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3 Plant Improvement and Protection ENHANCING CROP PERFORMANCE Crop performance is affected by a combination of many factors, not the least of which is the collection of genes (or variants of individual genes, referred to as alleles) that provide the plant with the potential for high yield in a given farming environment. The right genes or alleles to overcome the constraints identified in Chapter 2 and enhance desirable traits in a crop are brought together by plant breeding, a complex process that, broadly defined, uses all the tools of modern plant science, including agronomy, field trials, propagation, tissue culture, genomics, molecular biology, biochem- istry, and plant physiology. This chapter describes existing and evolving tools for improving and protecting crops. The first and largest part of the chapter focuses on plant-based applications; the second part addresses plant protection using biological control methods. For many crop species, sources of germplasm that are able to overcome particular constraints have been identified, and conventional breeding tech- niques can be used to bring together the desired genes or alleles (Pingali, 2001). Within the range of germplasm available to breeders, crops contain alleles that can improve performance with respect to a variety of traits, but in many instances they do not. This is where the potential for genetic engineering of crop plants can make a tremendous contribution. Novel genes for improving a crop can come from plant, animal, or bacterial spe- cies, and molecular techniques are used to introduce them into a candidate crop. Once they are introduced into a plant, conventional plant breeding approaches are used to incorporate them into the local, elite germplasm. 

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emerging technologies benefit farmers  to Conventional and transgenic approaches to enhance crop performance are complementary and rely on many of the same molecular and informational tools. Box 3-1 contains a list of plant traits of which variants are selected by breeders (sometimes inadvertently) as targets in the process of creating improved plants for various environments. Many of the traits are linked by biochemical interactions that influence the expression and control of gene products. Sometimes the genes controlling the different traits are ge- BOX 3-1 Examples of Traits Targeted for Improvement • rchitecture—height, number of leaves, tillers, branches, leaf angle, number A of flowers and seeds, seed size, root structure, surface area. • Optimal planting density. • Flowering time and photoperiod responses. • rowth rates and regulation of hormones: brassinolide, auxins, gibberellins, G cytokinins, ethylene. • Growth responses to light quality and quantity. • hotosynthesis rates and overall carbon fixing during growing season, chlo- P roplast number and positioning, C3 vs. C4 metabolism, pathway regulation. • Heterosis (hybrid vigor) and male sterility for hybrid production. • Fertility, inbreeding and outbreeding. • itrogen and phosphorus uptake, use efficiency, translocation, storage, reduc- N tion, portioning between plant parts. • ater use efficiency: uptake, storage, transpiration rates, loss, tolerance of W chronic drought and transient drought. • Heat or cold shock and sustained tolerance to heat, cold, freezing. • Seed germination in cold. • Flooding tolerance. • Oxidative stress tolerance. • Heavy-metal and salt tolerance. • Biosynthesis of key metabolites. • Nutritional composition—seeds, roots, leaves, fruits, stems. • Digestibility (by humans and animals). • Root endosymbionts. • Resistance to viral, fungal, and bacterial pathogens. • Resistance to weeds and to herbicides that control them. • Resistance to insects and other pests and predators.

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Plant imProvement Protection  and netically linked and do not undergo recombination in meiosis. Failure to understand these associations leads to inefficiency in the breeding process and to poor crop performance. These relationships exist even when a new, transgenic trait is introduced into a plant genome, which emphasizes the need to continue improving germplasm even when transgenic solutions are available for some traits. It is beyond the scope of this report to describe a strategy for every trait that would be worth targeting. Examples of opportunities with potentially high returns are discussed throughout the chapter, which focuses on oppor- tunities to overcome some of the major problems that constrain agricultural productivity in sub-Saharan Africa (SSA) and South Asia (SA). Essential Features of Breeding Programs Because the success of every trait modification project depends on the competence of breeding programs, it is worth drawing attention to the quality of the breeding process itself. In particular, two essential features of modern breeding programs should be emphasized. First, successful crop improvement is based on a foundation of knowledge that informs all the intellectual and physical efforts of plant breeders in the laboratory and in the field. The different types of information needed are likely to be gener- ated by a variety of sources, so the task of plant breeders is to draw the information together as the basis of a breeding strategy. With relevant information, breeders can consider options for genetic and operational tactics to resist disease, weed, and pest damage; to enhance yield traits; and to begin a science-based, comprehensive breeding program to generate candidate germplasm. Among the types of knowledge important to plant breeders are the following: • An understanding of the appropriate crop for breeding and its fundamental genetics. This knowledge comes from extensive analysis of the needs of specific human societies (including farmers and consumers) and of the relevant production constraints on a crop that have the potential to be genetically manipulated. • An understanding of the markets for and uses of crops and the types of improvements that can add value to the crops. • Knowledge of the genetic and phenotypic diversity in the available crop germplasm (enhanced by similar information on other crops). • Knowledge of the biology of relevant pests, weeds, diseases, and stresses that routinely limit yield in the crop. • Knowledge about the specific processes that result in yield loss in farmers’ fields.

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emerging technologies benefit farmers 4 to The second feature of a successful breeding program involves under- standing that in evaluating germplasm, trials and selections take place in environments similar to those in which the crop will be grown. Therefore, crop yield trials in these regions are essential, requiring trained local man- power. The international agricultural research centers of the Consultative Group on International Agricultural Research have endeavored to establish consortia with national programs to achieve this testing, but an expansion of the effort is needed. Trials can be carried out under favorable conditions to estimate yield potential, but such conditions are not usually encountered area-wide. Additional realistic trials need to be conducted to select toler- ance traits relevant to the major constraints under conditions encountered by small-scale farmers. Similarly, a fundamental tenet of plant breeding is the ability to assay the trait in question. For example, during breeding and selection, plants have to be subjected to the most common strains of pests, weeds, and diseases that will challenge them in the farmer’s field. That is not a simple task, because given that pests, weeds, and diseases are not prevalent every year, breeding and selection processes need to be coupled to tests for tol- erance and sensitivity to the specific strains of indigenous or potentially indigenous pests, weeds, and diseases. Local and emerging diseases need to be precisely identified for each crop; the involvement of local farmers in the selections and tests could increase the likelihood that the final products will be adopted, and additional local knowledge can be incorporated into the selection processes. The establishment and scale-up of modern plant breeding programs in SSA and SA should have high priority in any organization looking to improve agricultural productivity. Plant breeding is rapidly evolving as an integrative technology supported by increasingly powerful molecular tools. Most of the expertise and knowledge needed to carry out this work is already available somewhere in the world. The message to the interna- tional development community is that crop improvement ultimately needs to be understood as a local and regional effort that is assisted by tools and knowledge developed by a broader community. EXISTING TOOLS FOR CONVENTIONAL PLANT IMPROVEMENT Annotated Sequences of Crop and Model Species for Comparative Genomics Some of the knowledge that plant breeders need to improve crops in SSA and SA already exists or is rapidly being generated. The sequences of the genomes of corn, sorghum, rice, and poplar have been or soon will be published. The cassava genome is currently being sequenced by the U.S. Department of Energy Joint Genome Institute. The genomes of tomato,

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Plant imProvement Protection  and the legume Medicago truncatula (barrel clover), and many other species are in line to be started or completed, although more attention to impor- tant legumes such as the common bean, cowpea, and pigeon pea, as well as other crops important to the poor such as species of Musa (e.g., banana and plantain) would certainly be welcomed. Nevertheless, the complete sequences of several genotypes of many additional crops will be known in 5 years; nearly every gene will be identified, variants for many important genes found, and the most relevant genes’ associations with traits estab- lished. The patterns of expression of co-regulated genes will become linked to phenotypes (the expression of the collection of genes that make up a trait in a given environment). Easily scorable genetic markers for every small chromosomal segment of much of the relevant germplasm will be known, and determinations of which chromosomal variants to select for in different environments will begin to emerge. All that will usher in a new platform for genomics-based breeding in which the needed genomes exist in the crop or in interbreeding relatives. Transgenic technologies will be needed to transfer the genes from other species where that is not the case. Two plants in particular are important models of the major species grown in SSA and SA. One is Arabidopsis, the most-studied reference plant; over the last 20 years, a detailed understanding of the molecular, biochemical, and cellular basis of pathways and circuits in Arabidopsis has been developed, and it will remain the leading source of knowledge on the biological systems of plant traits in the coming decade. The other is rice, the model plant of the grass species, including maize, wheat, pearl millet, sorghum, and others. Progress in understanding the biology of rice traits will be slower than in that of Arabidopsis, but it will be more directly rel- evant to cereal crops in the developing world. Research tools and genetic stocks available to address the fundamental questions concerning potential constraints on rice yield are rapidly increasing and are being used by a growing consortium of scientists around the world. Moreover, because of their common ancestry, the grasses have retained the same general order of genes along chromosomal segments (synteny), so mapping of genes on chromosomes of one species can be helped enormously by knowledge of a reference genome, such as that of rice or maize (Bennetzen and Ma, 2003). Diversity in gene order sometimes exists between these genomes over short distances, but this does not eliminate the value of synteny in aiding com- parisons between crop genomes. It also helps in finding truly orthologous (similar) genes between species. DNA Markers DNA markers—sequences of DNA shown to be associated with par- ticular genes or traits—have great potential to assist plant breeders (Jena et al., 2006; Steele et al., 2006), but for various reasons they have been

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emerging technologies benefit farmers  to underused in breeding programs. The use of qualitative phenotypic infor- mation with markers to determine the optimal crosses and offspring can shorten the cycle of crop improvement from 5 to 2 years (Jannink et al., 2001; Arbelbide and Bernardo, 2006). Methods for assaying genetic vari- ants are readily available and improving each year. When the contribution of a variant gene to a trait is known, the variant can be used as a marker of the trait. A candidate plant for breeding can be identified by the pres- ence of a marker in its genome without the need to test it for its phenotypic expression. That can help in choosing diverse parents for specific traits; in reducing the number of breeding generations by making it possible to select homozygotes more efficiently; in accelerating backcrossing of a trait to an elite parent, especially when the desired trait is recessive; and in selecting desirable progeny while rejecting poorer genotypes without the need for complex assays, such as assays of tolerance to diseases. The use of molecular markers has highlighted the importance of genes from wild relatives for crop improvement (Tanksley and McCouch, 1997; Koornneef et al., 2004). As evidenced by recent work on tomato, the results of introgressing ancestral genes can sometimes be spectacular (Frydman et al., 2004). Another example of the richness that diversity can provide is New Rice for Africa, NERICA. African farmers are showing enthusiasm for these new inter-specific hybrids that combine the best of Asian and African rices (Jones et al., 1997). Better knowledge of the genetic diversity of indig- enous tree species, particularly those of central Africa, could be applied to forest improvement (Juma and Serageldin, 2007). Genetic markers that link DNA sequences to traits are increasingly available in rice, maize, cassava, cowpea, wheat, and sorghum, and these crops are becoming better understood genetically (Buckler and Thornberry, 2002; McCouch et al., 2002; Somers et al., 2004; Duputie et al., 2007; Huang and Wu, 2007; Timko, 2007). Box 3-2 provides one example of the value of such markers. In general, however, tropical forage plants have received little attention from molecular and conventional plant breeders with a few notable excep- tions: alfalfa (which is grown in some tropical highlands), Brachiaria spp., Pennisetum purpureum (elephant or napier grass), and Panicum maximum (Guinea, colonial, or Tanganyika grass) have been studied (Jank et al., 2005). Characterization of forage traits that need improvement and studies of genetic markers for those traits have just begun, and temperate forage still receives far more attention than that grown in the tropics (Spangenberg et al., 2005; Smith et al., 2007). The burgeoning interest in biofuels, includ- ing use of switchgrass, should complement and accelerate our understand- ing of processes related to those occurring in forage digestion by ruminants. However, the collections of germplasm of tropical forage are poorly funded, and loss of current accessions (separate populations) is a distinct threat.

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Plant imProvement Protection  and BOX 3-2 Molecular Breeding and Transgenic Approaches Can Be Combined to Offer New Approaches to Crop Improvement A recent publication offers a striking example of how use of the tools of molec- ular breeding can be coupled with transgenic technologies for crop improvement. Using knowledge gained from extensive breeding efforts that had identified a number of quantitative trait loci (QTLs) in rice that related to number of grains per panicle, plant height, and heading date, Xue et al. (2008) used map-based cloning to identify the gene underlying one such major QTL. The gene was identified as a CCT domain protein that plays a key role in regulating photoperiod-controlled flowering and may also control a number of other functions in growth and dif- ferentiation. The superior allele for the gene identified by this technique was then inserted and overexpressed in a recipient rice cultivar, leading to dramatic altera- tion in yield potential, plant height, and heading date. This information can now allow breeders to introgress this trait into other locally adapted rice cultivars. Mutation Breeding and Mutant Analysis TILLING (targeting induced local lesions in genomes) is a method whereby natural or induced mutations in known genes are created in large populations of plants and the populations are screened for the mutation with sensitive molecular biology methods (Henikoff et al., 2004). When plants with a mutation in a selected gene are found, their phenotype can be studied in detail, and relationships between the gene and a trait can be assessed. Most mutations are not beneficial, but if mutating a gene leads to a specific phenotype, its relationship to a trait can be inferred. In the rare cases in which a mutation is beneficial, the approach can be used to identify useful mutant alleles that can be introduced into a crop plant by conventional breeding (see Box 3-3); this constitutes a nontransgenic method for altering deleterious traits or modifying biochemical pathways. Many approaches to mutant analysis and control of gene expression have been used in Arabidopsis and rice. Making mutant analysis relevant to crops in SSA and SA will require high-throughput assessment of the phe- notypic consequences of overexpression, underexpression, or mutation of candidate genes in the crops as identified in functional genomics studies of Arabidopsis and rice.

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emerging technologies benefit farmers  to BOX 3-3 Nontransgenic Herbicide Resistance in Maize for Striga Control Breeding for Striga resistance has been somewhat successful in sorghum, a plant that is native to Africa with different strains and wild relatives whose germ- plasm carries modicums of resistance to Striga (Ejeta, 2005; Ejeta and Gressel, 2007). If and when such genes are isolated, they might be transgenically trans- ferred to other crops such as maize. Recently, a non-transgenic approach has been developed for maize that is showing good promise in the fields of Western Kenya. Unlike sorghum, maize did not co-evolve with Striga and is expected to have fewer genes for resistance, and all breeding efforts (of which there have been many over 3 decades) have given rise to lines that at best work in certain locales but not others. At present, the only technology that seems to work over large areas is mutant-based resistance to systemic herbicides, which has been back-crossed into local elite germplasm (Kanampiu et al., 2003). The herbicide is applied to the seed and requires far less chemical (one-tenth) than is typi- cally sprayed, and this does not require spray equipment. Because the herbicide remains in the maize root zone, legumes can be interplanted and not affected (Kanampiu et al., 2003). This technology is also appropriate for other crops af- fected by Striga. Three groups are generating mutant sorghums resistant to the same groups of herbicides. With the mutant sorghums there is the inevitability that the resistance gene will flow to major sorghum weeds, namely shattercane and Sorghum halepense (Ejeta, 2005). This will not give an advantage to those weeds as long as only seed treatments of herbicide are used and the seed is certified to be weed-free. EXISTING AND EVOLVING TOOLS FOR CONVENTIONAL AND TRANSGENIC APPROACHES TO PLANT IMPROVEMENT Studies of the commercialization of discoveries in many disciplines often reveal that 2 decades pass before consumers see the results from discoveries translated into products. In plant innovation, the timescales are often especially long because the long generation times of plants and the requirement to test an innovation in multiple versions of a plant in multiple environments add years to the process. In addition, public-sector labora- tories responsible for plant breeding in SSA and SA rarely have the means to adopt new technologies rapidly and on a sufficient scale to achieve the high impact that is possible. Using the pace of a multinational plant breeding company as a bench- mark, obtaining a research finding and testing it in a model plant might

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Plant imProvement Protection  and require 5 years, and deploying and optimizing a trait in elite germplasm for SSA and SA another 5 to 10 years. Production, testing, and distribution of a crop for consumers could then take another 5 to 10 years, especially if the crop is transgenic and therefore has a longer regulatory testing phase under current regulatory regimes. The development of such transgenic technolo- gies would need to be done in conjunction with the development of crops that are appropriate for SSA and SA. This section highlights frontier, paradigm-changing technologies that show promise for agriculture but need further development. Creative, world-class research will be needed to move them into practice if they are to be incorporated into plant breeding programs and production agriculture. And the technologies will require education and training for users, from the breeder to the farmer and consumer. Technologies for Rapid Sequencing and Annotation of Crops of Sub-Saharan Africa and South Asia The most fundamental tool in modern plant breeding is a complete and annotated genome sequence of a crop of interest coupled with the ability to probe the DNA of selected germplasm to look for favorable gene combina- tions. Because that tool does not exist for many of the crops of importance to farmers in SSA and SA, the sequencing of the genomes of these crops is identified as an emerging and essential tool for plant improvement. For example, temperate maize (or corn), the focus of U.S. studies, is different from tropical maize. How? And what genes are involved in the dif- ferences? U.S. and European crop improvement programs in both the public and the private sectors tend to target temperate crops, so understanding how many genes control the temperate vs. tropical phenotype would seem to have value in connecting the “northern” efforts with the “southern” and in looking at the effects of global warming on agriculture (for example, for maize, see CIMMYT, 2007). High-quality reference sequences and genome annotations of all the relevant major crops in SSA and SA can be built on the sequences and annotations of rice and sorghum already available, the emerging sequence of maize, and the reference sequence of Arabidopsis. Breeders in SSA and SA also need resequencing capacity to complement their efforts in assess- ing and understanding the genetic diversity in the available germplasm of these major crops. Much of the sequencing work could be accomplished wherever there are adequate facilities and staff. A number of radically new sequencing technologies have become com- mercially available within the last few years and have resulted in a dramatic increase in the speed of DNA sequencing and a decrease in the cost. State- of-the-art machines now generate up to 500 million bases per day. At least

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emerging technologies benefit farmers 0 to six companies are in a race to deliver “a complete human genome sequence for $1,000.” The agriculture sector has an opportunity to capitalize on this race. Gaining help from world-class sequencing centers that are likely to test and purchase machines is essential for securing early opportunities for application to the germplasm of SSA and SA. Large efforts are also being made in developed countries to obtain the sequences of major insect pests, pathogens, and weeds. These are neces- sary for determining weak points that might be targeted and determining whether to try to find new insecticides, fungicides, and herbicides or to try to use RNA interference (RNAi) or other technologies for control. Such in- formation is not being garnered for SSA-specific and SA-specific constraints, so these areas are at a disadvantage. Information Technology and Computational Biology One of the single most important activities for improving breeding ef- forts across SSA and SA will be in unifying available information, especially from national programs. This will involve data curation, germplasm geno- typing, and breeding value estimates based on markers. Crop varieties will need to be evaluated in tens to hundreds of locations to make rapid progress so that a wide range of environmental fluctuations are experienced in a single year. When DNA is sequenced quickly and at low cost, it probably will no longer be a bottleneck in plant science and breeding. However, man- aging all the data generated on each crop to create the reference genome sequences and to define genetic diversity with a high degree of accuracy will require substantial attention from researchers in the biological sciences and information technology (IT). There is tremendous opportunity to apply 21st century bioinformatics —which merges techniques from applied mathematics, informatics, sta- tistics, computer science, artificial intelligence, chemistry, and biochem- istry—for effective plant breeding. In many regards, breeding efforts in developing countries are not unified and trials are not well replicated, and much of the agricultural efforts are similar to in situ breeding efforts of the late-19th and early-20th centuries in the United States that provided almost no yield increase for maize. Therefore the potential to leapfrog and breed more effectively is great if researchers in SSA and SA are able to implement some of these existing techniques for plants with user-friendly computer programs to access and use genomic information. IT and software innova- tions will be needed to enable the agriculturally oriented programs that can help breeders to profit from knowing the sequence and position of all the genes in the chromosomes of SSA and SA species. Accurate and easy an- notation of all the genes in a genome sequence is still beyond the ability of the scientific community. As soil, climate, weather, and remote sensing data

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Plant imProvement Protection  and and models continue to advance, these parameters combined with genomics and informatics could be especially helpful for adapting crops for specific environments. Computational biology and IT should be a special focus of an effort to bring the power of data acquisition to the practice of plant breeding and crop production. Technologies for Determining Genetic Variation in Key Crops Plant improvement is based on and necessarily exploits genetic varia- tion. Thus, being able to characterize the variation in every gene in the plants of a breeding nursery can bring the most powerful knowledge to the breeder. The breeder’s dream would be to know and understand the genetic diversity of equivalent chromosomal segments in the crop germplasm. Such knowledge would revolutionize the ability to pick parents successfully and select progeny more successfully. However, few breeders recognize the po- tential importance of that information and are content to focus on “good x good” crosses, ignoring the major benefits that might be hidden in other, less adapted germplasm. Equivalent chromosomal segments evolve independently in different populations but can be brought together in new combinations in breeding programs. It is desirable to know how many substantially different versions (haplotypes) of each chromosomal segment are present in the germplasm of a species and what the differences are. Answers to such questions are provided initially by the use of markers that measure sequence differences in chromosomal DNA (McCouch et al., 1997; Mohan et al., 1997; Bernado and Yu, 2007). The commercial technologies for using markers are advancing rapidly, to the point where tens of thousands of data points can be gathered in a day. The technologies for measuring polymorphisms are many and are evolving rapidly in synchrony with the DNA technologies described above because high-throughput sequencing technologies are excellent for revealing sequence differences. With efficient sequencing technologies, it is possible to reveal variants of the same gene or allele between hybrids or different acces- sions. It can be accomplished for thousands of genes at a time in genomic DNA, in libraries of complementary DNA (cDNA), or in selected regions of the genome. With high-throughput sequencing technologies, fragments of copies of messenger RNAs can be sequenced to reveal rarely expressed genes. When the fragments of genes are assembled, they can be aligned with genomic DNA sequences to define the correct gene structure. By sequencing copies of mRNAs from different accessions, one can identify single nucleo- tide polymorphisms (SNPs) between allelic genes and use them as markers. That is now the fastest way to obtain polymorphic markers (Barbazuk et al., 2007; Emrich et al., 2007), and crops in SSA and SA could be brought

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