STRATEGIC PLANNING FOR THE FLORIDA CITRUS INDUSTRY

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STRATEGIC PLANNING FOR THE FLORIDA CITRUS INDUSTRY Addressing Citrus Greening Disease Committee on the Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease (Huanglongbing) Board on Agriculture and Natural Resources Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This study was supported by the Florida Department of Citrus Contract No. 07-27. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for the project. International Standard Book Number (ISBN)-13: 978-0-309-15207-5 International Standard Book Number (ISBN)-10: 0-309- 15207-0 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, N.W., Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. Cover: Photo credits: Asian citrus psyllid by David Hall; lopsided fruit; huanglongbing symptoms on leaves of a branch, and on citrus trees by Mike Irey. Copyright 2010 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Suggested Citation: National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON THE STRATEGIC PLANNING FOR THE FLORIDA CITRUS INDUSTRY: CITRUS GREENING DISEASE (HUANGLONGBING) GEORGE BRUENING, Chair, University of California, Davis (Emeritus) JOSEPH-MARIE BOVE, Université Victor Segalen Bordeaux 2, La Brède, France (Emeritus) PAUL CITRON, Medtronic, Inc., Minneapolis, Minnesota (Retired) PHILIP W. MILLER, Monsanto Company, St. Louis, Missouri LOWELL R. NAULT, The Ohio State University, Wooster (Emeritus) MARYLOU L. POLEK, California Citrus Research Board, Visalia HOWARD-YANA SHAPIRO, Mars Inc., McLean, Virginia ANTHONY M. SHELTON, Cornell University, Geneva, New York LAVERN W. "PETE" TIMMER, University of Florida, Lake Alfred (Emeritus) JAMES H. TUMLINSON, III, The Pennsylvania State University, University Park RAYMOND K. YOKOMI, USDA Agricultural Research Service, Parlier, California Project Staff CAMILLA Y. ABLES, Study Director KAMWETI MUTU, Research Associate KAREN L. IMHOF, Administrative Assistant ERIN MULCAHY, Senior Program Assistant v

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BOARD ON AGRICULTURE AND NATURAL RESOURCES NORMAN R. SCOTT, Chair, Cornell University, Ithaca, New York PEGGY F. BARLETT, Emory University, Atlanta, Georgia ROGER N. BEACHY, Donald Danforth Plant Science Center, St. Louis, Missouri HAROLD L. BERGMANN, University of Wyoming, Laramie RICHARD A. DIXON, Samuel Roberts Noble Foundation, Ardmore, Oklahoma DANIEL M. DOOLEY, University of California, Oakland JOAN H. EISEMANN, North Carolina State University, Raleigh GARY F. HARTNELL, Monsanto Company, St. Louis, Missouri GENE HUGOSON, Minnesota Department of Agriculture, St. Paul KIRK C. KLASING, University of California, Davis VICTOR L. LECHTENBERG, Purdue University, West Lafayette, Indiana PHILIP E. NELSON, Purdue University, West Lafayette, Indiana ROBERT PAARLBERG, Wellesley College, Watertown, Massachusetts KEITH PITTS, Marrone Bio Innovations, Davis, California CHARLES W. RICE, Kansas State University, Manhattan HAL SALWASSER, Oregon State University, Corvallis PEDRO A. SANCHEZ, The Earth Institute, Columbia University, Palisades, New York ROGER A. SEDJO, Resources for the Future, Washington, DC KATHLEEN SEGERSON, University of Connecticut, Storrs MERCEDES VAZQUEZ‐AÑON, Novus International, Inc., St. Charles, Missouri Project Staff ROBIN A. SCHOEN, Director KAREN L. IMHOF, Administrative Assistant AUSTIN J. LEWIS, Senior Program Officer EVONNE P.Y. TANG, Senior Program Officer PEGGY TSAI, Program Officer CAMILLA YANDOC ABLES, Associate Program Officer KARA N. LANEY, Associate Program Officer RUTH S. ARIETI, Research Associate JANET M. MULLIGAN, Research Associate KAMWETI MUTU, Research Associate ERIN P. MULCAHY, Senior Program Assistant vi

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Acknowledgments The authoring committee is grateful to the staff at the National Research Council, particularly Dr. Camilla Y. Ables and Robin A. Schoen, for assembling information from many diverse sources, preparing tables, figures and appendixes, supervising the report preparation process, handling numerous communications, checking documents and facts, and providing their advice on many issues. We had the benefit of input from a Liaison Committee, the members of which appear in Appendix C, as well as written and verbal presentations from many experts, who are listed in Appendix D. The committee drew on numerous sources in addition to conventional publications, including websites, newsletters, and personal communications. We have attempted to identify these sources in Appendix I but regret that we may have failed to identify each and every source. This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the NRC’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of this report: Harold W. Browning, University of Florida, Lake Alfred (Retired) Steven A. Slack, Ohio Agricultural Research and Development Center, Wooster Joseph G. Morse, University of California, Riverside Michael S. Irey, United States Sugar Corporation, Clewiston, Florida T. Erik Mirkov, Texas A&M University, Weslaco Mikeal L. Roose, University of California, Riverside Stephen M. Garnsey, Fallbrook, California Gail C. Wisler, U. S. Department of Agriculture, Beltsville, Maryland Steven J. Castle, U. S. Department of Agriculture, Maricopa, Arizona Saskia Hogenhout, John Innes Centre, Norwich, United Kingdom Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations nor did they see the final draft of the report before its release. The review of this report was overseen by Elaine A Backus, U. S. Department of Agriculture. Appointed by the National Research Council she was responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were vii

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viii ACKNOWLEDGMENTS carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution.

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Contents SUMMARY, 1 1 INTRODUCTION, 13 Background, 13 Purpose and Scope of the Study and the Formation of the Committee, 14 Charge to the Committee, 14 Committee’s Approach to the Study, 15 Organization of the Report, 15 2 CHALLENGES TO CITRUS PRODUCTION, 17 Economic Importance of Citrus: Worldwide, United States, Florida, 17 History and Evolution of the Citrus Industry in Florida, 18 Ecology, Climate, Water and Florida Citrus, 23 Diseases and Pests that Threaten Citrus Production, 27 Review and Assessment of Current Huanglongbing Management Strategies in Florida, 49 Significant Citrus Diseases and Insect Pests Other than Huanglongbing, 55 Economics of Citrus Production in the Presence of Huanglongbing, 55 Federal, State, and Local Regulatory Agencies and Industry Organizations and Their Impact on the Citrus Industry, 59 Relationships of Federal, State, and Industry Entities in Florida and How They Address Citrus Diseases, 60 3 CITRUS GREENING RESEARCH AND DEVELOPMENT AND INDUSTRY PREPAREDNESS, 67 Clas Genomics and Culture, 67 Research Supporting Current Huanglongbing Mitigation Practice: Removing Huanglongbing-Affected Trees, 69 Research Supporting Current Huanglongbing Mitigation Practice: Reducing Asian Citrus Psyllid Access to Citrus, 72 ix

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CONTENTS x Huanglongbing Epidemiology and Asian Citrus Psyllid Behavioral Ecology, 76 Research on Citrus Breeding and Genetics, 78 Transgenes for Resistance to Clas, 82 Transgenic and Viral and Bacterial DNA Vectors for Mediating Gene Expression in Citrus, 82 Citrus Cultural Practices Modified to Accommodate Endemic Huanglongbing, 86 Model Systems and Chemical Screening, 87 Summaries of Experiences with Other Major Plant Diseases, 87 An Overview of Resources for Citrus Pest Management Projects, 87 Recent History of Industry Funding in Florida, 89 Florida Citrus Advanced Technology Program, 89 Research Communication and Information Exchange, 91 4 RECOMMENDATIONS ON ORGANIZATIONAL CHANGES, TECHNOLOGY DEVELOPMENT, AND SYSTEMS APPROACHES FOR MINIMIZING THE IMPACTS OF HUANGLONGBING AND OTHER DISEASES AND PESTS IN FLORIDA CITRUS, 93 Recommendations for Organizational Changes, 94 Informational Initiatives: Communicating to the Public and Public Officials the Seriousness of Huanglongbing and Other Threats to Florida Citrus Production and the Countermeasures That May Be Needed, 98 Recommendations for Research and Technology with the Potential to Advance Huanglongbing Mitigation in the Near-Term or Near-to-Intermediate-Term, 99 Recommendations for Research and Technology with the Potential to Advance Huanglongbing Mitigation in the Long-Term, 120 5 STRATEGIES FOR IMPLEMENTING PLANS FOR MITIGATION OF HUANGLONGBING AND OTHER PROBLEMS IN CITRUS PRODUCTION, 127 Implementing Plans for Huanglongbing Mitigation, 127 Accelerating Product Development and Commercialization: Grants Vs. Contract Prizes and Alternatives, 130 Intellectual Property Management with the Aim of Stimulating Deployment of Huanglongbing Technology, 134 Consequences and Backup Plans Should Huanglongbing Countermeasures Prove to Be Insufficiently Effective, 139 Recommended Measures for the Control of Non-Huanglongbing Diseases and Pest Problems, 140 Metrics for Progress, 142 GLOSSARY, 143 REFERENCES, 147

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CONTENTS xi APPENDIXES, 183 A Committee Statement of Task, 185 B Committee Biographies, 187 C Liaison Committee on Strategic Planning for the Florida Citrus Industry: Citrus Greening Disease, 193 D Oral Presentations and Written Statements Submitted to the Committee, 195 E Significant Citrus Diseases Other Than Huanglongbing, 199 F Significant Citrus Insect and Mite Pests, 203 G Missions of University, Government, and Non-government Agencies with Responsibilities Related to Citrus Production and Marketing, 207 H Citrus Bacterial Canker: Outbreaks and Regulatory Response, 213 I Detection of Asian Citrus Psyllid and Huanglongbing in Florida and Major Events and Activities That Occurred in Response to Their Detection (June 1998–August 2009), 217 J Funded Projects on Citrus Greening (2008–2010), 235 K Huanglongbing Research Milestones (1956–2009), 271 L Witches’ Broom Disease Outbreak in Brazil and Control Attempts: Success and Failure in Bahia, Brazil (1989–2009), 305 M Vector-borne Maize Pathogens: Lessons Learned, 307

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Tables, Figures, and Boxes TABLES Table 2-1 Impact of 2004-2005 Hurricanes on Florida Citrus Crop Yield (Number of Boxes), 20 Table 2-2 Bacterial Agents Associated with Huanglongbing, 32 Table 2-3 Geographical Distribution of Huanglongbing-associated Liberibacters and their Insect Vectors, 42 Table 2-4 Government, University and Non-Government Agencies with Responsibilities Related to Citrus Production and Marketing, 61 Table 3-1 Major Citrus Species that have been Genetically Transformed to Produce Citrus Plants with Genes of Agronomic Interest, 80 Table 4-1 Recommended Changes in Organizations Connected to Citrus Production, 94 Table 4-2 Recommended Informational Initiatives, 98 Table 4-3 Near- and Near-to-Intermediate-Term Recommendations, 100 Table 4-4 Long-Term Recommendations, 120 Table 5-1 External Research Vehicle Characteristics, 131 FIGURES Figure 2-1 Worldwide orange production; percent total production, 2005–2007, 18 Figure 2-2 Path of hurricanes Charley (August 13, 2004), Frances (September 5, 2004), Jeanne (September 26, 2004), and Wilma (October 24, 2005), 20 Figure 2-3 Florida citrus production in tons and dollar value, 21 Figure 2-4 Acreage of existing commercial and bearing citrus groves, 22 Figure 2-5 Distribution of huanglongbing in Florida from October 2005 to October 2009, 23 Figure 2-6 Citrus production areas in Florida, 25 Figure 2-7 Asian citrus psyllid life cycle, 35 xiii

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xiv TABLES, FIGURES, AND BOXES Figure 2-8 Huanglongbing symptoms on citrus tree and leaves on a branch, 38 Figure 2-9 Huanglongbing symptoms on citrus leaves and fruit, 40 Figure 2-10 World distribution of Candidatus Liberibacter spp. and their insect vectors, 45 Figure 2-11 Electron micrograph of Candidatus Liberibacter sp. in the phloem of infected citrus tree, 46 Figure 3-1 Conceptual model of agency relationships, 90 Figure 5-1 Decision tree for using an inducement prize rather than other types of research or development support, 135 BOXES Box 2-1 Huanglongbing Management in South Africa, 51 Box 2-2 Huanglongbing Management in China, 52 Box 2-3 Huanglongbing Management in São Paulo State, Brazil, 53

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Abbreviations and Acronyms ACP Asian citrus psyllid ABP anti bacterial peptide ACPS advanced citrus production system AFRI Agriculture and Food Research Initiative APHIS Animal and Plant Health Inspection Service (USDA) ARS Agricultural Research Service (USDA) CAC Citrus Administrative Committee CC (or CBC) citrus canker, citrus bacterial canker CCTF Core Citrus Transformation Facility CDFA California Department of Food and Agriculture cDNA complementary DNA CHMA Citrus Health Management Areas CHRP Citrus Health Response Program CiLV bacilliform virus (causal agent of Leprosis) CLaf Candidatus Liberibacter africanus CLam Candidatus Liberibacter americanus CLas Candidatus Liberibacter asiaticus c-PCR competitive polymerase chain reaction CPHST Center for Plant Health Science and Technology CRDF Citrus Research and Development Foundation CREC Citrus Research and Education Center CSD citrus sudden death CTAB cetyltrimethylammonium bromide CTV citrus tristeza virus CVC citrus variegated chlorosis DEP Department of Environmental Protection DNA deoxyribonucleic acid DMDS dimethyl disulfide DMS Differential Mobility Spectrometer DOD US Department of Defense DOE US Department of Energy DOL US Department of Labor DPI Division of Plant Industry (FDACS) dsRNA double stranded RNA xv

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xvi ABBREVIATIONS AND ACRONYMS ELISA enzyme-linked immunosorbent assay EM electron microscopy EPA US Environmental Protection Agency EST expressed sequence tag FCIRCC Florida Citrus Industry Research Coordinating Council FCM Florida Citrus Mutual FCP Florida Citrus Packers FCPA Florida Citrus Processors Association FCPMA Florida Citrus Production Managers Association FCPRAC Florida Citrus Production Research Advisory Council FDA US Food and Drug Administration FDACS Florida Department of Agriculture and Consumer Services FDOC Florida Department of Citrus/Florida Citrus Commission FFSP Florida Foundation Seed Producers, Inc. FGFSA Florida Gift Fruit Shippers Association FIFRA Federal Insecticide Fungicide and Rodenticide Act FL DEP Florida Department of Environmental Protection FNGLA Florida Nursery, Growers and Landscape Association GC guanine-cytosine GWSS glassy winged sharpshooter HIPREE Huanglongbing Information Platform for Research, Extension and Education HLB huanglongbing ICE US Immigration and Customs Enforcement IFAS Institute of Food and Agricultural Sciences (UF) ICGC International Citrus Genome Consortium IOCV International Organization of Citrus Virologists IP intellectual property IPM integrated pest management IR-4 Interregional Project Number 4 IRM insecticide resistance management programs IRREC Indian River Research and Education Center LFM lateral flow microarray MA monoclonal antibodies Mbp megabase pairs MCDV maize chlorotic dwarf virus MDMV maize dwarf mosaic virus miRNA micro RNA

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ABBREVIATIONS AND ACRONYMS xvii NAE National Academy of Engineering NIH National Institutes of Health n-PCR nested polymerase chain reaction NSF National Science Foundation NVDMC New Varieties Development and Management Corporation OHS Open Hydrophonics System OMRI Organic Materials Review Institute OSHA US Occupational Safety and Health Administration OSU Ohio State University PASS potentially actionable suspect samples PCR polymerase chain reaction PC-STR psyllid control and symptomatic tree removal PFD postbloom fruit drop PI principal investigator PIPE Pest Information Platform for Extension and Education PIPRA Public Intellectual Property Resource for Agriculture PMAP Pest Management Alternatives Program PPQ Plant Pest and Quarantine (+) ssRNA positive, single stranded RNA q-PCR quantitative real-time polymerase chain reaction rDNA ribosomal DNA R&D research and development RFP Request for Proposals RNA ribonucleic acid RNAi RNA interference rRNA ribosomal RNA RTi-PCR real-time polymerase chain reaction SAB scientific advisory board SAR systemic acquired resistance SCRA Specialty Crops Regulatory Assistance SGDL Southern Gardens Diagnostic Laboratory SIT sterile insect technique SNP single nucleotide polyphormism SPS Saõ Paulo State SWFREC Southwest Florida Research and Education Center TEM transmission electron microscopy TIG Technology Innovation Group, Inc. tRNA transfer RNA

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xviii ABBREVIATIONS AND ACRONYMS UAE United Arab Emirates UC University of California UF University of Florida USDA US Department of Agriculture USPTO US Patent and Trademark Office WBDL witches’ broom disease of limes VOC volatile organic compound