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
Washington, DC
www.nap.edu
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This activity was supported by Contract/Grant No. 10003459 with the Citrus Research and Development Foundation. 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.
International Standard Book Number-13: 978-0-309-47214-2
International Standard Book Number-10: 0-309-47214-8
Digital Object Identifier: https://doi.org/10.17226/25026
Cover photo credits: Top left: cross-sections of citrus fruits courtesy of the U.S. Department of Agriculture’s Agricultural Research Service; Top right: citrus plant infested with Asian citrus psyllids courtesy of the U.S. Department of Agriculture’s Animal and Plant Health Inspection Service; Bottom left: citrus leaf with symptoms of citrus greening courtesy of the U.S. Department of Agriculture’s Agricultural Research Service; Bottom middle: shoots of mature Hamlin sweet orange in tissue culture potentially altered with disease resistance genes courtesy of Janice Zale; Bottom right: close-up photo of Asian citrus psyllid courtesy of the U.S. Department of Agriculture’s Agricultural Research Service.
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Suggested Citation: 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: https://doi.org/10.17226/25026.
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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 at Urbana-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.
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, Nestlé Purina PetCare, St. Louis, MO
GEBISA EJETA, Purdue University, West Lafayette, IN
JAMES S. FAMIGLIETTI, California Institute of Technology, Pasadena, CA
FRED GOULD, NAS,1 North Carolina State University, Raleigh, NC
DOUGLAS B. JACKSON-SMITH, The Ohio State University, Wooster, OH
JAMES W. JONES, NAE,2 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, NAM,3 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.
Preface
Citrus huanglongbing (HLB) is a complex, challenging, and devastating disease that threatens a major U.S. 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 facets 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, following 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, observations, perspectives, and experience. The information gathered from these sources and during these interactions 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 contributors and regret any inadvertent omissions.
The committee owes much to Dr. Camilla Y. Ables, Study Director, whose knowledge of citrus production 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 organization 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 Foundation (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, and USDA ARS), 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 skills in analysis and composition 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
Acknowledgments
This Consensus Study Report was reviewed in draft form by individuals chosen for their diverse perspectives 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, The University of Texas at Tyler
Christopher Dardick, Agricultural Research Service, U.S. Department of Agriculture
John Dougherty, Monsanto (retired)
Sheng Yang He, NAS,1 Michigan State University
George G. Kennedy, North Carolina State University
Steven Lindow, NAS,2 University of California, Berkeley
Hanu Pappu, Washington State University
Gail Wisler, Agricultural Research Service, U.S. Department of Agriculture (retired)
Raymond Yokomi, Agricultural Research Service, U.S. Department of Agriculture
___________________
1 National Academy of Sciences.
2 National Academy of Sciences.
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,3 University of North Carolina, and Michael Ladisch, NAE,4 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.
___________________
3 The National Academy of Sciences.
4 The National Academy of Engineering.
3 HLB RESEARCH AND DEVELOPMENT EFFORTS
HLB Pathogen, Vector, and Hosts
Sociological and Economic Aspects of HLB and Its Management
Overall Findings, Conclusions, and Recommendations
4 NOTABLE OUTCOMES, PITFALLS, AND FUTURE DIRECTIONS
Biology and Ecology of the HLB Causal or Associated Pathogen and Its Insect Vector
Interactions of the HLB Pathogen, Vector, and Host
Overarching Findings, Conclusions, and Recommendations for Future Research Efforts in HLB Management
BOXES AND TABLES
BOXES
4-3 Key Research Findings: Interactions of the HLB Pathogen, Vector, and Host
4-4 Recommendations for Future Research: Interactions of the HLB Pathogen, Vector, and Host
4-5 Key Research Findings: HLB Management
4-6 Recommendations for Future Research: HLB Management
TABLES
1-1 NRC (2010) Research and Technology Recommendations
1-2 HLB Research Areas Funded by CRDF, MAC Group, NIFA CDRE, and CRB
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Acronyms and Abbreviations
ACP | Asian citrus psyllid, Diaphorina citri |
AHL | acyl-homoserine lactone |
AMP | antimicrobial peptide or antimicrobial protein |
APHIS | U.S. Department of Agriculture Animal and Plant Health Inspection Service |
ARS | U.S. Department of Agriculture Agricultural Research Service |
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) |
CHMA | Citrus Health Management Area |
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, Florida) |
CRISPR | clustered regularly interspaced short palindromic repeats |
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) |
FAO | Food and Agriculture Organization of the United Nations |
FCPRAC | Florida Citrus Production Research Advisory Council (precursor agency to CRDF) |
GE | 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 |
IOCV | International Organization of Citrus Virologists |
IPM | integrated pest management |
IRCHLB | International Research Conference on Huanglongbing |
K | potassium |
LAMP | loop-mediated isothermal amplification |
MAC | Multi-Agency Coordination (USDA) |
MAPK | mitogen-activated protein kinase |
MeSA | methyl salicylate |
Mn | manganese |
mRNA | messenger RNA |
N | nitrogen |
NAREEE | National Agricultural Research, Extension, Education, and Economics |
NBS-LRR | nucleotide binding site–leucine-rich repeat |
NCBI | National Center for Biotechnology Information |
NI | near- to immediate-term |
NIFA | National Institute of Food and Agriculture |
NIH | National Institutes of Health |
NRC | National Research Council |
NVDMC | New Varieties Development & Management Corporation |
Orco | olfactory receptor co-receptor |
P | phosphorous |
PAMP | pathogen-associated molecular pattern |
PCR | polymerase chain reaction |
PGR | plant growth regulator |
PI | principal investigator |
PTI | PAMP-triggered immunity |
qPCR | quantitative polymerase chain reaction |
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 Crop Research Initiative |
SDE | Sec-dependent effector |
Sec | general secretory system |
SNP | soft or nonclumping nanoparticles |
SOD | superoxide dismutase |
T1SS | Type I secretion system |
TCPB | Texas Citrus Producers Board |
UC | University of California |
UCR | University of California, Riverside |
UF | University of Florida |
USDA | U.S. Department of Agriculture |
UV | ultraviolet |
VOC | volatile organic compound |
Zn | zinc |
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