Published online October 13, 2017 REVIEWRESEARCH & INTERPRETATION Bringing New Plant Varieties to Market: Plant Breeding and Selection Practices Advance Beneficial Characteristics while Minimizing Unintended Changes Kevin C. Glenn,* Ben Alsop, Erin Bell, Mike Goley, Jonathan Jenkinson, Bing Liu, Cheryl Martin, Wayne Parrott, Chris Souder, Oscar Sparks, William Urquhart, Jason M. Ward, and John L. Vicini K.C. Glenn, E. Bell, M. Goley, J. Jenkinson, B. Liu, C. Martin, C. ABSTRACT Souder, O. Sparks, W. Urquhart, and J.L. Vicini, Monsanto Company, Commercial-scale plant breeding is a complex 800 North Lindbergh Blvd., St. Louis, MO 63167; B. Alsop, Benson process in which new crop varieties are con- Hill Biosystems, 1100 Corporate Square Dr., St., Louis, MO 63132; tinuously being developed to improve yield and W. Parrott, Dep. of Crop and Soil Sciences, Univ. of Georgia, Athens, agronomic performance over current variet- GA 30602; J.M. Ward, Royal Canin USA, 500 Fountain Lakes Blvd., ies. A wide array of naturally occurring genetic Suite 100, St. Charles, MO 63301. Received 26 Mar. 2017. Accepted 26 changes are sources of new characteristics June 2017. *Corresponding author ([email protected]). Assigned available to plant breeders. During conventional to Associate Editor Candice Hirsch. plant breeding, genetic material is exchanged Abbreviations: GM, genetically modified; PCR, polymerase chain that has the potential to beneficially or adversely reaction; QTL, quantitative trait locus; RM, relative maturity. affect plant characteristics. For this reason, commercial-scale breeders have implemented extensive plant selection practices to identify armers and consumers have an exceptional choice of crop the top-performing candidates with the desired Fvarieties in the marketplace, with this abundance typically characteristics while minimizing the advance- being unquestioned. The advent of genetically engineered crops ment of unintended changes. Selection prac- brought the concept of genetic modification into public discourse tices in maize (Zea mays L.) breeding involve and prompted a greater interest in how our food is produced. For phenotypic assessments of thousands of can- didate lines throughout hundreds of different some, there has arisen a misunderstanding on the origin of crop environmental conditions over many years. varieties and the different methods, including the original steps Desirable characteristics can also be introduced needed for domestication, by which humans have modified the through genetic modification. For genetically genetics of our food sources (plants and animals). This misunder- modified (GM) crops, molecular analysis is used standing has been reinforced through the media and, importantly, to select transformed plants with a single copy has affected government policies around the world. of an intact DNA insert and without disruption of Plant varieties can always be improved. They can yield endogenous genes. All the while, GM crops go more, better resist pests and diseases, survive shipping better, or through the same extensive phenotypic char- simply taste better. Agricultural productivity in the United States acterization as conventionally bred crops. Data increased 50% between 1982 and 2007 while using less land and from both conventional and GM maize breeding labor (O’Donoghue et al., 2011). Productivity per unit input has programs are presented to show the similarities increased 250% since 1948 (USDA-NASS, 2017). Plant breed- between these two processes. ing and technological advances in production practices contribute equally to these increases. Today’s modern crop varieties were all derived from plant breeding. Plant breeding is an ongoing, cyclical process that involves identifying plants with desirable Published in Crop Sci. 57:2906–2921 (2017). doi: 10.2135/cropsci2017.03.0199 © Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA This is an open access article distributed under the CC BY license (https:// creativecommons.org/licenses/by/4.0/). 2906 WWW.CROPS.ORG CROP SCIENCE, VOL. 57, NOVEMBER–DECEMBER 2017 characteristics (yield, quality, resistance to abiotic and Maize, in particular, has a high level of sequence biotic stresses, etc.) and devising strategies to combine and structural diversity (Buckler et al., 2006; Springer these characteristics to obtain superior varieties (Acquaah, et al., 2009; Lai et al., 2010). A genomic comparison of 2012). In its simplest form, plant breeding results in two maize inbreds, B73 and Mo17, revealed an unprec- improved crop varieties (the commercial product, also edented level of genomic structural diversity compared referred to as cultivars or hybrids, depending on the crop) with most higher eukaryotes studied thus far (Springer et through the mating of two or more parental lines that al., 2009). For example, by a conservative estimate, at least contain desirable characteristics. The target characteris- 180 putative single-copy genes were present in one inbred tics are measured over multiple generations throughout but absent in the other, and >400 instances of putative different environments and stress conditions. Offspring sequence copy number variation between the two inbreds with desirable characteristics are selected, whereas off- were observed (Springer et al., 2009). Likewise, a compar- spring with undesired characteristics are eliminated from ison (Hirsch et al., 2016) between B73 and PH207 found further breeding. The degree of improvement in the new >2500 genes present only in one of those inbreds. variety depends on the level of genetic variation affecting The traditional perspective has been that conventional the characteristics of interest and the ability to accurately breeding does not introduce new genes, only variations measure the expression of these characteristics in many (alleles) of already existing genes. However, the emer- different environmental conditions (Fehr et al., 1987). gence of the pangenome concept (Golicz et al., 2016) Genetic engineering, commonly referred to as genetic makes it clear that conventional breeding results in the modification, is an additional tool that affords plant breed- introduction of additional genes and alleles, as well as ers new sources of characteristics, such as genes that confer novel combinations of genes. It is evident that the same abiotic or biotic stress tolerance, with many of these genes mechanisms of genome instability found in nature that not available in the crop’s genome (Prigge and Melch- lead to genetic diversity (Table 1) are also active during inger, 2012; Weber et al., 2012; Prado et al., 2014; Schnell conventional breeding (Weber et al., 2012; Schnell et al., et al., 2015). After a genetically modified (GM) line con- 2015). One example is from a recent comparison of DNA taining the desired DNA insert is chosen, the DNA insert structure (both large chromosomal changes and single- is introduced (via backcrossing) into well-characterized, nucleotide polymorphisms) across a collection of soybean conventionally bred elite varieties. The selection process [Glycine max (L.) Merr.] cultivars, many derived by con- that follows is essentially the same as is used for conven- ventional breeding (Anderson et al., 2016). This study tionally bred crops. showed that genetic changes accumulated spontaneously Using hybrid maize (Zea mays L.) as the example, data across many conventional germplasm (i.e., standing varia- are presented from Monsanto case studies to illustrate the tion). Another recent study of many maize varieties (both commercial-scale breeding practices used to supply seed to conventional and GM) showed that most of the observed farmers. The range of sources of genetic variation, extent compositional differences were associated with the back- of testing, and scope of plant selection processes used for crossing practices from conventional breeding (Venkatesh conventional breeding are presented first, followed by a et al., 2015). Repetitive DNA sequences and structural parallel overview for GM varieties. variations in plants have the potential to contribute to genetic change. Similarly, transposable genetic elements CONVENTIONAL PLANT BREEDING in maize and many other plant species can mediate genetic Sources of Genetic Variation Used for changes (Hirsch and Springer, 2017). Transposable ele- Conventional Breeding Programs ments are DNA sequences that can change position within Plant breeders improve crops by identifying sources of a genome, resulting in small insertions and deletions, as genetic variation for the characteristics of interest. Plant well as larger rearrangements such as inversions, deletions, genomes (the genetic material in each species) are highly and duplication of genes (Zhang and Peterson, 2004; variable, even within and among closely related spe- Zhang et al., 2006; Weber et al., 2012). cies (Weber et al., 2012). Table 1 shows various natural Horizontal gene transfer across phylogenetic bound- biological processes that create genetic diversity. These aries is another natural process that results in genetic include the movement of transposable elements, vertical variation in plants (Bock, 2010; Soucy et al., 2015), gene flow via mating with wild relatives, horizontal gene including transfer of DNA from bacteria, viruses, and flow (Bock, 2010) from unrelated plants, Agrobacterium, unrelated plants (Bergthorsson et al., 2003; Staginnus et florendoviruses, pararetroviruses, and mutations such as al., 2007; Liu et al., 2012; El Baidouri et