- Open Access
Plant breeding for organic agriculture: something new?
Agriculture & Food Security volume 4, Article number: 25 (2015)
The role of both organic (OF) and conventional (CF) farming remains open to debate particularly when related to food security and climate change. Targeting plant breeding for OF can contribute to reduce its yield gaps vis-à-vis CF. Currently, the cultivars produced for CF are also used in OF, however, it is unreasonable that all lines bred for CF will always perform well in OF. Nonetheless, plant breeding goals for OF and CF converge at aiming for high productivity, host plant resistance or tolerance to biotic and abiotic factors, and high resource-use efficiency. Likewise end-use quality and local adaptation may be more important for OF as the resource recycling and quality of the inputs that are used vary from region to region, even though OF practices are highly regulated. This article provides an overview on organic plant breeding (OPB) with a perspective from conventional plant breeding, highlights the main traits, their source of variation, and what methods and tools are available for their breeding. It concludes listing some organic crop breeding achievements and providing an outlook on what needs to be done for OPB.
Food supply is a major concern for human kind and takes place in a complex global scenario. On one side there is an increasing demand for food, i.e., the human population, projected to be by 9 billion in 2050 and its dietary shifts, requires more food to be produced, and at the same time humankind is undergoing through an increase of certain medical conditions (type II diabetes, coronary heart disease, etc.) that reduce life expectancy . On the other side, there are factors that seriously threat food production, i.e., climate change and the constant pressure of pests and pathogens, of which the global patterns of infestation/infection are also expected to vary due to this changing climate.
There is much debate on how exactly food must be produced. Even though, there is a general agreement in that sustainable agriculture is to what agricultural systems should aim. However, sustainability has been conceptualized in several ways . From its Latin root (sustinere), sustainable means “to maintain,” “to support,” or “to endure.” Sustainability, in the ecological context, is the conservation of the ecological balance by avoiding the depletion of natural resources . The American Public Health Association (APHA) defines sustainable food systems as the ones “that provide healthy food to meet current food needs while maintaining healthy ecosystems that can also provide food for generations to come with minimal negative impacts to the environment” . This food system should also promote local production and make “nutritious food available, accessible and affordable to all” individuals .
Organic and conventional farming (CF) systems are the center of a heated debate; particularly, when highly relevant topics, such as food security and climate change, are discussed. Especially, when supporters of organic farming (OF) claim that this system is synonymous of agricultural sustainability or imply in their argumentation that OF is the only way to achieve sustainable food production  and that it could also secure global food supply [6, 7]. These arguments have been thoroughly analyzed by other authors [8–10], and the conceptual differences between sustainable agriculture and OF have already been pointed out .
It is important to note here that low-input farming systems, which are driven by resource-limited farmers, are considered within CF. This implies that the so called “breeding for CF” also encompasses those low-input/tech cropping systems. We consider that this inclusion is relevant since OF enthusiasts usually consider CF only as a high-input system, and also because of the plant breeding purposes of obtaining widely adapted cultivars.
Organic farming, food supply, and the environment
The aim of OF is the creation of holistic farming systems that are sustainable in all regards. This approach should therefore rely on the use of farm-derived renewable resources that provide acceptable levels of crop, livestock, and human nutrition. OF should also provide protection from pests and pathogens due to the harmonious management of resources and understanding of ecological and biological processes. The very well-known characteristic of OF is that it produces food without the use of any synthetic fertilizer or pesticide, and neither with the use of genetically modified organisms (GMO). For this reason OF enthusiasts consider these systems to have positive impacts on the environment by enhancing soil fertility, contributing to mitigate climate change, and conserving biodiversity.
Research has shown that OF can contribute to reduce soil carbon losses, mainly due to the application of organic fertilizers such as compost or stacked manure which should derive from the integration of crop production and livestock. Research comparing the dynamics of soil organic carbon between OF and CF shows that the former can significantly increase the concentration, stock, and sequestration rates of organic carbon in the soil . Still, this feature alone of OF is not able to mitigate climate change, because it does not tackle the issue of reducing the emission of greenhouse gases (GHG), and neither accounts for N2O or other emissions derived from agricultural practices .
GHG emissions in OF vary depending on the agricultural product. For example, organic beef and some organic crops emit less GHG compared with their counterparts in conventional systems, whereas the organic production of milk, pork, poultry, and egg emit between 16 and 46 % more GHG because of their higher methane and N2O emissions [12, 13].
High concentrations (7 %) of organic matter in the soil are another feature of OF . The evidence shows that this is not due to the higher inputs (65 %) of organic fertilizers per se in OF than in CF, but rather due to a cascade effect in which an increased microorganism activity decomposes the organic residues . But, tillage and crop rotation may play a role in increasing the organic matter content in the soils. In CF also it is possible to increase the concentration of organic matter in the soils by increasing manure inputs .
Biodiversity in OF is generally reported to be between 10.5 and 30 % higher than in CF [14–16]. However, when Gabriel et al.  studied the biodiversity in winter cereals in UK by contrasting both farming systems, they concluded that this increase in biodiversity is highly correlated with grain yield reductions independently of the production system. This finding means that CF can be as diverse as OF with lower yields, and thus OF “per se does not have an effect (on biodiversity) other than via reducing yields and therefore increasing biodiversity.” Hence, “in high-productivity landscapes, OF is not an efficient way of maximizing diversity and yield, but land sparing might be” .
The positive impacts of OF on the environment are reduced when looking at the yield gap between this production system and CF. While OF has positive environmental effects when its impact is measured per area unit, it has negative environmental effects in a product unit basis . This is because for OF to reach production levels similar to those of CF there would be a need to increase the agricultural land by 84 % , and in the current situation humankind cannot afford to increase the land area where food is produced.
Edible yields in OF are generally lower than in CF. However, the differences highly depend on the agricultural system . For example, the yield difference in fruit and oilseed crops is 3 and 11 % lower than in CF, respectively; while organic cereals and vegetables have a 26 and 33 % of yield reduction in OF . The grain yield gap between OF and CF winter wheat systems is 54 % in the United Kingdom , while in Sweden and Finland the edible yield of cereals and potatoes is about 46 and 60 % lower, respectively . Seufert et al.  also made a comparison of yield gaps between developing and developed countries and found that the differences are by 43 and 20 % lower yields in OF, respectively. Kirchmann et al.  suggest that the main limitation for OF to have high yields is the availability of soil nutrients, weed control, and limited possibility to increase fertility in low-nutrient soils. Other research reported that both farming systems can have similar yields [18, 19]. However, to reach this level of productivity, the nutrient inputs in the form of manure need to be as high or higher than in CF systems, which in great measure originate from conventional systems .
Organic farming supporters frequently raise the issue that modern cultivars and particularly transgenic crops fail in contributing to sustainable food production systems due to the strong selection pressure on pests and pathogens caused by those modern resistant cultivars, since eventually such host plant resistance is broken causing new outbreaks of pests and pathogens . However, this is a characteristic of any host plant resistance that puts strong selection pressure on the pathogens and pests [21, 22]. Since in great measure, resistance depends on the type of pathogen that the plants deal with, the evolutionary potential of the pathogen population, and the type of resistance that is being utilized [21, 22]. Yet, it has been shown in wheat that it is possible to breed for broad and durable resistance [23–25].
Conventional farming could certainly become more sustainable by adopting practices that have less negative impacts on the environment , and in that sense there is a great potential to improve CF systems. Furthermore, a question that would naturally rise is whether OF is really a sustainable food production system according to the APHA definition, since productivity and affordability are generally not considered in the definition of OF. Thus in agreement with other authors [8–10], we consider that OF today is not the way to sustainably feed the world, particularly in a scenario where food demand is constantly increasing, for which it requires high food productivity with extreme care of the natural resources. However, addressing demand-side factors through policies can greatly contribute to feed the world and preserve the environment . From the food supply perspective we think that sustainable cropping systems can be achieved, by adopting practices that are less harmful to the environment, e.g., deploying resistant or tolerant cultivars to biotic and abiotic stresses along with the improvement of the resource-use efficiency through breeding efforts to reduce the inputs that are harmful to the environment, accompanied with better agronomic practices and technologies that also enhance productivity and resource-use efficiency.
OF may be successful for a niche market in certain developed countries in Europe and the USA, while helping to enrich the organic C content in soil. That said, the higher productivity of integrated farming (OF and CF) is essential for enabling food security in most developing countries.
Organic plant breeding
Targeting plant breeding for OF can contribute to reduce the yield gaps between both production systems: CF and OF. However, the issues of whether these systems should necessarily be regarded as competing entities between each other and if they should necessarily be comparable in terms of productivity require further analysis. Since it is not clear whether OF yields should aim to be equal to those in CF or simply being higher than they are today.
For both conditions, the breeding goals converge at aiming for higher productivity, incorporation of resistance or tolerance to biotic and abiotic factors, and higher resource-use efficiency (water, nutrients, light, etc.). Local adaptation may be more important for OF as the resource recycling and quality of the inputs that are used can vary from region to region, even though OF practices are highly regulated. Likewise, organic plant breeding (OPB) aims to fit cultivars into farming systems relying on renewable organic resources.
One frequent issue noted by OF enthusiasts is that the cultivars bred for CF do not always perform well under OF conditions [27, 28]. There is no reason, however, to think that all cultivars produced by conventional breeding programs will perform well in all environments, even in all CF environments. Consequently, it is unreasonable to think that all lines produced in an organic breeding program will perform well in all OF conditions. The genotype-by-environment interaction (G × E) is a common situation that plant breeders have to deal with and if exploited correctly it is still possible to make important progress in crop improvement. Even under CF, which for some OF supporters it simply consists of high-input-standardized practices, G × E is a highly important aspect to be considered, because in reality there are also low-input and diverse CF systems, driven by the resource-poor farmers in developing countries. Hence, from the pure plant breeding perspective, OF can be considered as a separate environment with a strong component of local adaptation, in which the necessary traits and selection methods should be incorporated.
Traits and sources of variation
Despite that the general breeding goals for both, OF and CF are similar, there are specific traits that are required for OF as the utilization of synthetic agrochemicals are banned in this system. Weed competitiveness and the ability to establish symbiont relations with micro-organisms in the soil are relevant for OF because they can enhance the uptake of resources and its use efficiency [27, 29]. Research has shown that there exists genetic variation for weed competitiveness in cereals [30–33], and that early vigor and allelopathy can be useful traits to enhance weed suppression [30, 34].
Genetic variation for nitrogen use efficiency has been found in potato [35, 36] or wheat , and genomic regions associated with this trait have been identified in barley . Additionally, studies have shown that nitrogen use efficiency can be improved through agronomic practices . Genetic variation and genomic regions associated with the uptake of micronutrients have also been reported in wheat [40, 41]. Nelson et al.  found, however, that the percent of arbuscular mycorrhizal fungi was negatively correlated with iron and zinc concentrations in winter wheat, but positively correlated with manganese, copper, and potassium. Mycorrhizal fungi play an important role in soil fertility and nutrient uptake in OF systems, whereas in CF their presence is severely reduced . Efforts to breed crops for high micronutrient uptake are undergoing in public plant breeding programs [44, 45], thus OPB can utilize the developed germplasm in such plant breeding programs.
Traits such as tolerance to abiotic stresses (heat, drought, salinity, water lodging, etc.) and host plant resistance to pathogens and pests are not exclusive for OF, but they are highly dependent of the geographical area where the breeding is targeted. Resistance to seed-borne pathogens is of great importance, since seed treatments are limited in organic seed production. Root diseases are considered to be important only during the conversion period from CF to OF [46, 47]. In wheat, for diseases such as rust and powdery mildew, OPB can take advantage of the achievements that have been made in breeding for durable and broad resistance to these diseases [23, 25, 48].
Several authors have described in a more detailed way the necessary traits and ideotypes of cereals and vegetables for OF [27, 29, 49, 50]. Here our aim is not to repeat those descriptions but to emphasize that in our view plant breeding for OF and CF only differs in certain specific traits that are important for the adaptation in either of the environments, but not in the general breeding goals. OPB requires the application of breeding methods that are therefore in line with the OF principles.
The sources of variation to incorporate relevant traits in cultivars for OF conditions are not different from the sources of variation for cultivars aimed for CF; that is in their natural origin. For instance, wild relatives and landraces are sources of variation for both plant breeding systems. The processes of how these sources of genetic variation are incorporated in the production of new cultivars are, however, regulated and subject to OF and OPB principles .
In the particular case of wheat, Lammerts van Bueren et al.  foresee the utilization of synthetic hexaploids in OPB programs, as they are a rich source of genetic variation for the development of new wheat cultivars . It is not clear, however, whether they can be used for organic wheat breeding, as they are produced with the aid of colchicine treatments  which operate below the cell level, and according to some reports they should be forbidden in OF [29, 53, 54].
Methods and tools
Organic plant breeding is restricted to specific conventional breeding practices, in general to crossing methods that do not break the reproductive barriers between species, and to selection methods based on the evaluation and selection of whole plant performance [29, 53, 54]; i.e., (1) intraspecific crossing, (2) backcrossing, (3) mass and individual selection, (4) selection via DNA markers, (5) hybrid cultivars—as long as next generation is fertile and the hybrid production does not chemically induce sterility, and (6) meristem culture. On the other hand, the technologies or methods that engineer plants at the DNA level are considered to be incompatible with OPB [29, 53–55], e.g., (1) genetically modified organisms and (2) the application of synthetic hormones and colchicine treatments.
New breeding techniques make it possible to precisely incorporate particular characteristics from wild crop relatives or landraces into modern crops. In that line, some authors have analyzed the possibility of implementing modern technologies in OPB to rewilding modern crop cultivars  and whether this modern techniques can fit within the four principles of OF (health, ecology, fairness, and care). However, Lammerts van Veuren et al. [57, 58], had already argued that cisgenesis and reverse breeding based germplasm are products of processes that corresponds to the development of GMO and thus this technique should be banned from OF and OPB.
Development of cultivars adapted to OF conditions can be successfully achieved if plant breeding programs combine the selection of the progeny in optimal and organic or low-input environments. This can be seen as one of the elements under which the Green Revolution took place : shuttle breeding, which consists in exchanging segregating generations between different environments to achieve wide adaptation or broad disease resistance. Alternation of germplasm between CF and OF at later segregating generations is considered an important component of commercially sustainable OPB programs by some authors [60–62]. A modality of this shuttle breeding scheme, is to only carry out selections of advanced generation progenies, developed by conventional breeding procedures, under optimum organic environments to determine their value for cultivation and use in further testing; this is advantageous, particularly when there is limitation of financial, human, and institutional resources in OPB.
Some authors consider, however, that it is necessary to carry out selection solely under organic environments as it is the only way for the plants to fully express their genetic potential [28, 63]. Thus, participatory plant breeding (PPB) and evolutionary breeding (EB), have been proposed as suitable breeding methods to target OF [64–68]. These methods facilitate the selection for local adaptation and for the particular needs of farmers, they also empower farmers as they allow closer interaction between them and breeders and give farmers greater freedom to choose germplasm. Particularly, for the case of PPB that can lead to a faster cultivar adoption [20, 69].
Organic crop breeding achievements
Private breeding companies (especially small–medium enterprises) and some public institutions, particularly in Europe and North America have finely established OPB programs. For instance in Austria, Canada, France, Germany, Switzerland, and USA organic winter wheat breeding programs have been initiated [27, 70]. Projects in PPB for OF have also been established in tomato [71, 72], cauliflowers , and Lolium , while there are other OPB undertakings for cabbage, broccoli , and onion  in The Netherlands or spinach in France .
Outlook: what is new and what needs to be done for OPB
OPB has certainly made steps forward toward the development of cultivars adapted to OF, particularly after finding that conventional plant breeding cannot always provide suitable cultivars for OF in various crops such as cereals and pulses [77–79]. Below we list some points that may contribute to the further development of cultivars for OF conditions.
Examine the implementation of shuttle breeding between OF and CF to open the possibility of developing cultivars adapted to both conditions.
Larger screening of plant materials deposited in gene-banks to identify useful genetic resources for OPB .
Evaluate the possibility to implement prediction of germplasm performance in key locations with the aid of high throughput genotyping platforms and phenotypic information derived from multi-location testing.
Determine if breeding perennial crops will be suitable for sustainable OF, however if crop rotation is part of the OF system, this may not be possible .
Assess the incorporation of remote sensing phenotyping for traits like weed competitiveness so evaluation and selection intensity can be increased and higher genetic gains can be achieved faster.
Appraise the use of cultivar mixtures to deploy host plant resistance or increase resilience in agro-ecosystems prone to abiotic stress .
Quality traits should also be given priority for OPB: micronutrient content and plant growing and storage as they can influence grain quality . Traits for low-input farming systems such as increased N-uptake and N-use [91–94] and enhanced competing ability against pathogens and weeds [95, 96] will be also important for OPB.
evolutionary plant breeding
genetically modified organisms
organic plant breeding
participatory plant breeding
Tilman D, Clark M. Global diets link environmental sustainability and human health. Nature. 2014;515:518–22.
Rigby D, Cáceres D. Organic farming and the sustainability of agricultural systems. Agric Syst. 2001;68:21–40.
Oxford Dictionaries. Oxford Dictionaries; 2014.
APHA. Toward a healthy sustainable food system; 2007. policy Number: 200712.
Henning J, Baker L, Thomassin P. Economics issues in organic agriculture. Can J Agric Econ Can d’agroeconomie. 1991;39:877–89.
Badgley C, Perfecto I. Can organic agriculture feed the world? Renew Agric Food Syst. 2007;22:80–2.
Badgley C, Moghtader J, Quintero E, Zakem E, Chappell MJ, Aviles-Vazquez K, Samulon A, Perfecto I. Organic agriculture and the global food supply. Renew Agric Food Syst. 2007;22:86–108.
Connor DJ. Organically grown crops do not a cropping system make and nor can organic agriculture nearly feed the world. Field Crop Res. 2013;144:145–7.
Seufert V, Ramankutty N, Foley AJ. Comparing the yields of organic and conventional agriculture. Nature. 2012;485:229–32.
Connor DJ. Organic agriculture cannot feed the world. Field Crop Res. 2008;106:187–90.
Gattinger A, Muller A, Haeni M, Skinner C, Fliessbach A, Buchmann N, et al. Enhanced top soil carbon stocks under organic farming. Proc Natl Acad Sci USA. 2012;109:18226–31.
Tuomisto HL, Hodge ID, Riordan P, Macdonald DW. Does organic farming reduce environmental impacts?—a meta-analysis of European research. J Environ Manage. 2012;112:309–20.
Aune J. Agroecology and strategies for climate change. Dordrecht: Springer; 2012.
Tuck SL, Winqvist C, Mota F, Ahnström J, Turnbull LA, Bengtsson J. Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis. J Appl Ecol. 2014;51:746–55.
Schneider MK, Lüscher G, Jeanneret P, Arndorfer M, Ammari Y, Bailey D, et al. Gains to species diversity in organically farmed fields are not propagated at the farm level. Nat Commun. 2014;5:4151.
Gabriel D, Sait SM, Kunin WE, Benton TG. Food production vs. biodiversity: comparing organic and conventional agriculture. J Appl Ecol. 2013;50:355–64.
Kirchmann H, Bergström L, Kätterer T, Andrén O, Andersson R. Can organic crop production feed the world? In: Kirchmann H, Bergström L, editors. Organic crop production—ambitions and limitations. Dordrecht: Springer; 2008.
Pimentel D, Hepperly P, Hanson J, Douds D, Seidel R. Environmental, energetic, and economic comparisons of organic and conventional farming systems. Bioscience. 2005;55:573.
Denison RF, Bryant DC, Kearney TE. Crop yields over the first nine years of LTRAS, a long-term comparison of field crop systems in a Mediterranean climate. Field Crop Res. 2004;86:267–77.
Ceccarelli S. GM crops, organic agriculture and breeding for sustainability. Sustainability. 2014;6:4273–86.
McDonald BA, Linde C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol. 2002;40:349–79.
Parlevliet JE. Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica. 2002;124:147–56.
Singh RP, Huerta-Espino J, William HM. Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk J Agric For. 2005;29:121–7.
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323:1360–3.
Herrera-Foessel SA, Lagudah ES, Huerta-Espino J, Hayden MJ, Bariana HS, Singh D, Singh RP. New slow-rusting leaf rust and stripe rust resistance genes Lr67 and Yr46 in wheat are pleiotropic or closely linked. Theor Appl Genet. 2011;122:239–49.
Smith P, Haberl H, Popp A, Erb K-H, Lauk C, Harper R, et al. How much land-based greenhouse gas mitigation can be achieved without compromising food security and environmental goals? Glob Chang Biol. 2013;19:2285–302.
van Bueren ETL, Jones SS, Tamm L, Murphy KM, Myers JR, Leifert C, Messmer MM. The need to breed crop varieties suitable for organic farming, using wheat, tomato and broccoli as examples: a review. NJAS-Wagening J Life Sci. 2011;58:193–205.
Murphy KM, Campbell KG, Lyon RS, Jones SS. Evidence of varietal adaptation to organic farming systems. Field Crop Res. 2007;102:172–7.
Zdravkovic J, Pavlovic N, Girek Z, Zdravkovic M, Cvikic D. Characteristics important for organic breeding of vegetable crops. Genetika. 2010;42:223–33.
Bertholdsson N-O. Early vigour and allelopathy—two useful traits for enhanced barley and wheat competitiveness with weeds. Weed Res. 2005;45:94–102.
Bertholdsson N-O, Andersson SC, Merker A. Allelopathic potential of Triticum spp., Secale spp. and Triticosecale and use of chromosome substitutions and translocations to improve weed suppression ability in winter wheat. Plant Breed. 2012;131:75–80.
Hoad S, Topp C, Davies K. Selection of cereals for weed suppression in organic agriculture: a method based on cultivar sensitivity to weed growth. Euphytica. 2008;163:355–66.
Zystro JP, de Leon N, Tracy WF. Analysis of traits related to weed competitiveness in sweet corn (Zea mays L.). Sustainability. 2012;4:543–60.
Bertholdsson N-O. Breeding spring wheat for improved allelopathic potential. Weed Res. 2010;50:49–57.
Ospina CA, van Bueren ETL, Allefs JJHM, Engel B, van der Putten PEL, van der Linden CG, Struik PC. Diversity of crop development traits and nitrogen use efficiency among potato cultivars grown under contrasting nitrogen regimes. Euphytica. 2014;199:13–29.
Tiemens-Hulscher M, van Bueren ETL, Struik PC. Identifying nitrogen-efficient potato cultivars for organic farming. Euphytica. 2014;199:137–54.
Baresel JP, Zimmermann G, Reents JH. Effects of genotype and environment on N uptake and N partition in organically grown winter wheat (Triticum aestivum L.) in Germany. Euphytica. 2008;163:347–54.
Kindu GA, Tang J, Yin X, Struik PC. Quantitative trait locus analysis of nitrogen use efficiency in barley (Hordeum vulgare L.). Euphytica. 2014;199:207–21.
Swain EY, Rempelos L, Orr CH, Hall G, Chapman R, Almadni M, et al. Optimizing nitrogen use efficiency in wheat and potatoes: interactions between genotypes and agronomic practices. Euphytica. 2014;199:119–36.
Hao Y, Velu G, Peña RJ, Singh S, Singh RP. Genetic loci associated with high grain zinc concentration and pleiotropic effect on kernel weight in wheat (Triticum aestivum L.). Mol Breed. 2014;34:1893–902.
White PJ, Broadley MR. Biofortification of crops with seven mineral elements often lacking in human diets—iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 2009;182:49–84.
Nelson AG, Quideau SA, Frick B, Hucl PJ, Thavarajah D, Clapperton MJ, Spaner DM. The soil microbial community and grain micronutrient concentration of historical and modern hard red spring wheat cultivars grown organically and conventionally in the black soil zone of the Canadian prairies. Sustainability. 2011;3:500–17.
Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T, Wiemken A. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia. 2004;138:574–83.
Pfeiffer WH, McClafferty B. HarvestPlus: breeding crops for better nutrition. Crop Sci. 2007;47:S–88.
Velu G, Ortiz-Monasterio I, Cakmak I, Hao Y, Singh RP. Biofortification strategies to increase grain zinc and iron concentrations in wheat. J Cereal Sci. 2013;59:365–72.
van Bruggen AHC, Termorshuizen AJ. Integrated approaches to root disease management in organic farming systems. Australas Plant Pathol. 2003;32:141.
Bailey K, Lazarovits G. Suppressing soil-borne diseases with residue management and organic amendments. Soil Tillage Res. 2003;72:169–80.
Singh RP, Trethowan R. Breeding spring bread wheat for irrigated and rainfed production systems of the developing world. In: Kang MS, Priyadarshan PM, editors. Breeding major food staples. Iowa: BlacWell Publishing; 2007. p. 107–40.
Wolfe MS, Baresel JP, Desclaux D, Goldringer I, Hoad S. Developments in breeding cereals for organic agriculture. Euphytica. 2008;163:323–46.
Konvalina P, Stehno Z, Moudry J. Testing of suitability of ideotype and varieties of wheat for organic and low input agriculture. Lucrări Ştiinţifice, Seria Agronomie. 2007;50:248–56.
Ogbonnaya FC, Abdalla O, Mujeeb-Kazi A, Kazi AG, Xu SS, Gosman N, et al. Synthetic hexaploids: harnessing species of the primary gene pool for wheat improvement. Plant Breed Rev. 2013;37:35–122.
Mujeeb-Kazi A. Interspecific crosses: hybrid production and utilization. DF: CIMMYT; 1995.
ENVIRFOOD. Plant breeding for organic farming: current status and problems in Europe. Talsi; 2005.
van Bueren ETL, Struik PC, Tiemens-Hulscher M, Jacobsen E. Concepts of intrinsic value and integrity of plants in organic plant breeding and propagation. Crop Sci. 2003;43:1922–9.
Verhoog H. Organic agriculture versus genetic engineering. NJAS Wagening J Life Sci. 2007;54:387–400.
Andersen MM, Landes X, Xiang W, Anyshchenko A, Falhof J, Østerberg JT, et al. Feasibility of new breeding techniques for organic farming. Trends Plant Sci. 2015;20:426–34.
Van Bueren ETL, Verhoog H, Tiemens-Hulscher M, Struik PC, Haring MA. Organic agriculture requires process rather than product evaluation of novel breeding techniques. NJAS Wagening J Life Sci. 2007;54:401–12.
van Beuren ETL, Tiemens-Hulscher M, Struik CP. Cisgenesis does not solve the late blight problem of organic potato production: alternative breeding strategies. Potato Res. 2008;51:89–99.
Braun H-J, Rajaram S, van Ginkel M. CIMMYT’s approach to breeding for wide adaptation. Euphytica. 1996;92:175–83.
Muellner AE, Mascher F, Schneider D, Ittu G, Toncea I, Rolland B, Löschenberger F. Refining breeding methods for organic and low-input agriculture: analysis of an international winter wheat ring test. Euphytica. 2014;199:81–95.
Mikó P, Löschenberger F, Hiltbrunner J, Aebi R, Megyeri M, Kovács G, et al. Comparison of bread wheat varieties with different breeding origin under organic and low input management. Euphytica. 2014;199:69–80.
Baenziger PS, Salah I, Little SR, Santra DK, Regassa T, et al. Structuring an efficient organic wheat breeding program. Sustainability. 2011;3:1190–205.
Reid TA, Yang R-C, Salmon FD, Spaner D. Should spring wheat breeding for organically managed systems be conducted on organically managed land? Euphytica. 2009;169:239–52.
Chiffoleau Y, Desclaux D. Participatory plant breeding: the best way to breed for sustainable agriculture? Int J Sustain Agric. 2006;4:119–30.
Dawson JC, Murphy KM, Jones SS. Decentralized selection and participatory approaches in plant breeding for low-input systems. Euphytica. 2008;160:143–54.
Dawson JC, Rivière P, Berthellot J-F, Mercier F, de Kochko P, et al. Collaborative plant breeding for organic agricultural systems in developed countries. Sustainability. 2011;3:1206–23.
Döring TF, Knapp S, Kovacs G, Wolfe MS, Murphy K. Evolutionary plant breeding in cereals—into a new era. Sustainability. 2011;3:1944–71.
Phillips SL, Wolfe MS. Evolutionary plant breeding for low input systems. J Agric Sci. 2005;143:245.
Desclaux D. Participatory plant breeding methods for organic cereals: review and perspectives. Driebergen: Eco-PB Congress; 2005. p. 17–23.
Löschenberger F, Fleck A, Grausgruber H, Hetzendorfer H, Hof G, Al E. Breeding for organic agriculture: the example of winter wheat in Austria. Euphytica. 2008;163:469–80.
Campanelli G, Acciarri N, Campion B, Delvecchio S, Leteo F, Fusari F, et al. Participatory tomato breeding for organic conditions in Italy. Euphytica. 2015;204:179–97.
Horneburg B, Becker HC. Selection for Phytophthora field resistance in the F2 generation of organic outdoor tomatoes. Euphytica. 2011;180:357–67.
Chable V, Conseil M, Serpolay E, Le Lagadec F. Organic varieties for cauliflowers and cabbages in Brittany: from genetic resources to participatory plant breeding. Euphytica. 2008;164:521–9.
Boller B, Tanner P, Schubiger XF. Breeding forage grasses for organic conditions. Euphytica. 2008;163:459–67.
van Beuren ETL, van Soest LJM, de Groot EC, Boukema IW, Osman AM. Broadening the genetic base of onion to develop better-adapted varieties for organic farming systems. Euphytica. 2005;146:125–32.
Serpolay E, Schermann N, Dawson J, van Bueren ETL, Goldringer I, et al. Phenotypic changes in different spinach varieties grown and selected under organic conditions. Sustainability. 2011;3:1616–36.
Kamran A, Kubota H, Yang R-C, Rhawa HS, Spaner D. Relative performance of Canadian spring wheat cultivars under organic and conventional field conditions. Euphytica. 2014;196:13–4.
Kokare A, Legzdina L, Beinarovica I, Maliepaard C, Niks RE, van Beuren ETL. Performance of spring barley (Hordeum vulgare) varieties under organic and conventional conditions. Euphytica. 2014;197:279–93.
Przystalski M, Osman A, Thiemt EM, Rolland B, Ericson L, Østergård H, et al. Comparing the performance of cereal varieties in organic and non-organic cropping systems in different European countries. Euphytica. 2008;163:417–33.
Desclaux D, Nolot JM, Chiffoleau Y, Gozé E, Leclerc C. Changes in the concept of genotype × environment interactions to fit agriculture diversification and decentralized participatory plant breeding: pluridisciplinary point of view. Euphytica. 2008;163:533–46.
van Bueren ETL, Østergård H, Goldringer I, Scholten O. Plant breeding for organic and sustainable, low-input agriculture: dealing with genotype–environment interactions. Euphytica. 2008;163:321–2.
Konvalina P, Capouchová I, Stehno Z, Moudrý J. Morphological and biological characteristics of the land races of the spring soft wheat grown in the organic farming system. J Cent Eur Agric. 2010;11:235–44.
Cox TS, Bender M, Picone C, van Tassel DL, Holl JB, et al. Breeding perennial grain crops. CRC Crit Rev Plant Sci. 2002;21:59–91.
van Beuren ETL, Backes G, de Vriend H, Østergård H. The role of molecular markers and marker assisted selection in breeding for organic agriculture. Euphytica. 2010;175:51–64.
Backes G, Østergård H. Molecular markers to exploit genotype–environment interactions of relevance in organic growing systems. Euphytica. 2008;163:523–31.
Burger H, Schloen M, Schmidt W, Geiger HH. Quantitative genetic studies on breeding maize for adaptation to organic farming. Euphytica. 2008;163:501–10.
Pswarayi A, van Eeuwijk FA, Ceccarelli S, Grando S, Comadran J, Russell JR, et al. Changes in allele frequencies in landraces, old and modern barley cultivars of marker loci close to QTL for grain yield under high and low input conditions. Euphytica. 2008;163:435–47.
Kiær LP, Skovgaard IM, Østergård H. Grain yield increase in cereal variety mixtures: a meta-analysis of field trials. Field Crop Res. 2009;114:361–73.
Ryffel GU. Orgenic plants: gene-manipulated plants compatible with organic farming. Biotechnol J. 2012;7:1328–31.
Revilla P, La A, Rodríguez A, Ordás A, Malvar RA. Influence of growing and storage conditions on bakery quality of traditional maize varieties under organic agriculture. Crop Sci. 2012;52:593–600.
Brancourt-Hulmel M, Heumez E, Pluchard P, Beghin D, Depatureaux C, Giraud A, Le Gouis J. Indirect versus direct selection of winter wheat for low-input or high-input levels. Crop Sci. 2005;45:1427–31.
Fess TL, Kotcon JB, Benedito AV. Crop breeding for low input agriculture: a sustainable response to feed a growing world population. Sustainability. 2011;3:1742–72.
Hirel B, Tétu T, Lea JP, Dubois F. Improving nitrogen use efficiency in crops for sustainable agriculture. Sustainability. 2011;3:1452–85.
Dawson JC, Huggins DR, Jones SS. Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improve the performance of cereal crops in low-input and organic agricultural systems. Field Crop Res. 2008;107:89–101.
Bertholdsson N-O. Use of multivariate statistics to separate allelopathic and competitive factors influencing weed suppression ability in winter wheat. Weed Res. 2011;51:273–83.
Østergård H, Kristensen K, Pinnschmidt HO, Hansen PK, Hovmøller MS. Predicting spring barley yield from variety-specific yield potential, disease resistance and straw length, and from environment-specific disease loads and weed pressure. Euphytica. 2008;163:391–408.
LAC-H and RO did the conception and design of this article, its literature review and analysis, and manuscript writing. Both authors read and approved the final manuscript.
We thank the anonymous reviewers and the Handling Editor for their comments on the manuscript.
The authors declare that they have no competing interests.