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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Page viii Cite
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Page xiii Cite
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: 10.17226/25026.
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PREPUBLICATION COPY A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease Committee on a Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease Board on Agriculture and Natural Resources Division on Earth and Life Studies A Consensus Study Report of

THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 This activity was supported by Contract/Grant No. 10003459 with the Citrus Research and Development Founda- tion. Any opinions, findings, conclusions, or recommendations expressed in this publication do not necessarily reflect the views of any organization or agency that provided support for the project. Digital Object Identifier: https://doi.org/10.17226/25026 Additional copies of this report are available for sale from the National Academies Press, 500 Fifth Street NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. Copyright 2018 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Suggested Citation: National Academies of Sciences, Engineering, and Medicine. 2018. A Review of the Citrus Green- ing Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease. Washington, DC: The National Academies Press. doi: https://doi.org/10.17226/25026. Prepublication Copy

The National Academy of Sciences was established in 1863 by an Act of Congress, signed by President Lincoln, as a private, nongovernmental institution to advise the nation on issues re- lated to science and technology. Members are elected by their peers for outstanding contribu- tions to research. Dr. Marcia McNutt is president. The National Academy of Engineering was established in 1964 under the charter of the Na- tional Academy of Sciences to bring the practices of engineering to advising the nation. Mem- bers are elected by their peers for extraordinary contributions to engineering. Dr. C. D. Mote, Jr., is president. The National Academy of Medicine (formerly the Institute of Medicine) was established in 1970 under the charter of the National Academy of Sciences to advise the nation on medical and health issues. Members are elected by their peers for distinguished contributions to medicine and health. Dr. Victor J. Dzau is president. The three Academies work together as the National Academies of Sciences, Engineering, and Medicine to provide independent, objective analysis and advice to the nation and conduct other activities to solve complex problems and inform public policy decisions. The National Academies also encourage education and research, recognize outstanding contributions to knowledge, and increase public understanding in matters of science, engineering, and medicine. Learn more about the National Academies of Sciences, Engineering, and Medicine at www.nationalacademies.org. Prepublication Copy

Consensus Study Reports published by the National Academies of Sciences, Engineering, and Medicine document the evidence-based consensus on the study’s statement of task by an au- thoring committee of experts. Reports typically include findings, conclusions, and recommen- dations based on information gathered by the committee and the committee’s deliberations. Each report has been subjected to a rigorous and independent peer-review process and it rep- resents the position of the National Academies on the statement of task. Proceedings published by the National Academies of Sciences, Engineering, and Medi- cine chronicle the presentations and discussions at a workshop, symposium, or other event con- vened by the National Academies. The statements and opinions contained in proceedings are those of the participants and are not endorsed by other participants, the planning committee, or the National Academies. For information about other products and activities of the National Academies, please visit www.nationalacademies.org/about/whatwedo. Prepublication Copy

COMMITTEE ON A REVIEW OF THE CITRUS GREENING RESEARCH AND DEVELOPMENT EFFORTS SUPPORTED BY THE CITRUS RESEARCH AND DEVELOPMENT FOUNDATION: FIGHTING A RAVAGING DISEASE Chair JACQUELINE FLETCHER, Oklahoma State University (Emerita) Members MAY R. BERENBAUM, NAS,1 University of Illinois, Champaign STEWART M. GRAY, Agricultural Research Service, U.S. Department of Agriculture RUSSELL L. GROVES, University of Wisconsin, Madison RALPH SCORZA, Ralph Scorza LLC (retired from Agricultural Research Service, U.S. Department of Agriculture) LINDSAY R. TRIPLETT, Connecticut Agricultural Experiment Station, New Haven JOHN TRUMBLE, University of California, Riverside BING YANG, Iowa State University, Ames Staff CAMILLA YANDOC ABLES, Study Director JENNA BRISCOE, Research Assistant 1 National Academy of Sciences. Prepublication Copy v

BOARD ON AGRICULTURE AND NATURAL RESOURCES Chair CHARLES W. RICE, Kansas State University, Manhattan, KS Members SHANE C. BURGESS, University of Arizona, Tucson, AZ SUSAN CAPALBO, Oregon State University, Corvallis, OR GAIL CZARNECKI-MAULDEN, Nestle Purina PetCare, St. Louis, MO GEBISA EJETA, Purdue University, West Lafayette, IN JAMES S. FAMIGLIETTI, California Institute of Technology, Pasadena, CA FRED GOULD, NAS1, North Carolina State University, Raleigh, NC DOUGLAS B. JACKSON-SMITH, Ohio State University, Wooster, OH JAMES W. JONES, NAE2, University of Florida, Gainesville, FL STEPHEN S. KELLEY, North Carolina State University, Raleigh, NC JAN E. LEACH, Colorado State University, Fort Collins, CO JILL J. MCCLUSKEY, Washington State University, Richland, WA KAREN I. PLAUT, Purdue University, West Lafayette, IN JIM E. RIVIERE, NAM3, Kansas State University, Manhattan, KS Staff ROBIN A. SCHOEN, Director CAMILLA YANDOC ABLES, Senior Program Officer JENNA BRISCOE, Research Assistant KARA N. LANEY, Senior Program Officer PEGGY TSAI YIH, Senior Program Officer 1 National Academy of Sciences. 2 National Academy of Engineering. 3 National Academy of Medicine. vi Prepublication Copy

Preface Citrus huanglongbing (HLB) is a complex, challenging, and devastating disease that threatens a major United States crop despite intense management efforts. Research on HLB over the past decade has involved scientists, growers, industry representatives, regulators, and administrators who have explored multiple fac- ets of the disease syndrome and the many environmental, horticultural, sociological, and economic factors that impact it. This National Academies of Sciences, Engineering, and Medicine study committee, follow- ing its Statement of Task to review and assess these research efforts, has relied upon many sources of information including refereed scientific journal articles, extension publications, websites, presentations by researchers and others at the 2017 International Research Conference on Huanglongbing as well as in a series of the National Academies-hosted scientific open forums and webinars targeted to specific research topics, project progress reports, and personal communications. The committee is grateful to each of the individuals who contributed to the committee’s work by sharing information about their research, observa- tions, perspectives, and experience. The information gathered from these sources and during these interac- tions was essential to the committee's understanding of the issues and to the writing of this report. Many of these people are acknowledged by name in Appendix B; we realize that we may have missed some contrib- utors and regret any inadvertent omissions. The committee owes much to Dr. Camilla Y. Ables, Study Director, whose knowledge of citrus pro- duction and pathology, as well as her professional and capable guidance, contributions and support at each stage of the committee’s work, were invaluable to this process. We also thank Robin A. Schoen, Director of the National Academies’ Board on Agriculture and Natural Resources, for her wise and thoughtful input and advice throughout the study, and Jenna Briscoe, Research Assistant, whose IT skills, meeting organi- zation support, and good cheer made these aspects of our work move seamlessly. We thank Dr. Harold Browning, Chief Operations Officer of our study sponsor, the Citrus Research and Development Founda- tion (CRDF), and the CRDF staff, who worked closely and tirelessly with us to assure that we had access to needed information. Thanks are due also to representatives of other HLB funding agencies and federal agencies (the California Citrus Research Board, USDA NIFA, USDA MAC, USDA APHIS, USDA ARS, and NSF), involved in HLB research and management, for providing information on their responsibilities activities and projects. Sincere thanks are due to the members of the study committee, a group of outstanding and experienced scientists who dug deeply into the literature, entered thoughtfully and enthusiastically into discussions with one another and with HLB information providers, and used their remarkable analysis and composition skills to create a report that is not only comprehensive, but perceptive and forward thinking. Over the past year, as the committee participated in four project meetings/research forums and three webinars in addition to numerous conference calls, members maintained a high level of energy, sustained by trust that their science- based and experience-informed findings, conclusions, and recommendations will provide support to HLB stakeholder groups for future decision-making and research prioritization on this challenging disease. Jacqueline Fletcher Chair, Committee on a Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease Prepublication Copy vii

Acknowledgments This Consensus Study Report was reviewed in draft form by individuals chosen for their diverse per- spectives and technical expertise. The purpose of this independent review is to provide candid and critical comments that will assist the National Academies of Sciences, Engineering, and Medicine in making each published report as sound as possible and to ensure that it meets the institutional standards for quality, 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 thank the following individuals for their review of this report: Blake Bextine, University of Texas at Tyler Christopher Dardick, Agricultural Research Service, US Department of Agriculture John Dougherty, Monsanto (retired) Sheng Yang He, NAS, Michigan State University George G. Kennedy, North Carolina State University Steven Lindow, NAS, University of California, Berkeley Hanu Pappu, Washington State University Gail Wisler, Agricultural Research Service, US Department of Agriculture (retired) Raymond Yokomi, Agricultural Research Service, US Department of Agriculture Although the reviewers listed above provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations of this report nor did they see the final draft before its release. The review of this report was overseen by Jeffery Dangl, NAS, University of North Carolina and Michael Ladisch, NAE, Purdue University. They were responsible for making certain that an independent examination of this report was carried out in accordance with the standards of the National Academies and that all review comments were carefully considered. Responsibility for the final content rests entirely with the authoring committee and the National Academies. Prepublication Copy ix

Contents ACRONYMS AND ABBREVIATIONS .................................................................................................................xiii EXECUTIVE SUMMARY ........................................................................................................................................ 1 SUMMARY .................................................................................................................................................................. 3 1 INTRODUCTION .......................................................................................................................................... 14 Citrus Greening, 14 Citrus Greening Research, 15 Study Origin/Rationale, 18 Statement of Task, 18 Committee’s Approach, 18 Scope and Organization of the Report, 19 References, 19 2 CURRENT KNOWLEDGE ON HUANGLONGBING (HLB) AND THE INTERACTIONS OF THE PATHOGEN, VECTOR, AND HOST .......................................................... 21 HLB: The Causal (or Associated) Bacteria, 21 HLB: The Psyllid Vector, 23 HLB: The Rutaceous Hosts, 25 Host Plant-Pathogen Interactions and Host Plant Defense Mechanisms, 28 Pathogen-Vector Interactions, 30 Vector-Host Interactions, 31 Diagnostics, 32 HLB Management, 33 References, 34 3 HLB RESEARCH AND DEVELOPMENT EFFORTS .............................................................................. 44 HLB Pathogen, Vector, and Hosts, 44 Vector-Host Interactions, 50 Pathogen-Vector Interactions, 53 Host – Pathogen Interactions, 55 HLB Management, 56 Sociological and Economic Aspects of HLB and Its Management, 60 Overall Findings. Conclusions, and Recommendations, 64 References, 66 4 NOTABLE OUTCOMES, PITFALLS, AND FUTURE DIRECTIONS ................................................... 74 Biology and Ecology of the HLB Causal or Associated Bacteria and Its Insect Vector, 74 Interactions of the HLB Pathogen, Vector, and Host, 81 HLB Management, 89 Overarching Findings, Conclusions, and Recommendations for Future Research Efforts in HLB Management, 109 References, 112 Prepublication Copy xi

Contents APPENDIXES A COMMITTEE MEMBER BIOGRAPHIES .............................................................................................. 126 B OPEN SESSION MEETING AGENDAS ................................................................................................... 131 C GLOSSARY .................................................................................................................................................. 140 D SELECTED CITRUS RESEARCH DEVELOPMENT FOUNDATION PROJECTS .......................... 150 TABLES AND BOXES TABLES 1-1 NRC (2010) Research and Technology Recommendations, 15 1-2 HLB Research Areas Funded by CRDF, MAC Group, NIFA/CDRE, and CRB, 16 BOXES 1-1 Statement of Task, 18 4-1 Key Research Findings, 74 4-2 Recommendations for Future Research, 81 4-3 Key Research Findings, 81 4-4 Recommendations for Future Research, 89 4-5 Key Research Findings, 89 4-6 Recommendations for Future Research, 108 xii Prepublication Copy

Acronyms and Abbreviations ACP(s) Asian citrus psyllid(s), Diaphorina citri AHL acyl-homoserine lactone AMP(s) antimicrobial peptide(s) APHIS U.S. Department of Agriculture Animal and Plant Health Inspection Service ARS U.S. Department of Agriculture Agricultural Research Service ATP adenosine triphosphate BANR Board on Agriculture and Natural Resources (NASEM) Bt Bacillus thuringiensis Ca calcium CCTF Core Citrus Transformation Facility (UF CREC) cDNA complementary DNA CDR constitutive disease resistance CDRE Citrus Disease Research and Extension (USDA NIFA SCRI) CDS Citrus Disease Subcommittee (NAREEE) CHMA(s) Citrus Health Management Area(s) CHRP Citrus Health Response Program (USDA APHIS) CLaf Candidatus Liberibacter africanus CLam Candidatus Liberibacter americanum CLas Candidatus Liberibacter asiaticus CRB Citrus Research Board (Visalia, California) CRDF Citrus Research and Development Foundation (Lake Alfred, Florida) CREC Citrus Research and Education Center (University of Florida, Lake Alfred, FL) CRISPR clustered regularly-interspaced short palindromic repeats CRISPR-Cas9 CRISPR-associated protein-9 nuclease CTV Citrus tristeza virus Cu copper CYPome cytochrome p450 complement DNA deoxyribonucleic acid dsRNA double-stranded RNA EDT early detection technology EFNP enhanced foliar nutrition program ENP(s) enhanced nutritional program(s) EPA Environmental Protection Agency EST expressed sequence tag FAO Food and Agriculture Organization of the United Nations FCPRAC Florida Citrus Advanced Technology Program (precursor agency to CRDF) G+C guanine and cytosine GE genetic engineering; genetically engineered GFP green fluorescent protein GM genetically modified GMO genetically modified organism HLB huanglongbing (alternate name: citrus greening disease) IFAS University of Florida Institute of Food and Agricultural Sciences IP intellectual property IPM integrated pest management Prepublication Copy xiii

Acronyms and Abbreviations IRCHLB International Research Conference on Huanglongbing K potassium LAMP loop-mediated isothermal amplification LED light-emitting diode MAC Multi-Agency Coordination (USDA) MAPK mitogen activated protein kinase Mb megabases MeSA methyl salicylate Mn manganese mRNA messenger RNA N nitrogen NAREEE National Agricultural Research, Education, Extension and Economics NASS U.S. Department of Agriculture National Agricultural Statistics Service NBS-LRR nucleotide binding site-leucine rich repeat NCBI National Center for Biotechnology Information NIFA U.S. Department of Agriculture National Institute for Food and Agriculture NIH National Institutes of Health NRC National Research Council NVDMC New Variety Development & Management Corporation Orco olfactory receptor co-receptor P phosphorous PAMP pathogen-associated molecular pattern PCR polymerase chain reaction PGR(s) plant growth regulator(s) PI principal investigator PTI PAMP-triggered immune response qPCR quantitative PCR R gene resistance gene R&D research and development RFA request for applications RNA ribonucleic acid RNAi RNA interference ROS reactive oxygen species SA salicylic acid SAR systemic acquired resistance SCRI Specialty Crops Research Initiative (USDA) SDE Sec-dependent effector Sec general secretory system SNP soft or non-clumping nanoparticles SOD superoxide dismutase T1SS Type I secretion system TCPB Texas Citrus Producers Board UC University of California UCR University of California at Riverside UF University of Florida USDA United States Department of Agriculture UV ultraviolet VOC volatile organic compound Zn zinc xiv Prepublication Copy

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Huanglongbing (HLB) or citrus greening, first observed more than a hundred years ago in Asia, is the most serious disease threat to the citrus-growing industry worldwide due to its complexity, destructiveness, and incalcitrance to management. First detected in Florida in 2005, HLB is now widespread in the state and threatens the survival of the Florida citrus industry despite substantial allocation of research funds by Florida citrus growers and federal and state agencies.

As the HLB epidemic raged in 2008, Florida citrus growers began allocating funds for HLB research in hopes of finding short-, medium-, and long-term solutions. This effort created the Citrus Research and Development Foundation (CRDF), an organization with oversight responsibility for HLB research and development efforts in Florida. This report provides an independent review of the portfolio of research projects that have been or continue to be supported by the CRDF. It seeks to identify ways to retool HLB research—which, despite significantly increasing understanding of the factors involved in HLB, has produced no major breakthroughs in controlling the disease—and accelerate the development of durable tools and strategies that could help abate the damage caused by HLB and prevent the possible collapse of the Florida citrus industry.

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