Achievements of the National Plant Genome Initiative and New Horizons in Plant Biology (2008)

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1 Introduction PLANT SCIENCES: VITAL TO HUMAN HEALTH AND EXISTENCE Nearly all organisms on Earth, including humans, depend on plants for sur- vival. Plants, along with photosynthetic marine algae, are the primary converters of solar energy into the usable, stored forms of energy that power life on Earth. Thus, current and future breakthroughs in plant biology research can have profound con- sequences for the future of humanity and for the entire biosphere. The rationale for expanded investments in plant genome research is straightforward and urgent: Plant genomics provides a foundation for rapid, fundamental, and novel insights into the means by which plants grow and reproduce, produce organs and tissues essential to human nutrition and energy production, adapt to different and often difficult environments, and help stabilize ecosystems. Plant genomics is already beginning to enable a variety of new technologies that will revolutionize plant breeding and enhance responsible stewardship of the environment. The United States and the world face enormous challenges related to the production of food and energy, maintenance of environmental quality, and miti- gation of climate change. The maintenance of food quantity, quality, nutritional content, and delivery are persistent issues, as reflected in chronic food crises around the world. To resolve the environmental problems derived from the growing use of nonrenewable fossil fuels, renewable but practical and environmentally sustainable alternatives are necessary. Climate change will force adaptation in plant communities, which will result 11 

12 Achievements of the N at i o na l P l a n t G e n o m e I n i t i at i v e in changes in plant distribution that are likely to have tremendous impact on human well being and ecosystem sustainability. Long-term records have indicated that the Earth’s atmosphere is warming at an unprecedented rate (Trenberth et al. 2007). The impacts of climate change will likely be highly variable in space and time, leading to difficult-to-predict outcomes in different parts of the world. How- ever, predicted effects include an increase in new outbreaks of pathogen and pest infestations, and an increased frequency of extreme climate events such as droughts, fires, and floods. These predicted effects could have severe impacts on agriculture and forestry (Easterling et al. 2007). Climate change as a result of asymmetries in CO2 emissions and carbon sequestration, and growing water shortages are likely to lead to dramatic changes in agricultural productivity and land use and availability (Reddy and Hodges 1999). By increasing knowledge of how plants cope with ex- treme stresses, plant genomics research can help scientists to more precisely breed or engineer plants that can thrive as climates change. Economically and energetically viable production of liquid fuels from plant biomass, in quantities that could contribute to a reversal in the world’s de- pendence on fossil fuels, will require increases in plant productivity and con- comitant advances in biomass-to-fuel conversion. Directed modification of plant productivity and the tailoring of lignocellulosic biomass for high rates of conver- sion to liquid fuels increasingly depends on plant genomics to describe, at high resolution, the pathways that control biomass production, structure, and chemistry (DOE 2006). Sustainable agriculture will require a reduction in fossil fuel-derived inputs and in agriculturally caused pollution (for example, runoff of excess nitrogen, phosphorus, potassium, and various pesticides) and soil degradation (for exam- ple, loss of soil carbon, and associated fertility and soil loss as a result of erosion). Meeting these goals will depend, in part, on technological advances suited to a wide variety of agricultural and ecological conditions around the world. Most crops in most years are harvested at yields that are not nearly as high as their corresponding record yields (Boyer 1982). Hence, optimal plant performance, which depends on the convergence of weather, water, and soil conditions and subsequent genome-en- coded physiological responses, is much higher than what is typically achieved. Plant genomics research can contribute to understanding the mechanisms that determine optimal plant performance by identifying natural mechanisms governing plant growth, development, and adaptation to weather and water stress, and by helping to catalogue the evolutionary diversity of agriculturally important genes. Basic plant genome research serves a wide diversity of agricultural and en- vironmental goals. Agricultural production in the United States can be broadly divided into three categories: large commodity crops (such as corn, soybean, wheat, sorghum, cotton, and forage species), specialty crops (including fruits, nuts, veg- 

Introduction 13 etables, and ornamental species), and forest trees. The traits of importance vary widely from emphasis on yield and on tolerance to stress in the commodities; to flavor, scent, and nutritional composition in the fruits and vegetables (Goff and Klee 2006); to color, form, shape, and pest tolerance in ornamentals; and to wood or fiber yield and quality in forest trees. All crops are produced across farms that use various economic models, ranging from large farms that use vertically integrated production and crop systems that focus on one or a few rotation species, to small acreage and diverse plantings in produce farms that sell directly to consumers through local farmers’ markets. All these farming models can be served by invest- ment in basic plant genome research. Plant genome science facilitates the otherwise difficult integrated study of complex, economically important traits. Plant biomass productivity, chemical composition, grain and fruit yield, adaptability to suboptimal environments, and defensive responses to pests are genetically conditioned traits. All of them derive from the integrated contributions of multiple genetic networks. The principle that plant performance traits have complex genetic determinants underlies most cur- rent strategies for plant improvement, which emphasize phenotypic evaluation of whole plants in realistic environments. The same principle also predicts that gains in plant productivity will be best achieved through tools for systematic analysis and genome characterization that are enabled by plant genome sciences. The fundamental goals of plant genome science are to understand plant growth, form, function, adaptation, diversity, and evolution. That knowledge is critical to sustained progress in plant improvement. Advances in basic plant biology not only help to direct breeding of current crops and traits of value, but also stimulate progress in new directions, such as domestication of new crops and generation of new types of crop products. Domestication of new crops is of special importance in the face of rapidly changing climates and global markets. Examples of how new plants and new uses for plants can arise include the emergence of soybean to become a dominant commodity from relative obscurity over the last 60 years, and the exploitation of kiwi fruit as a new specialty crop over the last few decades. The breeding of major commodity crops already is benefiting directly from plant genomics research. The four largest commodity crops—corn, soybean, sor- ghum, and wheat—have an annual farm gate value (defined as value of crops to the grower) of $75 billion (NASS 2007a,b). The output of those crops is processed into a wide range of food, feed, and industrial applications, cutting a broad swath across the U.S. economy. Plant genomics efforts to date have focused, to a large extent, on these crops, driving an expansion of basic knowledge and establishment of research platforms, as well as the application of DNA markers to increase the efficiency of public and private sector breeding (see Chapter 2). In industry, the application of 

14 Achievements of the N at i o na l P l a n t G e n o m e I n i t i at i v e DNA marker-assisted selection for pest resistance in soybeans has resulted in the cost-effective development of high-performing soybean cyst nematode-resistant cultivars (Calhill and Schmidt 2004). The specialty crops as a group are economically valuable and are used to gen- erate products with which the public is intimately familiar. Specialty crops, too, are poised to benefit from plant genomics research. Despite their limited acreage compared to the commodities, the total annual value of specialty crops is about $50 billion (ERS 2007). However, that value is highly segmented: For example, $10 billion of value is divided among 34 major types of vegetables (NASS 2007c). Research aimed at specialty crop improvement is confounded by the market seg- mentation; some crops receive relatively high levels of attention from public and private breeders, and others little or none. The paucity of basic plant genomic information and the cost of its application are current limiting factors to the improvement of nearly all specialty crops. Plant genomics research in the public sector and associated DNA sequence databases, and the rapid decline in costs of sequencing and genotyping technologies, are expected to have an impact on breed- ing of specialty crops in the near future. In many cases, research using one or another specialty crop is driven by important basic biological questions represented by that crop and the family of plants to which it belongs. As one example of many, the Solanaceae include closely related plants such as potato, tomato, eggplant, and many others domesticated for human use. That plant family is morphologically and physiological diverse and is thus a model to study the evolution of plant form and function. In addition, in- creasing consumer interest in locally produced and fresh market produce suggest that further investment in understanding their biology, physiology, diversity, and breeding is worthwhile. Forest trees are America’s largest renewable resource and are well poised to benefit from plant genomics research. With over 32 million acres, the United States leads the world in area of planted forests (AFPA 2007). The United States is the world’s leading producer, consumer, and exporter of pulp and paper products. The annual value of wood used in manufacturing in 2002 was $20 to 30 billion (D. Adams, Oregon State University, personal communication, September 28, 2007). The industry is also reliant on renewable sources of energy; the pulp and paper industry supplies more then half of its energy needs, primarily through co-genera- tion with its waste materials (DOE 2005a). Forest tree improvement is still a primi- tive discipline relative to breeding of the major crops. The issue is compounded by trees’ long generation times, intolerance of inbreeding, high cost of vegetative propagation, large genome size, and recalcitrance to transformation. However, strong programs of cooperative tree breeding and genomics research are enabling the use of plant genomics information in forestry improvement, particularly for coniferous trees, such as the pines, and angiosperm species, such as poplar. 

Introduction 15 A central challenge for plant genome science is to understand how plants work at different levels of organization. This requires understanding how cells and organs make up an individual plant, and how that individual plant functions as a member of a community with other plants and microorganisms, all considered in ecological contexts that range from crop monocultures to highly diverse rain forests, across wide climatic ranges. Plant genome scientists seek to describe how plants grow from a fertilized egg and a small group of cells to a whole plant, shrub, or tree, as well as how they convert CO2 and light into sugar and its derived prod- ucts of economic value, including starch, protein, fiber, oil, and wood. Scientists also seek to define the evolutionary mechanisms by which species have adapted to the vast diversity of natural environments, producing an extraordinary diversity of forms. Their studies include how genetic variation within species allows them to mate, disperse, occupy wide geographic ranges, and persist over tens to hundreds of millions of years. The comparative power of plant genomics—whereby most of the genes, and the pathways they act in, can be rapidly compared between nearly any species—enables evolutionary lessons from model or wild species to directly inform plant improvement or genetic conservation efforts in crop species. Plant genome sciences and enabling technologies are in a state of rapid de- velopment, leading to many new discoveries and applications. The precision, ac- curacy, and speed of basic plant genome technologies (such as basic DNA sequenc- ing and gene expression analysis methods, and computational tools for analyzing and interpreting genomic data) continue to increase, and the costs of generating these data are dropping. These factors enable progress in the study of physiologi- cal mechanisms and organismal communities that were not previously tractable. The intensive use of plant models has led to dramatic progress in understanding of basic plant genomic biology. Twenty years after the adoption of Arabidopsis as a unifying model for plant biology—and the consequent birth of modern plant genomics research as embodied in the National Plant Genome Initiative (NPGI) and the National Science Foundation’s (NSF) independent Arabidopsis 2010 Proj- ect—plant scientists are leveraging genomics technologies to accelerate the pace of basic discovery. In turn, the application of plant genome sciences to important societal problems has begun, though application has been slowed by social contro- versies in cases where genetic transformation was the avenue for translation. THE NATIONAL PLANT GENOME INITIATIVE History The Interagency Working Group on Plant Genomes (IWG) was established in May 1997 by the Office of Science and Technology Policy (OSTP) under the direction of the National Science and Technology Council’s Committee on Science, 

16 Achievements of the N at i o na l P l a n t G e n o m e I n i t i at i v e in recognition of the unprecedented scientific opportunities that plant genome research offered at that time. That recognition was predicated on the observation that very little crop genomics was being pursued in the public sector, and that crop genomics was being performed almost exclusively in a small number of corpora- tions. Subsequent discussions between leading plant scientists, organized by the IWG, yielded a strong consensus that genomic tool development should be the highest priority for the early stages of NPGI, with a focus on the transitioning of model plant discoveries into crop species. The importance of basic research was driven home by the rapid success that had come from the choice of Arabidopsis as a model plant for study of the basic principles of plant growth and development. With Arabidopsis as a guide, it was clear that crop genomics could move quickly to real world applications. IWG members, which included representatives from NSF, U.S. Department of Agriculture (USDA), U.S. Department of Energy (DOE), National Institutes of Health (NIH), Office of Management and Budget (OMB), and OSTP, were charged to: “(1) identify science-based priorities for a plant genome initiative; and (2) de- termine the best strategy for a coordinated Federal approach to supporting such an initiative, based on respective agency missions and capabilities.” Subsequently, IWG developed a plan for a national plant genome initiative. The plan was approved by NSTC, and NPGI was officially established in 1998 as a coordinated national plant genome research project. In the nine-year history of NPGI, members of the IWG have worked together to coordinate all activities in plant genome research among agencies to leverage re- sources and expertise. Since 1998, the membership of IWG has grown and currently includes the U.S. Agency for International Development (USAID) and the U.S. For- est Service (USFS), in addition to NSF, USDA, DOE, NIH, OMB, and OSTP. Plant genome research activities that existed prior to the inception of NPGI contributed to or have become part of NPGI. For example, NSF, USDA, and DOE were engaged in a $4-million-a-year project to sequence the genome of Arabidopsis before the inception of NPGI and this was incorporated into the goals of NPGI in 1998. The USDA Agricultural Research Service had maintained the maize stock center at the University of Illinois for many years, which has since expanded its operation to accommodate the growth of stocks resulting from NPGI activities. During the 9 years of NGPI, and the nearly 20 years of focused and parallel investments in Arabidopsis research, U.S. plant science research has led the way internationally by any measure of productivity (see Appendix B). The total U.S. investment in competitive, peer-reviewed plant biology, including the flagship research programs, is less than $1 billion per year, roughly 30-fold less than com- parable totals from NIH for programs focused on human health (Somerville 2006). Furthermore, U.S. leadership has, to date, often driven parallel investments by the 

Introduction 17 European Union, Japan, China, Australia, and other entities worldwide, creating a unique and academically rewarding international collaborative environment. In part because of this success, it is safe to say that without substantial growth from current funding levels, plant science research in the United States will soon trail that in Asia and Europe, likely leading to concomitant loss of competitiveness for U.S. science, technology, and plant agriculture. Goals of NPGI Initial Goals in 1998 The initial goal of NPGI was to understand the structure and function of every gene in plants with a focus on the species that are important to agriculture, environment, energy, and health. As stated in the 1998 NPGI plan, “This increased emphasis on the plant genome will radically change fundamental plant science research and its application to agriculture, forestry, energy, and the environment, as well as to the production of pharmaceuticals and other plant-based industrial chemicals and materials” (NSTC 1998). The scientific objectives for reaching those goals can be divided into three components: • Genome structure—studies of the organization of genomes. • Functional genomics—studies that relate genome structure and organiza- tion to plant function at the cellular, organismal, or evolutionary level. • Application of the genomic information and knowledge for development of improved plants and novel plant-based products for human uses. The initial plan was to invest in the first two components, thereby to provide linkages to the third component. The plan recommended increased federal investment to • Accelerate the completion of the genome sequence of the model plant spe- cies Arabidopsis thaliana. • Participate in an international effort to sequence rice. • Develop the biological tools to study complex plant genomes such as corn, wheat, soybean, and cotton. • Increase the knowledge of gene structure and function of important plant processes. • Develop appropriate capabilities for handling and analyzing data. • Ensure the accessibility of new information to the broader community of plant biologists. • Maximize training opportunities that would arise from NPGI. 

18 Achievements of the N at i o na l P l a n t G e n o m e I n i t i at i v e Goals in the 2003–2008 Plan The objectives for 2003–2008 were to build on the scientific and technical ad- vances of the first five years to ensure continued advancement in plant genomics and plant sciences. Technology development, data management and accessibility, and training of new generations of scientists were recognized as important goals. The six objectives were (NSTC 2003) • Continued elucidation of genome structure and organization. • Functional genomics—understanding the biological role of genomic sequences. • Translational plant genomics—applications of genomic tools. • Bioinformatics in every plant scientists’ research toolbox. • Education, training, and outreach. • Consideration of broader impacts. STUDY CHARGE AND SCOPE NPGI will celebrate its 10th anniversary in 2008, and it is appropriate to assess what the initiative has achieved and to set goals for the future. IWG commissioned the National Research Council to convene a committee to assess the achievements of NPGI and recommend future research directions. The committee was charged to address the following: • Review the accomplishments of NPGI to date. • Assess the contribution of NPGI to science, research infrastructure, educa- tion of the next generation scientists, and international research collaboration. • Discuss the broad impacts of NPGI to fundamental advances in biological sciences. • Assess the contributions of NPGI to the application of scientific knowledge including technological innovation and economic competitiveness. • Recommend future research directions and objectives for NPGI. The committee was not to make budgetary recommendations. Because the committee was charged to assess the contributions of NPGI to science, research infrastructure, education of the next generation of scientists, and international research collaboration, the committee conducted an in-depth as- sessment of research projects funded directly by NPGI participating agencies. The committee’s assessment presented in Chapter 2 used three mechanisms. First, the committee analyzed the data provided by IWG on NPGI-funded projects. Second, the committee sent a questionnaire to all leading principal investigators of NPGI- 

Introduction 19 funded projects (n=277) to ask them about the career paths of their trainees; their self-described most important contributions, published or otherwise, from their NPGI projects; their interactions with industry; and a list of all their publications citing NPGI funding (see Appendix C for the questionnaire). Third, the committee hosted a public workshop and invited plant scientists from universities, government agencies, and industry to solicit their evaluation of the achievements of NPGI in the last nine years and to discuss possible future directions of the program (see Appendix D for workshop agenda). The scope of the study, however, was not limited to assessing only the funded research. The IWG has not only supported many activities and programs related to plant genomics over the last nine years, but also it has coordinated plant research among agencies. Research results from NPGI have been used to formulate mis- sion-focused programs in participating agencies, as detailed in Chapter 2. Some IWG agencies also have provided, and continue to provide, databases, genomic technologies, sequencing facilities, and other in-kind support for plant genome research that IWG considers part of NPGI. A direct assessment of those contribu- tions is difficult because there is not a clear definition of what endeavors are directly related to NPGI and which are ongoing within each IWG member agency that only peripherally support NPGI goals. The committee attempted to take those NPGI-related activities into consider- ation, assessed whether NPGI has been achieving its goals, and recommends here future directions required to increase the impact of plant genome science research in the United States and around the world. In Chapter 3, the committee makes nine recommendations for NPGI on the basis of the contemporary societal issues facing the nation at present, the progress that NPGI has made to date and the areas that could be improved, and how NPGI could best achieve its goals.