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

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Summary Humans have used plants as major sources of food, fiber, energy, and animal feed for millennia. The organized harnessing of plant products through domestica- tion was a key step in the ascendance of human civilization. Subsequent modern plant breeding has led to greatly enhanced productivity and incorporation of new, desirable traits into a wide variety of plants used by humans for diverse applica- tions. Despite the long history of human-plant interactions, investment in plant biology research has never been as important as it is today, as a growing global human population increases the demand on plant production in the face of de- creased fresh water supplies and societal pressures to maintain the quality of arable and “natural” land. The need to enhance plant production will be exacerbated by extreme weather patterns as a result of global climate change. Plant genome science facilitates the integrated study of complex, impor- tant traits with value to human society. Plant biomass productivity, chemical composition, grain and fruit yield, adaptability to suboptimal environments, and defensive responses to pests are genetically conditioned traits. All derive from the integrated contributions of multiple genetic networks. In fact, the principle that plant performance traits are the result of complex genetic determinants acting under various environmental influences underlies most current strategies for plant improvement. 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 National Plant Genome Initiative (NPGI) was initiated in 1998 in  

 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 BOX S-1 Charge to the Committee • Review the accomplishments of NPGI to date. • Assess the contribution of NPGI to science, research infrastructure, education of the next generation of 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. recognition that research in plant genomics provides a foundation for rapid, fundamental, and novel insights into the means by which plants grow and re- produce, produce organs and tissues essential to human nutrition and energy production, adapt to different and sometimes stressful environments, and help stabilize ecosystems. As NPGI approaches its 10th anniversary, the Interagency Working Group on Plant Genomes (IWG) asked the National Research Council (NRC) to convene a committee to assess the achievements of NPGI and recom- mend future research directions (Box S-1). To address the statement of task, the committee gathered information from IWG, from principal investigators who received research grants from NPGI, and from plant scientists from universities, government agencies, and industry through a workshop to solicit their evaluation of the achievements of NPGI in the last nine years and to discuss possible future directions of the program. The assessment of NPGI comes at a vital period in the history of federally sup- ported scientific research. Budgets are more or less flat or, in some cases, declining. Yet the needs for revolutionary breakthroughs and technological advancement are acute and international competition is increasing, so that a new vision for plant genome sciences over both the short and long term is necessary. 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, in recognition of the unprecedented scientific oppor- tunities that plant genome research offered at that time. IWG membership currently includes the National Science Foundation, U.S. Department of Agriculture, U.S. Department of Energy, National Institutes of Health, U.S. Agency for International Development, U.S. Forest Service, Office of Man- agement and Budget, and OSTP. 

Summary  ASSESSMENT NPGI has been very successful by all measures applied in this study. NPGI has contributed to revolutionary breakthroughs in genome sequencing of plants, including the genomes of Arabidopsis, rice, and, soon, maize and a variety of these plants’ pests and pathogens. Genome sequence, however, is only the first step to- ward understanding integrated gene function. NPGI has supported a wide range of investigations into gene regulatory mechanisms in model and crop plants and funded studies on natural variation and crop domestication to better understand complex traits. Furthermore, NPGI has enabled the development of more efficient DNA-based breeding tools to improve crop value and yield. The NPGI funding has also supported the development of artificial chromosome libraries for several crops and research to align these DNA sequences in their proper location along the normal chromosomes. Far more than just genomics, the technologies and in- formation developed by NPGI and by the parallel and complementary program Arabidopsis 2010 Project of the National Science Foundation (NSF) are the primary platforms for basic research in fundamental plant science—including genetics, biochemistry, physiology, developmental biology, evolutionary biology, and population biology. Plant genome scientists, as a community, have made excellent use of the synergies provided by exploitation of an easily manipulable model species, Ara- bidopsis, to elucidate basic biological principles that are likely to be broadly operative across plant biology and can thus facilitate rapid applications to crop genomics and improvement. In fact, it is difficult to list all the major break- throughs that the analyses of plant genomes and gene function have enabled in the last nine years across NPGI and the NSF Arabidopsis 2010 Project. These have been powered mostly by genetic advances in Arabidopsis, and have often been followed up by studies of similar genes and their related function in crop species. Among them are the discovery of receptors for nearly all of the major plant hormones; an increasingly detailed understanding of how these receptors control subsequent plant developmental programs; knowledge of how exposure to winter-like tem- perature, vernalization, and the correct photoperiod leads to flowering; how flow- ers, leaves, and roots are built; and how the plant “immune system” controls the interplay of the different lines of pathogen defense. Some of these breakthroughs are now being translated to practical applications in crop species. This synergism The NSF’s Arabidopsis 2010 Project is not part of the committee’s review, but it is unofficially in- tertwined with NPGI. The Arabidopsis 2010 Project focuses on using a rapid growing model species to understand many of the basic aspects of plant growth and development that provide conceptual touchstones across at least the flowering plants (NSF 2007a). 

 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 is the best rationale for further and separate development of both NPGI and the independently funded Arabidopsis 2010 Project. Additionally, the direct application of genomics to less tractable, but eco- nomically important, plant species and to less intensively studied ecological models is increasingly feasible, particularly as costs for many genomics tech- nologies decline. These genomic studies have led to recent breakthroughs in the understanding of the molecular events controlling the traits that were selected by humans during domestication of, for example, maize, rice, tomato, and wheat. Similarly, genomics is now being used to understand evolutionary processes in ecologically relevant settings and guide breeders toward new forms of crop adapta- tion to stressful environments. The significance of NPGI-funded research is reflected by the impact of the articles published by the principal investigators. The NPGI “literature footprint” is heavily weighted toward important, broadly applicable publications in the best scientific journals. About 21 percent of primary peer-reviewed research articles that cited NPGI support were published in journals with citation impact factor of 9 or above, and around 45 percent of them were published in journals with cita- tion impact factor of 6 or above; this is an excellent record. In addition, there have been many publications in crop breeding and agronomic journals, demonstrating transfer of technology to the applications sector. The publication record shows that NPGI research is not only a leading source of plant biology knowledge, but also a source of research that is broadly applicable to the wider biosciences community. Basic research funded by NPGI to date has served as the springboard for several applied, agency-specific, mission-oriented programs that capitalize on either new funding from the public or on public-private partnerships. Examples of programs that leverage basic plant genomics discoveries made though NPGI include the U.S. Department of Energy (DOE) Bioenergy Research Centers and the Plant Feedstocks Genomics Bioenergy Program run jointly by DOE and the U.S. Department of Agriculture (USDA) Cooperative State Research, Education and Extension Service (CSREES). The USDA Agricultural Research Service and CSREES have refocused or increased investment in their agency-specific programs as a result of NPGI discoveries. The committee interprets these agency-specific research programs in plants to be a function of both maturation of NPGI and a broadly accepted view that plant biology will contribute significantly to long-term energy solutions. NPGI principal investigators also reported diverse and substantive trans- lational activities. These activities range from starting their own companies on the basis of research results to patent filings and licensing arrangements with a variety of plant biotechnology entities. Hence, NPGI research is moving towards real world application and crop improvement. 

Summary  In addition to advancing basic science, NPGI has contributed to internation- al collaborative projects and to the training of a large number of students and postdoctoral fellows. These efforts have created a pool of employees for growing enterprises in all bioscience sectors in the United States and around the world. A number of NPGI-funded projects involve international partners, and these proj- ects leverage the resources, expertise, and facilities of many countries to achieve a richer and more comprehensive set of genome datasets than could be obtained by any single national effort. These collaborations can enhance the competitive ability of the United States to contribute to solutions to global challenges. For example, coordination among researchers from six groups across three continents in the Arabidopsis genome sequencing project paved the way for subsequent multinational endeavors, including the international consortium to sequence the rice genome. NPGI is a model for international scientific collaboration, and the ability of the United States to contribute to global challenges has been significantly enriched by these research programs. NPGI is not merely a funding mechanism, but it also is an interagency collaboration that coordinates activities in plant genomics. All of the member agencies contribute to the goals of NPGI by providing in-kind support, distribut- ing resources, and keeping each other abreast of the latest genomic technologies to ensure efficient use of resources. Other than the Arabidopsis 2010 Project and the USDA-CSREES National Research Initiative, there are few other funding sources in the United States that support the basic disciplines of plant science that are comparable to NPGI. The committee therefore takes it as axiomatic throughout this report that the crop-focused NPGI and the independently funded, rapid discovery Arabidopsis 2010 Project should continue in parallel. To miss the opportunity to capture and increase the momentum of the last 10 years would diffuse the tremendous gains made thus far, and sacrifice vital routes to tackle national and global problems that could be addressed with plant-based resources. RECOMMENDATIONS AND GOALS: NEW HORIZONS IN PLANT GENOMICS The committee’s major recommendations incorporate a significant broaden- ing of the NPGI mission to include the basic biology of economically relevant traits in models and crop species, deeper investigations into plant diversity and plant adaptation to various ecological niches, and continued expansion of translation to breeders and farmers. This broadening is justified by the wealth of knowledge to be gained from comparative genomic analyses within and across species, and by the need to understand how plants function to provide, in essence, 

 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 the conditions required for human survival. The diversity of plants, combined with hundreds of millions of years of natural selection, has resulted in evolution- ary “solutions” to problems of growth and survival across many radically different ecological conditions, and in the face of large variations in environmental stress. The conserved nature of genetic networks across species and the ability to transfer knowledge from one species to another via comparative genomics and subsequent marker-assisted breeding, and by direct genetic engineering in many cases, can lead to potential major innovations in crop improvement. The committee’s recommendations for an expanded NPGI will require re- search at scales ranging from single principal investigators, across collabora- tions of investigators at multiple institutions, to large dedicated data produc- tion centers, all of which will use experimental methods of inquiry that span the entire scale of plant biology. The scale ranges from atomic-level analysis of plant cell constituents to analyses of agronomic yield and plant organ or tissue composition, and from the study of individual cells to population-wide analyses of whole-plant phenotypes in field environments or natural ecological com- munities. Indeed, for effective translation of the insights from plant genomics to aid crop improvement, conservation, and ecological studies, considerable efforts need to be allocated to studying plant phenotypes and physiology in both realistic agricultural and natural environments. The astounding breadth of plant genomics will attract, motivate, and empower scientists across a wide spectrum of disciplines and should result in synergistic gains in knowledge and application. The committee focused its recommendations on three different time horizons: The 5-year goals represent immediate, pragmatic “next steps” in plant genome science, the 10-year goals require significant development of new tools and re- sources to enable transformative solutions to real world problems, and the 20-year “achievements” reflect the committee’s desire to define some admittedly long- range, high-risk, high-reward areas that would significantly alter society’s ability to understand how plants work. The committee used the following guiding principles for the development of the recommendations across these time horizons: • NPGI research should encompass the most innovative, competitive, peer- reviewed basic science aimed at detailed and system-wide understanding of plant form, function, performance, and evolution in a strictly peer-reviewed, competitive environment. • Addressing core molecular, cellular, and developmental concepts of plant biology is most efficient and productive in highly developed model plant systems; research most easily done in these systems should receive high priority. • The diversity of plant form and function utilized by humans is very broad; hence parts of the overall genomics toolkit should be devoted to investigate spe- 

Summary  cific aspects of plant tissue and organ development, environmental adaptations, or biochemical processes that are not well represented in core model species. • Field-robust, high-resolution genotyping and phenotyping methods for use in studies of natural adaptations and in molecular-assisted plant breeding should be available across a broad swath of wild and cultivated plant species. • Priorities for NPGI and associated plant sciences should be framed towards addressing the large challenges facing humanity, including biobased energy, climate change, sustainability, food security, and human health and nutrition. The committee’s major recommendations are that NPGI should: 1. Expand plant genome sequencing, plant-associated microbial sequenc- ing, and plant-associated metagenome sequencing, and associated high quality annotation, by (a) using the Department of Energy’s Joint Genome Institute’s sequencing capacity to generally serve plant sciences and (b) empowering in- dividual principal investigators or collaborative groups to access and utilize next-generation sequencing technologies for a broad spectrum of genomics and metagenomics discovery. 2. Develop “omics” resources and toolkits at high resolution in a few, care- fully chosen plant species, including expansion and deeper investment in cur- rently leading model species. 3. Develop “omics” resources at a broader, shallower level across a number of additional species to (a) expand the phylogenetic scope of functional infer- ence, particularly when this is justified to test clearly specified hypotheses, (b) understand physiological and developmental processes to a depth that is not feasible in the model systems, and (c) provide the foundation to improve U.S. competitiveness of important crop and tree species. 4. Use systems-level approaches to understand plant growth and devel- opment in controlled and relevant environments, with the goal to create the iPlant, a large family of mathematical models that generate computable plants genuinely predictive of plant system behavior under a range of environmental conditions. 5. Increase the understanding of plant evolution, domestication, and per- formance in various ecological settings via investment in comparative genomics, and in the metagenomics of living communities of interacting organisms. 6. Enable translation of basic plant genomics towards sustainable deliver- ables in the field, and continue to use NPGI as a foundation for new, agency- specific, mission-oriented plant improvement programs. 7. Develop and deploy sustainable, adaptable, interoperable, accessible, and evolvable computational tools to support and enhance Recommendations 1–6. 

 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 8. Improve the recruitment of the best, broadly trained scientists into plant sciences. 9. Promote outreach on plant genomics and related issues that are critical to educating the American public on the value of genomics-based innovations. These recommendations are very well aligned with Federal Research and De- velopment Budget Priorities (http://www.ostp.gov/html/budget/2008/m06-17.pdf) as articulated by Office of Science and Technology Policy and the Office of Man- agement and Budget: Agencies should target investments toward the development of a deeper understanding of complex biological systems, which will require collaborations among physical, compu- tational, behavioral, social, and biological scientists and engineers who will, among other things, need to develop the data management tools and platforms necessary to facilitate this research. Access to new biotechnological tools and increasing amounts of genetic sequence data will open new avenues for research into the functional implications of gene expression. . . . Continued research at both the cellular/sub-cellular and the organism/community lev- els has the potential to have significant impact on national security and homeland security, health, environmental management, and education. CONCLUSION Plant genome sciences, and plant biology as a whole, are vital enterprises that contribute significantly to human health, energy security, and enlightened and careful environmental stewardship. Because photosynthetic organisms play a central role in all of the Earth’s major ecosystems, understanding how plants function, and how to modify and improve their ability to carry out specific physi- ological processes—the goals of plant genome research—are likely to have deep and far-reaching ultimate environmental impacts. NPGI demonstrates that the plant genome science research community is vibrant and capable of continued imaginative breakthroughs that will drive technological advancement. IWG should capitalize on the research capacity built and important knowledge gained via NPGI to date and expand the program so that the member organizations’ current and future agency-specific and mission-oriented programs will always be built on a strong foundation of fundamental plant biology research. Akin to President Kennedy’s call to land an astronaut on the moon, or President Nixon’s declaration of war on cancer, the time is now ripe for a major, national research effort toward sustainability in the production of food, fuel, and fiber in a societal climate that should demand responsible environmental stewardship. Our society’s overall response to these challenges will entail conservation, rapid 

Summary  and significant gains in fuel use efficiency, and the development of a distributed, diversified energy portfolio. Plants will provide a necessary part of the solutions to several of these issues. Plant genome science research can play a large part in this important revolution.