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Introduction

CITRUS GREENING

Huanglongbing (HLB), also known as citrus greening, has gained renown as the most serious threat to citrus worldwide. First observed more than a hundred years ago in Asia, the disease is a challenging threat due to its complexity, its destructiveness, the susceptibility of most commercial citrus species and cultivars regardless of rootstock, and the lack of an effective method for suppressing its causal agents or its insect vectors.

HLB is associated with three species of the genus Liberibacter: Candidatus Liberibacter asiaticus (CLas), Candidatus Liberibacter africanus, and Candidatus Liberibacter americanus. All Ca. Liberibacter species that cause disease in citrus are transmitted by Diaphorina citri (Kuwayama), the Asian citrus psyllid (ACP), and Trioza erytreae (del Guerco), the African citrus psyllid. The pomelo psyllid, Cacopsylla (Psylla) citrisuga Yang & Li, was found to be a carrier of CLas that may potentially transmit CLas to healthy citrus (Cen et al., 2012). Trees infected with HLB have blotchy mottling of leaves, shoot stunting, and gradual dieback of branches. They produce small, deformed fruits with bitter juice, which is unmarketable. Infected trees do not die right away; they can remain in a steady state of decline for several years. If not removed from the grove and destroyed, infected trees can serve as sources of inoculum. For a detailed account of HLB history, etiology, biology, epidemiology, detection, geographical distribution, and control methods, the reader is referred to Huanglongbing: A Destructive, Newly-Emerging, Century-Old Disease of Citrus by Bové (2006) and Citrus Huanglongbing: The Pathogen and Its Impact by Gottwald et al. (2007).

HLB may have originated in southern China,¹ where yellowing and leaf mottle on citrus trees were reported by Reinking in 1919. However, there are reports that symptoms of HLB were observed in India in the 1700s and 1800s, and that by 1912 it had become a severe problem in Bombay province (Capoor, 1963). By the 1970s, HLB had devastated many citrus-growing regions in Asia and Africa. At that time, ACP had been established in the Western Hemisphere for several decades, having been first reported in Brazil in 1942 (da Costa Lima, 1942). By 1998, it was found in south Florida and was soon thereafter widespread throughout the state (Halbert and Manjunath, 2004). In 2004, HLB was first detected in the Americas, in the São Paulo state of Brazil. In 2005, HLB was detected in Miami-Dade County in Florida. HLB has since been reported in six other states in the United States: California, Georgia, Hawaii, Louisiana, South Carolina, and Texas. The disease is now widespread in all citrus-growing counties of Florida, having been reported in the Florida Panhandle, among the last remaining disease-free regions, in 2016 (Iriarte et al., 2017). Between 2000 and 2014, citrus acreage in the state declined from roughly 750,000 acres (303,514 hectares) to 476,000 acres (192,630 hectares), and production volume has declined by 58% since 2005. In Florida alone, HLB has caused a cumulative loss of $2.994 billion in grower revenues over the 2006–2007 to 2013–2014 period, an average of $374 million per year (Hodges et al., 2014).

CITRUS GREENING RESEARCH

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. By the summer of 2010 CRDF was managing a portfolio of about 124 projects worth $14.3 million, which aimed to address the research and technology recommendations in the National Research Council (NRC) 2010 report Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease (see Table 1-1). Projects funded during that time were focused on the following areas: (1) interrupting the breeding/feeding of psyllids, (2) vector management, (3) creating disease-resistant plants produced through

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¹ This widely accepted assumption has been mentioned in literature; however, evidence that HLB did not originate in China has been presented by Beattie et al. (2008) in their paper “On the Origins of Citrus, Huanglongbing, Diaphorina citri and Trioza erytreae” available at https://www.plantmanagementnetwork.org/proceedings/irchlb/2008/presentations/IRCHLB.K.2.pdf. Accessed May 4, 2018.

TABLE 1-1 NRC (2010) Research and Technology Recommendations

traditional breeding methods or genetic engineering, and (4) control of the HLB bacteria and improvement of the host response (CRDF, 2010). Between 2010 and 2017, CRDF invested $124 million in 398 citrus projects, of which about 90% are focused on HLB.² The categories of the currently funded CRDF projects, established by the CRDF’s Research Management Committee, are presented in Table 1-2.

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² H.W. Browning, COO, CRDF, personal communication, June 13, 2017.

TABLE 1-2 HLB Research Areas Funded by CRDF, MAC Group, NIFA CDRE, and CRB

SOURCES: MAC 2014 and 2015 Research Areas (USDA, 2017a); MAC 2016 Research Areas (USDA APHIS, 2016); NIFA CDRE RFA (USDA NIFA, 2017); CRB Research Areas Funded/2017 Priorities (Schulz, 2017).

The U.S. Department of Agriculture (USDA) also has been supporting HLB research, providing more than $380 million between fiscal years (FY) 2009 and 2015. Since 2015 it has allocated an additional $43.6 million (for 14 HLB projects) through the National Institute of Food and Agriculture (NIFA) Specialty Crop Research Initiative (SCRI) Citrus Disease Research and Extension (CDRE) program (USDA, 2016). The CDRE program’s regional and national priorities address these four general categories: (1) the HLB pathogen, (2) the HLB insect vector, (3) citrus orchard production systems, and (4) nonagricultural citrus tree owners. In January 2017, NIFA funded four grants worth $13.6 million through its CDRE program. In April 2017, the agency announced the availability of $21.8 million for HLB research, also through their CDRE program. The most recent HLB-related request for applications (RFA) issued by NIFA requested that applicants address the six areas of highest priority for delivery of solutions in the near or intermediate timeframe, that were identified by the Citrus Disease Subcommittee of the National Agricultural Research, Extension, Education, and Economics (NAREEE) Advisory Board. According to the RFA, these priority areas (see Table 1-2) are to be addressed “through the integration of research and extension activities that use systems-based, trans-disciplinary approaches.”

The USDA Agricultural Research Service (ARS) is also actively involved in HLB research. In 2017, the ARS annual expenditures on HLB-related research exceeded $21 million. Collaborative investigations are ongoing at seven ARS locations in California, Florida, Maryland, and New York, and with scientists at several universities. Areas of study include breeding for resistance to HLB, impact of HLB on flavor quality, vector control and transmission disruption, early detection, therapeutic treatments via thermotherapy, and antimicrobial sprays.³

In December 2013, the HLB Multi-Agency Coordination (MAC) Group⁴ was formed by then–agriculture secretary Thomas Vilsack to promote coordination across federal and state agencies and industry in order to rapidly deliver near-term solutions to help citrus growers maintain grove productivity until long-term solutions could be developed. The MAC Group awarded $20 million to 31 projects in FY 2014–2015 and $3 million to six projects in FY 2016–2017 (USDA, 2017a). The focus areas of projects funded by the MAC Group in 2014 and 2015 are listed in Table 1-2. As of June 2017, the MAC Group has awarded about $25.5 million in projects;

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³ G. Wisler, USDA-ARS (retired), personal communication, January 25, 2018.

⁴ The HLB MAC Group is composed of representatives from USDA Animal Plant Health Inspection Service (APHIS), USDA NIFA, USDA Agricultural Research Service, Environmental Protection Agency, State Departments of Agriculture from Arizona, California, Florida, and Texas, and the citrus industry.

an additional $5.5 million was received by the MAC Group from Congress for FY 2017–2018, which brings the total amount of MAC funding for HLB research to $31 million.⁵

The USDA Animal and Plant Health Inspection Service (APHIS) Citrus Health Response Program (CHRP) provides funding for the administration of domestic regulations, pest surveys, coordinated area-wide suppression of ACP, and other initiatives in partnership with state regulatory agencies and the citrus industry in Florida, California, Texas, and Arizona (USDA, 2017b). From FY 2014 to FY 2016, however, CHRP also invested about $1.6 million on six research projects that were focused on HLB detection, HLB management practices, and ACP biocontrol (CRDF, 2016).

California citrus growers, through the Citrus Research Board (CRB), have invested $33 million in ACP and HLB research since 2008. HLB projects funded since 2008 fall into six categories (see Table 1-2). The 2017 CRB HLB research priorities (Schulz, 2017) are also listed in Table 1-2. To date, CRB has funded about 97 HLB research projects and has co-funded about 5 projects with CRDF.⁶

Texas growers also fund citrus research through the Texas Citrus Producers Board (TCPB) but not to the same extent as California and Florida growers. From 2015 to 2016, TCPB invested about $193,000 on research related to HLB and citrus production/plant improvement (USDA, 2017b).

STUDY ORIGIN/RATIONALE

In late 2016, CRDF contacted the Board on Agriculture and Natural Resources of the National Academies of Sciences, Engineering, and Medicine to request an independent review of the portfolio of research projects that have been or continue to be supported by the CRDF. This request was made 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.

STATEMENT OF TASK

This study was carried out by the Committee on a Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease in

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⁵ A. McMellen-Brannigan, APHIS, personal communication, June 29, 2017.

⁶ G. Schulz, President, CRB, personal communication, June 19, 2017.

accordance with the statement of task in Box 1-1. The committee members’ biographical information is given in Appendix A of this report.

COMMITTEE’S APPROACH

This review of the HLB research and development efforts was conducted using information from various sources, including CRDF (which provided publicly accessible information on past and current projects), principal investigators of past and current projects supported by CRDF, HLB researchers who were invited to speak at committee open sessions and webinars, refereed journal articles, and nonrefereed publications (e.g., trade magazines, extension materials, and meeting or conference proceedings).

The committee held four meetings and three webinars between March and December 2017. At CRDF’s request, the first committee meeting was held in conjunction with the 5th International Research Conference on Huanglongbing (IRCHLB) in Orlando, Florida. At this meeting, the committee members had the opportunity to listen to oral presentations at the IRCHLB. The committee also talked with CRDF representatives, received clarification on the committee’s charge, and learned about HLB research supported by USDA APHIS, the HLB MAC Group, and California’s CRB from some of the invited speakers.

The committee’s second, third, and fourth meetings were held in May (Irvine, California), July (Washington, D.C.), and November (Washington, D.C.), respectively. Public forums were held during the open sessions of the second, third, and fourth meetings on the following topics: (1) citrus breeding and transformation for HLB resistance, (2) ACP control and management, and (3) cultural practices to keep HLB-infected trees productive. Webinars were held in August, September, and October on the following topics: (1) HLB diagnostics and detection, (2) CLas and bacterial control, and (3) economic and sociological impacts of HLB and HLB management strategies. The speakers and agendas for the forums and webinars are provided in Appendix B.

To aid its analysis of what is currently known about HLB and the research efforts, progress, and pitfalls, the committee classified the various research projects (funded by CRDF and other agencies) into these categories: HLB causal (or associated) bacteria biology and ecology, HLB insect vector biology and ecology, HLB plant hosts, host–pathogen interactions, pathogen–vector interactions, vector–host interactions, diagnostics, and management (bacterial control, insect control, and cultural control).

Part of the committee’s charge was to determine which research areas should be continued or discontinued by highlighting notable outcomes in each of these research areas; the committee addressed this charge by highlighting notable outcomes in each area, reviewing factors that hamper or present significant challenges (pitfalls) to the work, and providing suggestions of possible areas for future research (Chapter 4). However, the committee was unable to define further the extent of research progress or to comment more specifically on the selection of research areas to be continued or discontinued because information available to it on research outcomes, applications, and impacts was insufficient to do so in many cases, particularly for recent projects. A number of projects have resulted in no, or relatively few, publications in peer-reviewed journals, and midterm and final research progress reporting to CRDF was inconsistent in both compliance and the amount of detail provided.

SCOPE AND ORGANIZATION OF THE REPORT

This report consists of four chapters. This chapter provides the context for this study. Chapter 2 provides key information about the disease that reflects the current understanding of the factors that influence its occurrence, severity, and incalcitrance to effective management. Chapter 3 examines the HLB research areas that have received or continue to receive support from CRDF and the HLB research efforts that are being funded by other agencies (state and federal) and overlaps or duplications with CRDF-funded research efforts. Chapter 4 presents significant research findings and progress, as well as issues of concern (pitfalls), from the past decade of CRDF-funded HLB research as well as from input to the committee by researchers, growers, and other stakeholders. Chapter 4 also includes possible future research directions for CRDF consideration, as well as overall major findings, conclusions, and recommendations of the committee.

REFERENCES

Iriarte, F., X. Martini, and M. Paret. 2017. Disease Alert: Citrus Greening and Asian Citrus Psyllids Found in the Panhandle. University of Florida IFAS Extension Panhandle Ag e-News, March 3. Available at http://nwdistrict.ifas.ufl.edu/phag/2017/03/03/disease-alert-citrus-greening-and-asian-citrus-psyllids-found-in-the-panhandle/. Accessed December 29, 2017.

NRC (National Research Council). 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press.

Reinking, O. A. 1919. Diseases of economic plants in Southern China. Philippine Agriculturist 8(4):109-135.

Schulz, G. 2017. Presentation at the Second Meeting on Review of Citrus Greening Research and Development Efforts, May 23, 2017, Irvine, CA.

USDA (U.S. Department of Agriculture). 2016. USDA Announces $22 Million Available for Research to Combat Citrus Greening. Press Release: April 21, 2016. Available at https://www.usda.gov/media/press-releases/2016/04/21/usda-announces-22-million-available-research-combat-citrus-greening. Accessed June 14, 2017.

USDA. 2017a. Huanglongbing (HLB) Multi-Agency Coordination Updates. Available at https://www.usda.gov/topics/disaster/multi-agency-response-devastating-citrus-disease/huanglongbing-hlb-multi-agency. Accessed June 23, 2017.

USDA. 2017b. USDA Efforts to Combat Huanglongbing (HLB). Available at https://www.usda.gov/topics/disaster/multi-agency-response-devastating-citrus-disease/usda-efforts-combat-huanglongbing. Accessed June 26, 2017.

USDA APHIS (Animal and Plant Health Inspection Service). 2016. HLB-MAC Research. Available at https://www.usda.gov/sites/default/files/documents/2016-hlb-mac-funded-projects.pdf. Accessed June 26, 2017.

USDA NIFA (National Institute of Food and Agriculture). 2017. Emergency Citrus Disease Research and Extension. Available at https://nifa.usda.gov/sites/default/files/rfa/2017_Emergency%20__final.pdf. Accessed June 23, 2017.

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