ conservation, and the goalsand methodology employed by current quinoabreeders.

Matanguihan et al. follow this with an in-depthdiscussion on the cytogenetics, genomic structure,and diversity of quinoa in Chapter 7. Informa-tion on close genetic relatives of Chenopodiumquinoa are discussed, along with DNA-basedmolecular genetic tools and linkage maps whichcan facilitate and accelerate the transfer of exoticgenes into C. quinoa. Also included in Chapter 7is a review of phenotypic and genetic diversitystudies which show that the genetic variability ofquinoa has a spatial structure and distribution.The congruence between genetic differentiationand ecogeography suggests that quinoa all overthe southern Andes may be undergoing similarprocesses of genetic differentiation. Not surpris-ingly, human activities, specifically seed exchangeroutes, have significantly affected the geneticstructure of quinoa.

In Chapter 8, Rojas and Pinto discuss theex-situ conservation of quinoa genetic resourcesfrom a Bolivian perspective. According to Rojasand Pinto, the Bolivian quinoa germplasm col-lection has the greatest diversity in the world,and this diversity represents the cultural impor-tance of quinoa in Bolivian customs, indigenousconsumption, and production. Chapter 8 alsoprovides insight into the center of origin anddiversity of quinoa, the geographical distributionof quinoa, and steps needed for the ex situmanagement and conservation of quinoa.

Chapters 9 and 10 discuss quinoa cultivation ntwo continents, Africa and North America, thatare considered nontraditional quinoa productionenvironments. In Chapter 9, Maliro and Guweladescribe the necessity of stabilizing food securityand alleviating malnutrition in Africa, and thepotential for quinoa as a novel crop to make apositive contribution to these efforts. The goals ofquinoa breeding in Africa and information from

Preface xiii

recent quinoa trials in Malawi and Kenya arediscussed in an effort to address the challengesand considerations for future quinoa researchin Africa. Key among these considerations isthe acceptability of quinoa into African diets.In Chapter 10, Peterson and Murphy discussquinoa introduction to the United States as a cropapproximately 30 years ago, and the key breeding,research, and production events in the timeperiod after its introduction. Recent research atWashington State University is highlighted inthis chapter.

In Chapter 11, Wu describes the nutritionalproperties of quinoa that have played an impor-tant role in bringing the crop to worldwideattention. Finally, in a refreshing departure fromthe scientific writing in the previous chapters,Nuñez de Arco provides an insider’s view into themarketing of quinoa in Chapter 12. Of particularinterest are the personal descriptions and snap-shots of the lives of smallholder farmers, of whichan estimated 35,000 produce quinoa in Bolivia,who discuss their philosophy of marketing quinoa

under the current fluctuations in the supply anddemand of this increasingly popular crop.

This book is a reflection of the increasingimportance of quinoa in the global market. Theroster of contributors – from South America,Europe, Africa and North America – also reflectsthe expansion of quinoa from its origins to newproduction areas in the world. It was a pleasureto work with colleagues from countries who havegrown quinoa for centuries, and with colleaguesfrom countries which are growing quinoa for thefirst time. We are indebted to these authors fortheir willingness to share their expertise and fortheir cooperation in the process of shaping thisbook. It is our hope that this book will contributeto quinoa knowledge to benefit growers, students,researchers, and professionals from universitiesand institutes involved in the improvement ofquinoa and its sustainable production.

Kevin M. MurphyJanet B. Matanguihan

Chapter 1

Quinoa: An Incan Crop to Face GlobalChanges in Agriculture

Juan Antonio González1, Sayed S. S. Eisa2, Sayed A. E. S. Hussin2,

and Fernando Eduardo Prado3

1Instituto de Ecologia – Area de Botánica, Fundación Miguel Lillo, Tucumán, Argentina2Agricultural Botany Department, Faculty of Agriculture, Ain Shams University (ASU), Cairo, Egypt3Facultad de Ciencias Naturales e IML, Fisiología Vegetal, Miguel Lillo 205, 4000 Tucumán, Argentina

INTRODUCTION

Environmental changes have always occurred inthe past but in the last decades these have escalatedto critical levels, presenting environmental riskto people, especially in terms of food supply, as itaffects crop yield, production, and quality. Rapidpopulation growth leads to increase in demandfor land and thus to accelerated degradation anddestruction of the environment (Alexandratos2005; IPCC 2007). Probably the most importantchange driven by human activity is the increasingaccumulation of greenhouse gases such as carbondioxide (CO2), among others (Wallington et al.2004; Montzka et al. 2011). Greenhouse gasescan absorb and emit infrared radiation, and thus aglobal earth warming occurs, otherwise known asthe greenhouse effect. Many scientists agree thateven a small increase in the global temperaturewould lead to significant climate and weatherchanges, affecting cloud cover, precipitation, windpatterns, the frequency and severity of storms,and the duration of seasons (Solomon et al. 2009).This scenario will lead to scarce natural resourcesand the reduction of food production.

Quinoa: Improvement and Sustainable Production, First Edition. Edited by Kevin Murphy and Janet Matanguihan.© 2015 John Wiley & Sons, Inc. Published 2015 by John Wiley & Sons, Inc.

The net consequences of global warming oncrop physiology and yield are not yet fully under-stood, but there are some evidences indicatingthat decrease in yield may be the main response(Parry et al. 2005). Another deleterious effectof global warming is the increase in diseases,especially those caused by fungi and bacteria, asa consequence of higher humidity (Chakrabortyet al. 2000; Hunter 2001). As most crops world-wide are well adapted to previous weatherconditions, many of these crops will becomeless productive and may even disappear in afuture of increasing climate change. It is thereforenecessary to explore plant species as alternativecrops or develop new crops to grow underthese changing weather patterns. In this sense,it is very important to take into account plantspecies that grow in different altitudinal levelsor those that have thrived in mountain regionsfor millennia. Mountain plants, especially thoseadapted and cultivated in different altitudinallevels, may be very important because of thegenetic richness that enabled those adaptations.

Quinoa (Chenopodium quinoa Willd.), a nativegrain to the Andean highlands in South America,could be an excellent alternative crop in manyregions of the world. Quinoa has been grown

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2 Quinoa: Improvement and Sustainable Production

in the Andes about 5,000–7,000 years ago andhas been cultivated in different ecological zonesfrom sea level in the northwest region of Chile toaltitudes over 4,000 m above sea level (masl) in theBolivian Altiplano (Fuentes et al. 2009). Owingto this plasticity, quinoa has been introduced tohigher latitudes as a new or alternative crop, withreports indicating an acceptable adaptation ofthis species in the United States, Canada, andEurope (Johnson and Ward 1993; Jacobsen 1997)and recently in Morocco (Jellen et al. 2005), India(Bhargava et al. 2006, 2007), and Italy (Pulventoet al. 2010).

A BRIEF HISTORY OF QUINOACULTIVATION

Archeological studies provide evidence on theconsumption of quinoa as human food thousandsof years before the first Spanish conquerorsarrived in America. Uhle (1919), taking intoaccount evidences from Ayacucho (Perú), saidthat quinoa domestication began almost 5,000years BC. According to Nuñez (1974), quinoa wasutilized in the north region of Chile at least 3,000years BC. Many chronicles and archeologicalstudies provide evidence that quinoa was usedby indigenous people for centuries in Colombia,Ecuador, Perú, Bolivia, Chile, and the Argen-tinean northwest. During pre-Columbian times,quinoa seed served as a staple food in the Incandiet, leading the Incas to call it the “mothergrain” and considered it as a gift of the sun god,“Inti.” It is believed that the Incas consideredquinoa to be a sacred plant. Religious festivalsincluding an offering of quinoa in a fountain ofgold to the Inti god were held. The Inca Emperorused a special gold tool to make the first furrowof each year’s quinoa planting. In Cuzco, ancientIncas worshipped entombed quinoa seeds asthe progenitors of the city. The first Spanishconqueror who mentioned quinoa was Pedrode Valdivia. In 1551, he wrote to Carlos I, theSpanish Emperor, about the presence of somecrops in the neighboring area of Concepción,Chile and specifically mentioned “…maize,potatoes and quinuas… ” (Tapia 2009). On the

other hand, in the Comentarios Reales de los Incas,a book written by Inca Garcilaso de la Vega andpublished in 1609 in Lisbon, Portugal, Garcilasomentioned “quinoa” as one of the first crops inthe Inca Empire (de la Vega 1966). Garcilasomentioned that there was an intent to exportquinoa to Spain but the seeds were nonviable.Other authors had also mentioned the existenceof quinoa in Pasto and Quito, Ecuador (Cieza deLeón 1560), in Collaguas, Bolivia (Ulloa Mogol-lón 1586), Chiloé island in Chile (Cortés Hogea1558), and in the Argentinean Northwest andCordoba province, Argentina (de Sotelo 1583).During the Spanish conquest of South Americain the sixteenth century, quinoa was scornedas a “food for Indians” and the conquerorsdestroyed fields of quinoa, actively suppressing its“non-Christian” production and consumption.The Incan peoples under the yoke of Spanishoppression were forbidden to grow it on painof death and were forced to grow corn instead.According to Tapia (2009), after the Spanishconquest, the quinoa crop was preserved byAndean peoples in “aynokas” (communal lands)for centuries. This cropping practice also allowedthe conservation of quinoa germplasm in situ(Tapia 2009). Today, quinoa is cultivated in morethan 50 countries beyond the Andes. As a result,the cloud of ambiguity that has enveloped thiscrop for more than four centuries is beginning todisappear (National Research Council 1989).

NUTRITIONAL VALUE OF QUINOA SEED

There is extensive literature on the chemicalcomposition of quinoa seed (González et al. 1989;Ando et al. 2002; Repo-Carrasco et al. 2003; Abu-goch 2009), which cover all nutritional aspectssuch as chemical characterization of proteins(Brinegar and Goundan 1993; Hevia et al. 2001),fatty acid composition of the seed oil (Wood et al.1993; Ando et al. 2002), mineral content (Koziol1992; Konishi et al. 2004; Prado et al. 2010), andnutritional value (Prakash et al. 1993; Ranhotraet al. 1993; Ruales and Nair 1992).

The lipid content of quinoa seed is higher thanthat in common cereals (Repo-Carrasco-Valencia

Quinoa: An Incan Crop to Face Global Changes in Agriculture 3

2011) and is mainly located in the embryo. Theoil of quinoa seed is rich in polyunsaturated fattyacids (linoleic and linolenic) and in oleic acid.Its level of unsaturated fatty acids in relation tohuman nutrition is better than those in othercereals (Alvarez-Jubete et al. 2009). According tothe Food and Agricultural Organization (FAO)recommendations on fats and fatty acids in humannutrition (FAO/WHO 2010), infant food shouldcontain 3–4.5% energy in the form of linoleicacid (LA) and 0.4–0.6% in the form of linolenicacid (ALA), which corresponds to LA/ALAratio (n-6/n-3 ratio) between 5 (minimum) and11.2 (maximum). The LA/ALA ratio of quinoaoil is 6.2 (Alvarez-Jubete et al. 2009) and thusfalls within the FAO/WHO (2010) recommendedvalues. Furthermore, a diet with a high n-6/n-3ratio promotes the pathogenesis of many degen-erative diseases such as cardiovascular disease,cancer, osteoporosis, as well as inflammatory andautoimmune diseases (Simopoulos 2001). Themain carbohydrate in quinoa seed is the starchwhere soluble sugars, that is, sucrose, glucose,and fructose are present at low levels (Gonzálezet al. 1989). Quinoa starch is located mainly inthe perisperm and it occurs both as small indi-vidual granules and larger compound granulescomposed of hundreds of individual granules(Prado et al. 1996). The individual granules arepolygonal with a diameter of 1.0–2.5 μm and thecompound granules are oval, with a diameter of6.4–32 μm (Atwell et al. 1983). Quinoa starch isrich in amylopectin and gelatinizes at relativelylow temperatures (57–71∘C). Moreover, it hasexcellent freeze-thaw stability attributed to itsrich amylopectin content (Ahamed et al. 1996).In comparison with common cereals, quinoa isan excellent source of γ-tocopherol (vitamin E),containing about 5 mg/100 g DM (Ruales andNair 1993). The content of γ-tocopherol is of par-ticular biological relevance because of its potentialanticarcinogenic and anti-inflammatory activities(Jiang et al. 2001). Quinoa also contains significantamounts of riboflavin, thiamine, and, especially,vitamin C that is uncommon in cereals (Koziol1992; Ruales and Nair 1993; Repo-Carrasco et al.2003). Recently, it has been demonstrated thatquinoa seed also contains high levels of folate

(Schoenlechner et al. 2010). The folate contentfound in quinoa is 132.7 mg/100 g DM, about10-fold higher than that in wheat seed. Quinoabran contains a higher amount of folate thanflour fraction (Repo-Carrasco-Valencia 2011).Furthermore, quinoa seed does not contain aller-genic compounds such as gluten or prolamine orenzyme (protease and amylase) inhibitors presentin most common cereals (Zuidmeer et al. 2008)or trypsin and chymotrypsin inhibitors present insoybean seeds (Galvez Ranilla et al. 2009).

Despite its healthy nutritional composi-tion, several cultivars of quinoa contain bittersaponins, glycosylated secondary metabolitesin the seed coat that act as antinutrients anddeterrents of seed predators such as birds andinsects (Solíz-Guerrero et al. 2002). Saponinsare concentrated in external layers of the seed(Prado et al. 1996) and include a complex mixtureof triterpene glycosides that are derivatives ofoleanolic acid, hederagenin, phytolaccagenicacid, serjanic acid, and 3β,23,30-trihydroxyolean-12-en-28-oic acid, which bear hydroxyl andcarboxylate groups at C-3 and C-28, respectively(Kuljanabhagavad et al. 2008). Presently, at least16 different saponins have been detected inquinoa seeds (Woldemichael and Wink 2001).Saponins are reported to be toxic for cold-bloodedanimals and have been used as fish poison bySouth American inhabitants (Zhu et al. 2002).They have some adverse physiological effects,as they are membranolytic against cells of thesmall intestine and possess hemolytic activity(Woldemichael and Wink 2001). Moreover,saponins form complexes with iron and mayreduce its absorption.

Although saponins have negative effects, theyalso have positive effects such as reducing serumcholesterol levels, possessing anti-inflammatory,antitumor, and antioxidant activities, andenhancing drug absorption through the mucosalmembrane. Saponins also exhibit insecticidal,antibiotic, antiviral, and fungicidal properties(Kuljanabhagavad and Wink 2009). Furthermore,saponins act as immunological and absorptionadjuvant to enhance antigen-specific antibodyand mucosal response (Estrada et al. 1998).

4 Quinoa: Improvement and Sustainable Production

Saponin content varies among genotypes,ranging between 0.2 and 0.4 g/kg DM (sweetgenotypes) and 4.7 and 11.3 g/kg DM (bit-ter genotypes). Therefore, selection of sweetgenotypes with very low saponin content inthe seeds is one of the main breeding goals inquinoa. However, selection for sweet genotypesis retarded by cross-pollination (Mastebroeket al. 2000). The tissue containing saponins is ofmaternal origin, and the saponin content of theseed reflects the genotype of the plant from whichthe grain is harvested (Ward 2001). Accordingto Gandarillas (1979), the saponin content traitis controlled by two alleles at a single locus,with the bitter allele (high saponin) dominantto the sweet allele (low saponin). More recently,researchers have observed that saponin content inquinoa seed is a continuously distributed variableand is therefore more likely to be polygenicallycontrolled and quantitatively inherited (Galweyet al. 1990; Jacobsen et al. 1996).

Quinoa seeds must be freed of seed coatsaponins before consumption. Saponins canbe easily eliminated by water washing or abra-sive dehulling. There was no difference in theremoval of saponins observed between the twomethods (Ridout et al. 1991), although the lattermethod has the advantage of not generatingwastewater. However, some nutrients can be lostwhen the abrasive dehulling method is used(Repo-Carrasco-Valencia 2011).

Among the nutritional attributes of quinoaseed, prominent is its high-quality protein thatis gluten-free and has an exceptional amino acidbalance. The presence of essential amino acidssuch as methionine, threonine, lysine, and trypto-phan are very important because they are limitingamino acids in most cereal grains (Gorinsteinet al. 2002). The high level of tryptophan foundin the seed of the Bolivian cultivar “Sajama” isnoteworthy (Comai et al. 2007). Protein quality isdetermined by its biological value (BV), which isan indicator of protein intake by relating nitrogenuptake to nitrogen excretion. The highest valuesof BV correspond to whole egg (93.7%) and cowmilk (84.5%) (Friedman 1996). The protein ofquinoa seed has a BV of 83%, which is higherthan that of fish (76%), beef (74.3%), soybean

(72.8%), wheat (64%), rice (64%), and corn(60%) protein (Abugoch 2009).

According to the FAO/WHO nutritionalrequirements for 10- to 12-year-old children,quinoa protein possesses adequate levels ofphenylalanine, tyrosine, histidine, isoleucine,threonine, and valine (FAO/WHO 1990). Con-sequently, there is no need to combine quinoaseed with other protein sources to supply humanrequirements for essential amino acids. Thisnutritional aspect of quinoa is very significant as itcan provide a new protein source for a good diet.Quinoa may also be an important alternative cropfor mountainous regions of the world, where manypeople live. In these regions, there are severe con-straints in obtaining good quality food and quinoawill be able to supply the nutrient requirementsthat other crops cannot, especially for children.

The nutritional composition of quinoa seed isdetermined by both the genotype and the envi-ronment. The metabolism of nitrogen-containingcompounds, that is, proteins and amino acids, maybe strongly affected by environmental conditions(Triboi et al. 2003). In a recent ecophysiologicalstudy carried out on 10 quinoa cultivars from theBolivian highland region (Patacamaya site, 3,600masl) and northwest Argentinean lowland region(Encalilla site, 2,000 masl), González et al. (2011)demonstrated that in six cultivars (Amilda, Kan-colla, Chucapaka, Ratuqui, Robura, and Sayaña)the protein content showed an increment in thelowland growing site when compared with seedsfrom the highland site. In contrast, four cultivars(CICA, Kamiri, Sajama, and Samaranti) showeda decreased content (Table 1.1). Similarly, it hasalso been demonstrated that both the content andthe composition of quinoa saponins are affectedby environmental conditions. Both droughtand salinity decreased the content and profile ofsaponins of quinoa cultivars (Solíz-Guerrero et al.2002; Dini et al. 2005; Gómez-Caravaca et al.2012). In effect, many metabolic and physiologicalaspects of crops are affected by agroecologicalconditions (Triboi et al. 2003). Soil type andclimatic conditions also play a crucial role in thesuccess of crops. These are important results andshould be taken into account when choosing acommercial cultivar.

Quinoa: An Incan Crop to Face Global Changes in Agriculture 5

Table 1.1 Protein content (g/100 g DW) of quinoa seeds cultivated in twoagroecological sites (Patacamaya, 3,600 masl and Encalilla, 2,000 masl).

Patacamaya Encalilla

Cultivar (g/100 g DW)Difference

(%)

Amilda 11.41 12.5 8.7Kancolla 14.44 15.17 4.8Chucapaka 11.67 14.34 18.6CICA 15.46 13.46 −14.9Kamiri 13.98 13.12 −6.6Ratuqui 10.38 15.53 33.2Robura 9.62 10.43 7.8Sajama 12 9.15 −31.1Samaranti 12.26 9.34 −31.3Sayaña 11.36 13.85 18.0

Quinoa may be considered as a potentialalternative crop in many regions of the worlddue to the nutritional quality of its seed and itsgood potential for adaptation (González et al.1989, 2012; Dini et al. 2005; Comai et al. 2007;Thanapornpoonpong et al. 2008). Probably allthese aspects were taken into account by theFAO when it included quinoa in the list of mostpromising crops for world food security andhuman nutrition in the twenty-first century (FAO2006). The National Aeronautics and SpaceAdministration (NASA) also included quinoawithin the Controlled Ecological Life SupportSystem (CELSS) to augment the inadequateprotein intake of astronauts in long-durationspace travel (Schlick and Bubnehiem 1993).

BOTANICAL AND GENETICCHARACTERISTICS OF THE QUINOAPLANT

Quinoa is an annual Amaranthaceae. This Andeangrain is an important crop of the Andean regionin South America from Colombia (2∘N) to centralChile (40∘S) (Risi and Galwey 1984; Jacobsen2003). Despite its wide latitudinal distribution,quinoa also has a broad altitudinal distribution.Quinoa may be cultivated at sea level, middlemountain (between 2,000 and 3,000 masl), andhigh mountain (above 3,000 masl). In relationto this altitudinal and latitudinal distribution

pattern, Tapia (2009) distinguished at least fiveecotypes of quinoa: (i) Valley quinoa, which arelate-ripening, with plant heights 150–200 cm ormore, and growing at 2,000 and 3,000 masl; (ii)Altiplano quinoa, which can withstand severefrost and low precipitation, growing aroundTiticaca Lake in Bolivia and Perú; (iii) Salarquinoa, which can tolerate salty soils with highpH values, growing on the plains of the BolivianAltiplano such as Uyuni and Coipasa; (iv) Sealevel quinoa, generally small plants (near 100 cm)with a few stems and bitter grains, found in thesouth of Chile; and (v) Subtropical quinoa, whichhave small white or yellow grains, growing in theinter-Andean valleys of Bolivia. Royal Quinoa(Quinoa Real) is probably the most recognizedquinoa cultivar in the international market. It isa bitter variety and is only produced in Bolivia,particularly in the districts of Oruro and Potosí,around the salt flats of Uyuni and Coipasa. Themicroclimatic conditions and physicochemicalproperties of the soil offer the appropriate habitatfor the production of this type of quinoa (Rojaset al. 2010). Morphophenological characteristicsof quinoa show that there is a huge diversity invarieties or local ecotypes (del Castillo et al. 2007).Therefore, available commercial quinoas exhibitwide genetic diversity, showing great variability inplant color, inflorescence and seeds, inflorescencetype, protein, saponin and betacyanine contents,and calcium oxalate crystals in leaves. Thisextreme variability may reflect wide adaptation to

6 Quinoa: Improvement and Sustainable Production

different agroecological conditions such as soil,rainfall, nutrients, temperature, altitude, drought,salinity, and UV-B radiation.

Quinoa is a dicotyledonous annual herba-ceous plant usually erect, with a height of about100–300 cm, depending on environmental con-ditions and genotype. Leaves are generally lobed,pubescent, powdery, rarely smooth, and alterna-tively inserted on a woody central stem. The plantmay be branched or unbranched, depending onvariety and sowing density. Stem color may begreen, red, or purple. The leafy flower cluster(a panicle with groups of flowers in glomerulus)arises predominantly from the top of the plantand may also arise from the leaf junction (axil) onthe stem. Flowers are sessile, of the same color asthe sepals, and may be hermaphrodite, pistillate,or male sterile. The stamens have short filamentsbearing basifixed anthers; the style has two orthree feathery stigma. The fruit occurs in anindehiscent achene, protected by the perigonium.The seeds are usually somewhat flat, measure1–2.6 mm, and approximately 250–500 seedscomprise 1 g. The seeds also exhibit a great varietyof colors – white, yellow, red, purple, brown, andblack, among others. Seed embryo can be up to60% of the seed weight and forms a ring aroundthe endosperm. The taproot (20–50 cm long) isprofusely branched and forms a dense web ofrootlets that penetrate to about the same depthas the plant height (National Research Council1989).

The vegetative period of quinoa is related tophotoperiod sensitivity and varies between 120and 240 days. Some varieties, such as CO-407from Chile, have a vegetative period between110 and 120 days, but others, such as the CICAvariety, have more than 200 days. On the otherhand, C. quinoa is a C3 species confirmed byanatomical studies and carbon isotope discrim-ination (González et al. 2011). The δ13C valuesof leaves of 10 varieties of quinoa ranged from aminimum of −27.3‰ to a maximum of −25.2‰(Table 1.2). Typical values of δ13C in C3 speciescan ranges from −35 to −20‰ (Ehleringer andOsmond 1989).

C. quinoa is an allotetraploid (2n= 4x= 36) andexhibits disomic inheritance for most qualitative

Table 1.2 Carbon isotope composition δ13C of 10varieties of quinoa.

Cultivar δ13C

Amilda −25.6Chucapaca −26.3CICA −26.6Kancolla −27.3Kamiri −26.7Ratuqui −26.4Sayaña −26.3Robura −25.7Sajama −25.2Samaranti −25.6

traits (Simmonds 1971; Risi and Galwey 1989;Ward 2001; Maughan et al. 2004). The speciesclosest to cultivated quinoa are Chenopodiumhircinum and Chenopodium berlandieri, whosebasic chromosome number (2n= 4x= 36) isthe same as that of the cultivated types, andChenopodium petiolare and Chenopodium pallidi-caule, which have 2n= 2x= 18 chromosomes(Fuentes et al. 2009). Quinoa species includesboth domesticated cultivars (subsp. quinoa) andfree-living, weedy forms (subsp. milleanum ormelanospermum) (Wilson 1981, 1988). Domes-ticated and weedy quinoa populations aresympatric, and share a fundamentally autogamousreproductive system as well as a wide range ofvariation in leaf and grain size and color (delCastillo et al. 2007). Wild and domesticated pop-ulations of quinoa exist under cultivation, whichindicates that domesticated quinoas are generallyaccompanied by wild populations in their variousdistribution areas. Thus, natural hybridizationbetween wild and domesticated populationsprobably occurs easily (Fuentes et al. 2009). Thehighest variation in cultivated quinoa is foundnear Titicaca Lake, between Cuzco (Peru) andLake Poopó (Bolivia), and this is where scientistsbelieve the crop was first domesticated (Heiserand Nelson 1974). The main varieties knownin this region are Kancolla, Cheweca, Witulla,Tahuaco, Camacani, Yocara, Wilacayuni, Blancade Juli, Amarilla de Maranganí, Pacus, Rosadade Junín, Blanca de Junín, Hualhuas, Huancayo,Mantaro, Huacariz, Huacataz, Acostambo, BlancaAyacuchana, and Nariño in Peru and Sajama,

Quinoa: An Incan Crop to Face Global Changes in Agriculture 7

Real Blanca, Chucapaca, Kamiri, Huaranga,Pasancalla, Pandela, Tupiza. Jachapucu, WilaCoymini, Kellu, Uthusaya, Chullpi, Kaslali,and Chillpi in Bolivia (Hernández Bermejo andLeón 1994). Throughout the Andean region,there are several genebanks where over 2,500quinoa accessions are preserved in cold-storagerooms: in Peru, at the experimental stations ofCamacani and Illpa (Puno), K’ayra and Andenes(Cuzco), Canaan (Ayacucho), Mantaro y SantaAna (Huancayo), Baños del Inca (Cajamarca); inBolivia, at the Patacamaya station of the IBTA;and in Ecuador, at the Santa Catalina station ofINIAP.

QUINOA AND ENVIRONMENTALSTRESSES: DROUGHT AND SALINITY

Soil salinization is one of the major environmen-tal issue affecting crop production, especiallyin marginal landscapes or areas with limitedresources (Munns and Tester 2008; Rengasamy2010; Munns 2011; Hussin et al. 2013). Theintensive use of valuable natural resources suchas land and water, along with high soil evapo-transpiration and inefficient irrigation systemsassociated with poor water and soil management,inevitably accelerate secondary salinization thatusually results in the loss of productive areas(Munns 2005; Hussin et al. 2013). Nearly 20%of the world’s cultivated areas and about half ofthe world’s irrigated lands are salt affected (FAO2008). Out of the current 230 Mha of irrigatedland, 45 Mha are salt-affected soils (19.5%), andof the almost 1,500 Mha dry agricultural land,32 Mha are salt affected to varying degrees byhuman-induced processes (Munns and Tester2008). Salinization of irrigated lands causes a lossof US$12 billion of the annual global income(Ghassemi et al. 1995).

In this context, enhancing salt tolerance of theconventional crops has proved to be somewhatelusive in terms of genetic manipulation to allowgreater yields in salt-affected soils and marginalareas (Flowers 2004). The results, althoughpromising, remain insignificant so far (Läuchliand Grattan 2007). An alternative approach is

the use of naturally occurring xero-halophyte forcrop production, “cash crop halophytes,” as theyalready have the required level of salt tolerance(Lieth et al. 1999). The sustainable utilizationof halophytes as cash crops may significantlycontribute toward food, feed, fuel, wood, fiber,chemical production, and environmental quality(dune stabilization, combating desertification,bioremediation, or CO2 sequestration) in manycountries (Geissler et al. 2010; Hussin et al. 2013).Hence, research has focused more and more onthe identification and selection of plant speciessuch as C. quinoa that are naturally tolerant todrought and salinity.

Quinoa is one of the few crops, if not theonly crop, able to grow in the most extremeenvironmental conditions (Jacobsen et al. 2003).In effect, quinoa can be cultivated from sea levelto 4,000 masl, even in the Bolivian Altiplano withan extreme altitude of 4,200 masl. Quinoa is alsoremarkably adaptable to different agroecologicalzones. It adapts to hot, dry climates, can grow inareas of varying relative humidity, ranging from40% to 88%, and can withstand temperaturesfrom −4 to 38∘C. Quinoa can grow in marginalsoils lacking in nutrients, in soils with a widerange of pH from acid to basic (Boero et al. 1999),and even tolerates soil infertility (Sanchez et al.2003). It also has excellent tolerance to extremefrost (Halloy and González 1993; Jacobsen et al.2005, 2007), long drought periods (Vacher 1998;González et al. 2009a; Jacobsen et al. 2009),salinity (González and Prado 1992; Prado et al.2000; Rosa et al. 2009; Ruffino et al. 2010; Hariadiet al. 2011), and high solar radiation (Palenqueet al. 1997; Sircelj et al. 2002; Hilal et al. 2004;González et al. 2009b). It has high water useefficiency (WUE) shown by its tolerance orresistance to lack of soil moisture and producesacceptable yields with rainfall of 100–200 mm(Garcia et al. 2003, 2007; Bertero et al. 2004).Quinoa resists up to 3 months of drought at thebeginning of its growth cycle. To make up forthis part of its growth cycle, the stalk becomesfibrous and roots strengthen. When rains come, itrecovers physiological activity (National ResearchCouncil 1989). Some varieties can grow in saltconcentrations similar to those found in seawater

8 Quinoa: Improvement and Sustainable Production

(40 dS/m) and even higher, well above thethreshold for any known crop species (Hariadiet al. 2011; Razzaghi et al. 2011).

Salt tolerance is a complex trait and attributedto a plethora of interconnected morphologi-cal, physiological, biochemical, and molecularmechanisms. These mechanisms are linked tothe major constraints of salinity on plant growth(i.e., osmotic effects, restriction of CO2 gasexchange, ion toxicity, and nutritional imbalance)and operate in coordination to alleviate both thecellular hyperosmolarity and ion disequilibrium(Koyro 2006; Flowers and Colmer 2008; Geissleret al. 2009). The primary deleterious effectof soil salinity on plant growth is due to anosmotic effect, resulting from the lower soil waterpotential (Ψ), defined as the work water can doas it moves from its present state to the referencestate. The reference state is the energy of a poolof pure water at an elevation defined to be zero(Munns 2002; Koyro et al. 2012). A low valueof (Ψ) interferes with plant ability to take upwater from the soil and, hence, causes a growthreduction, along with a range of physiologicaland biochemical changes similar to those causedby water deficit (Larcher 2001; Schulze et al.2002; Munns 2005). To endure osmotic con-straint, salt-tolerant plants are more restrictivewith water loss via transpiration by a sensitivestomatal closure response. Inevitably, this leadsto a decrease in the apparent photosynthetic ratedue to a restricted availability of CO2 for thecarboxylation reaction (stomatal limitation ofphotosynthesis) (Huchzermeyer and Koyro 2005;Flexas et al. 2007; Dasgupta et al. 2011; Benzartiet al. 2012), thereby suppressing plant growthand productivity (D’Souza and Devaraj 2010;Gorai et al. 2011; Tarchoune et al. 2012; Yan et al.2013).

According to several studies, quinoa toleranceto drought and salinity stresses is dependenton its vegetative stage (Bosque Sanchez et al.2003; Garcia et al. 2003; Jacobsen et al. 2003).At the cotyledonary stage, the high adaptabilityof quinoa to soil salinity is related to metabolicadjustment. In studies carried out with seedlingsof the Sajama cultivar, it was demonstrated thatsalinity tolerance depends on improved metabolic

control of ion absorption and osmotic adjustmentthrough osmolyte accumulation derived from asalt-induced altered carbohydrate metabolism(Rosa et al. 2009; Ruffino et al. 2010), whereasin early maturing stage, it is also related tostructural and physiological adaptations. In thisway, quinoa avoids the negative effects of droughtthrough the development of a deep and dense rootsystem, reduction of the leaf area, leaf dropping,special vesicular glands (salt bladders), smalland thick-walled cells adapted to losses of waterwithout loss of turgor even at severe water losses,and stomatal closure (Jensen et al. 2000; Adolfet al. 2013).

Although quinoa was classified as a highlysalt-tolerant species (Jacobsen 2003; Hariadi et al.2011; Razzaghi et al. 2011; Eisa et al. 2012; Adolfet al. 2013), many quinoa cultivars show distinctvariability in their germination and growthresponses to salinity. More than 200 quinoa acces-sions have been tested under saline conditionsand found to be different in their responses tosalinity. Differences were observed at germinationstage and also later during the vegetative growthstage (Adolf et al. 2012). Moreover, salt toleranceat germination is not necessarily correlated withthe degree of tolerance at later developmentalstages. Eisa et al. (2012) found that the growthof the Peruvian quinoa cultivar “Hualhuas” wasslightly stimulated in response to a low salinitylevel (20% seawater salinity). The same trend ofsalt-induced growth stimulation has been recentlyobserved for the cultivar “CICA” (Fig. 1.1). Theoverall growth of CICA plants based on freshweight (FW) gain was significantly increased∼85% compared with control plants grownunder non-saline conditions. This increase wasmainly a result of increased shoot FW rather thanroot FW (Fig. 1.1). Similar salt-induced stimu-lation of growth has also been reported for otherPeruvian and Bolivian quinoa cultivars (Wilsonet al. 2002; Koyro and Eisa 2008; Hariadi et al.2011). Furthermore, the Andean hybrid grownat salinity level of 11 dS/m showed increases inboth leaf area and dry mass when comparing withplants grow at control salinity level of 3 dS/m.As shown in Fig. 1.1, salinity tolerance thresholdfor CICA variety was at 200 mM NaCl, whereas

Quinoa: An Incan Crop to Face Global Changes in Agriculture 9

Ctr. 100 200NaCI concentration (mM)

300 400 5000

50

100

150

200

b

a

bc

cded

e

Fre

sh w

eigh

t (g)

R S AI JI In Poly. (Growth)

Fig. 1.1 Development and growth responses of differentorgans (expressed as fresh weights) of C. quinoa cv. CICAgrown at different NaCl concentrations. The dotted line marksthe C50 value. Each column represents the mean value ofthree replicates and the bars represent standard deviations.Columns with the same letter are not significantly different at P≤0.05, Duncan test. (R) root, (S) stem, (Al) adult leaf, (Jl) juvenileleaf, and (In) inflorescence.

C50 was slightly above 40% seawater salinity. Thesalinity tolerance threshold is the salt level thatleads to the initial significant reduction in themaximum expected yield (Shannon and Grieve1999), whereas C50 is the water salinity leading to50% growth reduction in the maximum expectedyield. In contrast, salinity levels above thresholdvalue (supraoptimal condition) severely inhibitplant growth in many quinoa cultivars (Hariadiet al. 2011; Eisa et al. 2012). Seawater salinity level(500 mM NaCl) led to a significant reduction(∼66%) in the FW of CICA plants relative tothe control (Fig. 1.1). Inhibition of the initiationof new leaves and the formation of small leaves,some with symptoms of nutrient disorders,might contribute to the low FW observed at thissalinity level. Interestingly, the plants displayedconspicuous growth and continued to grow evenat seawater salinity levels (Fig. 1.1). Together,these results indicate that the CICA cultivar ishighly salt tolerant and productive, capable ofgrowing even under sea water salinity levels.

Salinity stress results in a decrease of pho-tosynthesis in a wide variety of plant species

(Sudhir and Murthy 2004). However, manyhalophyte species show higher level of photo-synthesis under conditions of elevated salinity(Andersone et al. 2012), depending on the levelof salt tolerance of the species and/or genotypes(Brock et al. 2007). Quinoa cultivars also showdifferent photosynthetic responses, depending onparental origin. Recently, Adolf et al. (2012) foundsignificant differences in both photosyntheticCO2 assimilation and stomatal conductance whentwo varieties of quinoa when grown under salineconditions. “Utusaya,” originating from the salarregion of Bolivia, maintained a relatively highstomatal conductance, with only 25% reductionin net CO2 assimilation when compared with theuntreated control plants. In contrast, the cultivar“Titicaca” that has been bred in Denmarkshowed a higher decrease in stomatal conductanceand also a 67% reduction in CO2 assimilation.Interestingly, in the Utusaya variety, both thestomatal conductance and the photosynthesis ratewere generally low under non-saline conditions,whereas these did not decrease in the Titicacavariety. Thus, it may be assumed that in salineenvironments, the Utusaya variety has a genet-ically improved osmoregulator mechanism tocounteract the deleterious osmotic effects of saltand has less need to reduce water loss by tran-spiration (Adolf et al. 2013). A similar trait wasobserved between the CICA (less salt tolerant)and the Hualhuas (more salt tolerant) cultivarsgrown under increasing saline levels. The CO2assimilation (net photosynthetic rate, PN) of theCICA cultivar steadily and significantly declinedwith increasing water salinity, reaching only 1.5%of the control values at seawater salinity treatment(Table 1.3). This result was consistent withobservations on the effect of salinity on photosyn-thesis in many salt-tolerant species (Ashraf 1999;Bayuelo-Jiménez et al., 2003; Qiu et al. 2003;Koyro 2006). In a previous study, however, Eisaet al. (2012) showed that the photosynthetic activ-ity of the Hualhuas cultivar was less affected withsalt-induced reduction of about 72% at seawatersalinity level. Furthermore, the photosyntheticresponses of the cultivars CICA and Hualhuascorrespond with the assumptions of Kao et al.(2006) and Moradi and Ismail (2007), who assume

10 Quinoa: Improvement and Sustainable Production

that relatively higher salt-tolerant species wouldhave less reduced net photosynthesis. On theother hand, the reduction of PN observed inCICA coincided with the progressive decreaseof stomatal conductance (CS), suggesting thatsalinity impacted the photosynthesis of CICAplants, at least partly, by an enhanced stomatalclosure. Positive correlations between PN and CShave been found in C. quinoa, Hualhaus cultivar(Eisa et al. 2012), Atriplex prostrata (Wang et al.1997), Atriplex nummularia and Atriplex hastata(Dunn and Neales 1993), Atriplex centralasiatica(Qiu et al. 2003), and Avicennia marina (Ball andFarquhar 1984).

According to Moradi and Ismail (2007) andCentritto et al. (2003), reduction of stomatalconductance is a significant way to decreasewater loss from the leaves via transpiration andcould be considered as an adaptive feature forsalt tolerance. In CICA plants, the salt-inducedreduction of CS gives a strong inhibition of thetranspiration rate (E), which reaches a minimumvalue at the highest salinity treatment (Table 1.3).This would contribute to conservation of waterand also maintain a positive water balance. In fact,lower values of E represent an additional adaptivemechanism for coping with high salinity levels,as it could reduce salt loading into leaves andhence prolong the leaf lifespan by maintaining asubtoxic level of salt (Everard et al. 1994; Koyro2006).

The coordinated regulation of CO2/H2O gasexchange is considered a key determinant forplant growth and biomass production under salineconditions (Romero-Aranda et al. 2001; Lu et al.

2002; Gulzar et al. 2003, 2005). In Hualhuas, Eisaet al. (2012) found that salt-induced reductionof transpiration rate was proportionally largerthan the photosynthetic rate, leading to improvedphotosynthetic water use efficiency (PWUE).However, this is not the case for CICA, as thesalt-induced reduction of photosynthetic rate wasproportionally larger than that of the transpira-tion rate, resulting in a marked decline of PWUE(Table 1.3). According to Naidoo and Mundree(1993) and Koyro (2000), increasing PWUEis an important adaptive feature for long-termsurvival of plants and would be an advantagein saline environments. This may explain therelatively lower salt tolerance of CICA comparedto Hualhaus. Interestingly, salt-induced reductionof PN in CICA showed a positive correlation withCS, but not with intercellular CO2 concentration(Ci) (Table 1.3), suggesting that Ci is not thelimiting factor for photosynthesis reduction inCICA under saline conditions.

Non-stomatal inhibition of photosynthesis insalt-stressed plants, particularly under severestress conditions, has also been reported forseveral other crop species such as Gossypiumhirsutum and Phaseolus vulgaris (Brugnoli andLauteri 1991), Oryza sativa (Dionisio-Sese andTobita 2000), Helianthus annuus (Steduto et al.2000), and Beta vulgaris (Dadkhah 2011), amongothers. This inhibition of photosynthetic capacityhas been attributed to an inhibited coupling factoractivity (Tezara et al. 2008), reduced carboxy-lation efficiency (Wise et al. 1992; Jia and Gray2004), reduced amount and/or activity of crucialphotosynthetic enzymes such as Rubisco (Parry

Table 1.3 Effect of elevated water salinity on the net photosynthesis rate (PN), transpiration rate (E), Stomatal conductance (Cs),ratio of the internal to the external CO2 concentration (Ci/Ca), and photosynthetic water use efficiency (PWUE) of C. quinoa cv.CICA. All of these values are at the light saturation point of photosynthesis.

Treatments PN (μmol m−2 s−1) E (mmol/m2s) Cs (mmol H2O/m2s) Ci/Ca PWUE (%)

Control 16.615a ± 1.011 2.733a ± 0.234 0.164a ± 0.018 0.491a ± 0.022 0.625a ± 0.019100 mM 12.310b ± 0.122 2.417a ± 0.045 0.140b ± 0.003 0.588b ± 0.006 0.510bc ± 0.006200 mM 10.907c ± 0.119 1.998b ± 0.019 0.111c ± 0.002 0.550b ± 0.010 0.546b ± 0.007300 mM 8.088d ± 0.398 1.232c ± 0.148 0.064d ± 0.008 0.577b ± 0.018 0.446c ± 0.034400 mM 1.105e ± 0.240 0.357d ± 0.032 0.017e ± 0.002 0.747c ± 0.029 0.256d ± 0.034500 mM 0.237e ± 0.048 0.280d ± 0.009 0.012e ± 0.000 0.882e ± 0.015 0.171e ± 0.018

Means within a column followed by the same letter are not significantly different at P ≤ 0.05, as determined by Duncan test. Eachmean represents three replicates.