T. R. Gottwald

Huanglongbing (HLB) is the most destructive citrus pathosystem worldwide. Previously known primarily from Asia and Africa, it was introduced into the Western Hemisphere in 2004. All infected commercial citrus industries continue to decline owing to inadequate current control methods. HLB increase and regional spatial spread, related to vector populations, are rapid compared with other arboreal pathosystems. Disease dynamics result from multiple simultaneous spatial processes, suggesting that psyllid vector transmission is a continuum from local area to very long distance. Evolutionarily, HLB appears to have originated as an insect endosymbiont that has moved into plants. Lack of exposure of citrus to the pathogen prior to approximately 100 years ago did not provide sufficient time for development of resistance. A prolonged incubation period and regional dispersal make eradication nonviable. Multiple asymptomatic infections per symptomatic tree, incomplete systemic distribution within trees, and prolonged incubation period make detection difficult and greatly complicate disease control.

Reliable, precise and accurate estimates of disease severity are important for predicting yield loss, monitoring and forecasting epidemics, for assessing crop germplasm for disease resistance, and for understanding fundamental biological processes including co-evolution. Disease assessments that are inaccurate and/or imprecise might lead to faulty conclusions being drawn from the data, which in turn can lead to incorrect actions being taken in disease management decisions. Plant disease can be quantified in several different ways. This review considers plant disease severity assessment at the scale of individual plant parts or plants, and describes our current understanding of the sources and causes of assessment error, a better understanding of which is required before improvements can be targeted. The review also considers how these can be identified using various statistical tools. Indeed, great strides have been made in the last thirty years in identifying the sources of assessment error inherent to visual rating, and this review highlights ways that assessment errors can be reduced—particularly by training raters or using assessment aids. Lesion number in relation to area infected is known to influence accuracy and precision of visual estimates—the greater the number of lesions for a given area infected results in more overestimation. Furthermore, there is a widespread tendency to overestimate disease severity at low severities (<10%). Both interrater and intrarater reliability can be variable, particularly if training or rating aids are not used. During the last eighty years acceptable accuracy and precision of visual disease assessments have often been achieved using disease scales, particularly because of the time they allegedly save, and the ease with which they can be learned, but recent work suggests there can be some disadvantages to their use. This review considers new technologies that offer opportunity to assess disease with greater objectivity (reliability, precision, and accuracy). One of these, visible light photography and digital image analysis has been increasingly used over the last thirty years, as software has become more sophisticated and user-friendly. Indeed, some studies have produced very accurate estimates of disease using image analysis. In contrast, hyperspectral imagery is relatively recent and has not been widely applied in plant pathology. Nonetheless, it offers interesting and potentially discerning opportunities to assess disease. As plant disease assessment becomes better understood, it is against the backdrop of concepts of reliability, precision and accuracy (and agreement) in plant pathology and measurement science. This review briefly describes these concepts in relation to plant disease assessment. Various advantages and disadvantages of the different approaches to disease assessment are described. For each assessment method some future research priorities are identified that would be of value in better understanding the theory of disease assessment, as it applies to improving and fully realizing the potential of image analysis and hyperspectral imagery.

Citrus huanglongbing is the most destructive disease of citrus worldwide. It is spread by citrus psyllids and is associated with a low-titer, phloem-limited infection by any of three uncultured species of alpha-Proteobacteria, 'Candidatus Liberibacter asiaticus', 'Ca. L. americanus', and 'Ca. L. africanus'. A complete circular 'Ca. L. asiaticus' genome has been obtained by metagenomics, using the DNA extracted from a single 'Ca. L. asiaticus'-infected psyllid. The 1.23-Mb genome has an average 36.5% GC content. Annotation revealed a high percentage of genes involved in both cell motility (4.5%) and active transport in general (8.0%), which may contribute to its virulence. 'Ca. L. asiaticus' appears to have a limited ability for aerobic respiration and is likely auxotrophic for at least five amino acids. Consistent with its intracellular nature, 'Ca. L. asiaticus' lacks type III and type IV secretion systems as well as typical free-living or plant-colonizing extracellular degradative enzymes. 'Ca. L. asiaticus' appears to have all type I secretion system genes needed for both multidrug efflux and toxin effector secretion. Multi-protein phylogenetic analysis confirmed 'Ca. L. asiaticus' as an early-branching and highly divergent member of the family Rhizobiaceae. This is the first genome sequence of an uncultured alpha-proteobacteria that is both an intracellular plant pathogen and insect symbiont.

Citrus Huanglongbing, aka greening disease, has been the subject of several reviews in recent years. In this article, the author presents a concise compilation of the main features and symptoms of the disease, the causal organisms and the vectors including impacts for Florida and Brazil, two relatively new areas where the disease has been discovered, as well as implications for California, Texas, and Arizona citrus industries, which are threatened by the close proximity to the new Florida epidemic, and the rest of the western hemisphere. Accepted for publication 19 June 2007. Published 6 September 2007.

UNLABELLED: SUMMARY Taxonomic status: Bacteria, Proteobacteria, gamma subdivision, Xanthomodales, Xanthomonas group, axonopodis DNA homology group, X. axonopodis pv. citri (Hasse) Vauterin et al. Microbiological properties: Gram negative, slender, rod-shaped, aerobic, motile by a single polar flagellum, produces slow growing, non-mucoid colonies in culture, ecologically obligate plant parasite. HOST RANGE: Causal agent of Asiatic citrus canker on most Citrus spp. and close relatives of Citrus in the family Rutaceae. Disease symptoms: Distinctively raised, necrotic lesions on fruits, stems and leaves. EPIDEMIOLOGY: Bacteria exude from lesions during wet weather and are disseminated by splash dispersal at short range, windblown rain at medium to long range and human assisted movement at all ranges. Crop loss: Severe infections cause defoliation, blemished fruit, premature fruit drop, die-back of twigs and general debilitation of the tree. Distribution: Citrus canker is not present in all subtropical to tropical regions of citriculture in the world, so considerable regulatory efforts are expended to prevent the introduction and spread of X. axonopodis pv. citri into areas in the Americas, Australia and elsewhere, with climates conducive to the disease. IMPORTANCE: Limited strategies exist for suppression of citrus canker on more susceptible cultivars. Blemished fruit are unmarketable and exposed fruit are restricted in market access. The economic impact of loss of markets is much greater than that from yield and quality reductions of the crop. USEFUL WEBSITES: http://doacs.state.fl.us/canker, http://www.apsnet.org/education/lessonsplantpath/citruscanker/top.htm, http://www.apsnet.org/online/feature/citruscanker/, http://www.plantmanagementnetwork.org/pub/php/review/citruscanker/, http://www.abecitrus.com.br/fundecitrus.html, http://www.biotech.ufl.edu/PlantContainment/canker.htm, http://www.aphis.usda.gov/oa/ccanker/.