XYLELLA FASTIDIOSA DISEASES IN EUROPE: NEW ENCOUNTERS

 di ALEXANDER PURCELL

 

 

The olives trees near Speccia, Italy are dead or have symptoms of Olive Quick Decline Syndrome, 2020. (Photo by Donato Boschia, with permission.)

The current epidemic of a lethal disease of olive, Olive Quick Decline Syndrome (OQDS) was first noted scientifically in 2013 near Gallipoli, Italy and continues to expand northward in Puglia¹. The disease is clearly the result of a “new (recent) encounter” between olive, a plant species native to the Mediterranean basin and a bacterium, Xylella fastidiosa subspecies pauca, which is probably native to South or Central America. Xylella fastidiosa causes a variety of diseases. I will use as a common term the non-italicized name “xylella” to indicate any genotype within the bacterial genus Xylella, although currently in Europe only the species Xylella fastidiosa has been detected. Xylellas cause significant diseases in grapevines, citrus, almond, peach, alfalfa, pecan, numerous oak species (Quercus spp.), elm, oleander, and numerous other forest or uncultivated plant species²^,³. All of these diseases can be explained as “new encounters” in an ecological and evolutionary sense. In other words, both the parasite and the plant had ever encountered each other. Although we are most interested in the diseases that Xylella causes, we should remember that xylellas can infect most plant species without causing noticeable symptoms⁴^,⁸. Disease is a much less common outcome from these “new encounters”, but the diseases resulting from new encounters can cause economic or ecological disasters. The histories and epidemiological characteristics of such diseases caused by X. fastidiosa can give an overview of what measures might be applied to manage the expanding problems caused by X. fastidiosa in Italy and Europe. What measures can we take to avoid future invasions by different strains of this bacterium?

Environmental requirements for endemic populations of X. fastidiosa

Xylellas in plants are restricted to the host plant’s xylem - a system of cells that transport water from the roots to tissues throughout the plant. Xylem sap has a relatively simple chemical profile compared to other plant fluids. It is mostly water containing dilute solutions of chemicals. The main nutrients for xylem sap-feeders are amino acids, organic acids, along with dissolved minerals and trace amounts of proteins, sugars and other organic molecules^9-10. Special microbes that only inhabit xylem are not commonly found in most plants, but this view may be incorrect because we direct most of our microbial investigations of xylem emphasize microbes that cause disease.  

 

An insect vector (bottom) acquires the bacterium Xylella fastidiosa from infected plants, then transmits the bacterium (upper right) to other plants. Most plant species have few bacteria and no symptoms when infected. But some plants, as shown by the oleander plant with leaf scorch symptoms (similar to symptoms seen in olive leaves) develop disease symptoms. (Photo by Rodrigo Krugner with permission)

The “disease triangle” of pathogen-plant-environment serves as a classic model for plant disease epidemiology. For disease caused by X. fastidiosa, the “environment” factor includes the insect vectors required to move this pathogenic bacterium from plant to plant. Infection alone is not the same as disease and does not inevitably lead to disease, as X. fastidiosa subsp. fastidiosa illustrates very well¹¹. As already mentioned, X. fastidiosa usually does not cause observable symptoms in the majority of the plant species that it infects. In addition, many infected but symptomless plants recover from infection over time for unknown reasons^6-8. Some infections disappeared from grapevines either without or after symptoms appeared after freezing exposures in a laboratory setting¹¹ or outdoors during winter^12-13. The severity of winter subfreezing temperatures seems to coincide with the incidence of Pierce’s disease in North America, suggesting that winter freezing temperature regimes limit the geographical range of Pierce’s disease of grapevines^12-14. Either the appearance of disease symptoms associated with diseases caused by xylellas or by detection methods for this bacterium have rarely occurred in severe winter areas. For example, molecular testing of elms with marginal leaf necrosis (leaf scorch) in southern Ontario, Canada detected X. fastidiosa in 3 of 114 trees¹⁵, suggesting that this disease occurred but was rare in this cold winter region. The resistance or tolerance of all wild grape species indigenous to the southeastern United States led Hewitt¹⁶ to conclude that this region of the USA was the probable region of origin for Pierce’s disease brought to California on wild grapes from the southeastern states for use as rootstocks.
Phony peach disease, caused by X. fastidiosa subsp. multiplex, is another example that supports the hypothesis that winter cold severity limited outdoor transmission tests with insect vectors and also represents a new encounter disease. In the case of phony peach disease, both the peach (Asian origin) and the xylella genotype (as inferred from is first observance and consequent spread) were exotic to where they first occurred. Outdoor vector transmission experiments in Chattanooga, Tennessee were inconclusive because of the lack of expected symptoms, but similar outdoor cage tests later conducted in Georgia succeeded in transmission¹⁷, which is consistent with winter climate limiting the winter survival of X. fastidiosa, symptom expression, or both. Peach is an introduced plant in North America, and was well established by the mid-1800s. The first record of phony disease was in central Georgia in about 1885, afterwards expanding from this initial sighting until it stabilized in the early 1930s¹⁸ at its current geographic distribution¹⁸. The documented spread of phony disease has all the features expected of a new encounter disease. The stabilization of the geographic limits of the disease in the 1930s with little change since further supports the hypothesis that winter cold severity is a limiting factor as to where the disease can be endemic. 

 

Maps of the estimated distributions of phony disease of peach in 1928 (top) and 1933. (From Hutchins, 1935.)

Final distribution of phony peach disease (Xylella fastidiosa subsp. multiplex) in the southeastern United States, circa 1950 (17). The darkest areas have the warmest winters. Southern parts of Florida and Louisiana had no peach trees. The current distribution of the disease is approximately the same 70 years later.

The information about the geographical distribution of phony disease of peach proved to be very comparable to the geographic limits of Pierces disease (PD). In 1989 I (A. Purcell) presented a talk at a viticulture conference held in Budapest on the potential of PD to invade Europe. I presented (but never published) a map of the United States that showed the approximate areas of where PD was severe (commercial viticulture with European grapes was impossible), moderate (always present at low to moderate levels but occasionally severe increases), rare (not consistently detectable) or absent. Superimposed on the same map were isotherms of the average of minimum January temperatures, based on National Weather Service data over the preceding 50 years. The isotherms were drawn by hand interpolation of tabular temperature data. Of all the criteria that I evaluated, the average minimum January temperature was the best fit to the geographic distribution of PD. Today, temperature data is much more widely available and downloadable from the Internet, and I am sure that I would evaluate different temperature criteria, for example, number of hours (or day-degrees) below 0oC from December to February. My estimates of where the same isotherms based on climatic maps (US Navy data) occurred in Europe predicted that temperature could be limiting in Central and Northern Europe. The intention for my presentation was to point out that temperature was not a limiting factor for the establishment of PD in Mediterranean Europe and North Africa. Of course the kinds and abundance of insect vectors, as well as the crops and plant communities be major environmental influences of the occurrence and intensity of PD. Despite how unsophisticated these simple maps were, they have help up surprisingly well in corresponding to new discoveries of xylella diseases in Europe since 2013. 

 

 

(Left) Distribution of Pierce’s disease of grapevine based on mail surveys of all eastern states from Texas north to Canada. Black lines indicate isotherms of indicated temperatures, such as 4.5^oC.  Data on PD for Texas was is now available in greater detail. Redrawing the map today would require moving the colored areas about 100 to 200 km northward (climate warming?). See text for more details. (On right).  Map of Europe showing the same estimated isotherms as for the map of USA. Red arrows indicate discoveries of Xylella fastidiosa in Europe from 2013 (Italy) to 2019. Both maps were previously unpublished but presented at numerous conferences and meetings since 1989 by A. H. Purcell. Map of Europe previously published (Sforza and Purcell, 2002, Phytoma La Défense des Végétaux 550:10-14.)

 

 

Genetic variability is a common and an important feature of X. fastidiosa

The genetic differences among the species and subspecies of the genus Xylella vary enormously as to what host plants develop disease. Subspecies of X. fastidiosa are delineated according to the similarity of DNA sequences in their genomes¹⁹. One of the first examples to document some effects of genetic variability on plant disease expression showed that a genetic grouping of isolates of X. fastidiosa subsp. fastidiosa from diseased grape and almond plants all caused disease in grape, but none of the genetically grouped isolates of the bacterium included in the subspecies multiplex from almond caused disease in grape. All the isolates from two almond genetic groupings infected grapes without causing symptoms²⁰. The genetic uniformity of isolates of X. fastidiosa subspecies (subsp.) pauca from olive with OQDS, as well as disease in other plants hosts³, supports the hypothesis that a single introduction of one genotype of X. fastidiosa triggered the current OQDS epidemic in olive trees in Puglia. Slightly different genotypes in the same subspecies pauca cause disease in orange and coffee in Brazil, but the genotype that causes OQDS in Italy does not infect citrus or grape²¹. Experiments in Brazil showed that very closely related genotypes of X. fastidiosa from diseased coffee neither infect nor cause disease in orange; genotypes that cause disease in orange do not infect coffee²². In summary, small changes in the genomes of X. fastidiosa can cause major differences in the range of plant species that the bacterium can infect and which plant species develop disease symptoms.  

Other examples of new encounters

Plants introduced by Europeans in their colonization of the Americas often produced larger crops than they produced in Europe because they were not accompanied by diseases and pests native to Europe or Asia, but other imported crops did not survive in their new environment. One notable example of an introduced crop plant from the Old World (Eurasia) encountering a native pathogen in the New World (Western Hemisphere) is that of Xylella fastidiosa and the commercial grape of Eurasia, Vitis vinifera. 

X. fastidiosa continues to be one of the most serious obstacles to the cultivation of vinifera grapes in areas of North and Central America with mild winter climates. Early European colonists of North America saw their new plantings of grapevines wither and die within one to three years. We now know that Pierce’s disease of grapevines was a major cause of collapses of grape plantings¹⁶, and Pierce’s disease still precludes the commercial culture of vinifera grapes in regions in North America such as all of Florida and areas within a few hundred kilometers of the Gulf of Mexico or the south Atlantic ocean, where climatic conditions are favorable for X. fastidiosa². Only during the 1970s did scientists discover that a previously undescribed bacterium that is now known as Xylella fastidiosa, caused Pierce’s disease²³, until then a virus had been presumed to cause Pierce’s disease^11-16. The profusion of native species of grape vines in North America was noted by the early European colonists, but they did not consider that the healthy condition of wild grapes in North and Central America might be related to the problems in growing vinifera grapes in North America. We now know that this healthy condition is due to their resistance and or tolerance to X. fastidiosa¹⁶. 

Wherever vinifera grapevines failed in the New World, a native pest or pathogen was responsible for these losses. Although Central Asia was most likely the ancestral home of V. vinifera, the number of Vitis species that are native to the Americas is nearly as great as the number native to Asia. Following the emergence of the scientific germ theory of disease in the middle of the 19th century, scientists gradually adopted the ideas that microorganisms such as bacteria (and decades later, viruses) could cause disease not only in humans and animals, but also plants. It is tempting to speculate scientifically that the interactions of the many viruses, bacteria, fungi, nematodes, and insect parasites of Vitis species native to the Americas promoted a diversity of grapevine species resistant to the most serious diseases and pests of Vitis vinifera: Exotic pathogens and an insect pest, all accidentally introduced from North America, posed the greatest threats to European viticulture: powdery mildew (fungus - Erysiphe necator , 1845 first noticed), downy mildew (fungus - Plasmopara viticola, 1834 first noticed in North America, later spread to France), and phylloxera (insect -Daktulosphaira vitifoliae, 1860s first noticed in France). The management of all of these three parasites continues to be a high priority for grape growers²⁴. Because grapevines are the obligate hosts of all of these devastating parasites of the grapevine, we can assume that they were introduced along with the importation of wild grape species from North America, most probably imported for botanical collections. Since first appearing in Europe, these pests have spread worldwide wherever vinifera grapes are grown commercially. Some practical management solutions involve using the genetic resources of wild grape species to minimize the damage of fungal pathogens by breeding hybrids of vinifera grapes crossed with wild species from the Americas. Some of these hybrids used for brandies (grappa, cognac, etc.) were resistant to mildew diseases, avoiding the need for fungicide treatments²⁵. These hybrids, however, had limited commercial success for wines. Wild grapes or their hybrids with other wild grapevines are used as rootstocks to avoid the lethal root damage caused by grape phylloxera that invaded Europe from North America. Unfortunately, using rootstocks increased the spread of grapevine viruses carried in the symptomless wild species used as rootstocks that tolerated these viruses²⁶.

We should not forget that some of intentional plant importations from the Americas produced huge economic and cultural benefits: potato, tomato, corn, and beans are examples. Newly introduced pests or pathogens typically attain much higher populations than in their region of origin because co-evolved natural enemies did not accompany the introduced crops. In cases where diseases and pests of these crop plants accompanied the original importations of their plant hosts or later were accidentally introduced, the imported pests caused more damage than in their region of origin. To correct this imbalance, searches for natural enemies or antagonists that co-evolved with their plant hosts may reveal candidates for biological control to reduce the pest populations to manageable levels²⁷. However, some well-meaning importations of natural enemies caused even more problems than those caused by the targeted pest. So great care must be taken to screen candidate biological control agents for their damaging other, non-targeted organisms²⁷. 

The growing numbers of invasive organisms are severe problems not just for agriculture but also for humans and animals and for ecosystems. The pace of accidental introductions of exotic pathogens and pests are accelerating. Fortunately, most accidental introductions of exotic organisms do not establish, but some invaders attain noticeably high populations and cause economic or ecological upsets²⁸. Preventing introductions of different xylella genotypes should be a high priority for all countries. Recent conferences in Australia²⁹ and New Zealand addressed the question of how to exclude xylellas from becoming established in their territories. Quarantines are at the top of the list for preventing invasions of xylellas. Also near the top of the list should be emergency action plans to eradicate introductions of novel genotypes. Eradication of invasive bacterial pathogens such as X. fastidiosa only have a chance to succeed when implemented very soon after they are detected. This was not the case for the detected outbreak in Puglia, where the extensive spread of OQDS and diseases of other plants like almond and oleander caused by the same Xylella made eradication impossible. Efforts now are concentrated on slowing the spread of X. fastidiosa further northward in Italy³⁰.

Insect vectors of X. fastidiosa

Sucking insects that specialize in feeding on xylem sap should be considered as potential vectors of X. fastidiosa³¹⁰. Europe is fortunate in having only one native species (Cicadella viridis) in a subfamily (Cicadellinae) of leafhoppers (family Cicadellidae) that specialize in feeding on xylem sap. A few other species of leafhoppers in this subfamily of xylem sap-feeders invaded Europe accidentally from North America, probably as eggs embedded within imported plants or as nymphs on live plants. Fortunately, these invasive sharpshooters have not been found feeding on plant species so far shown to be disease hosts of X. fastidiosa. Some species in other insect families of xylem sap-feeding insects are common and often abundant in Europe. All spittlebug species (superfamily Cercopoidea) specialize in feeding on xylem sap, and all tested species have proven to be X. fastidiosa vectors³¹. 

 

 

 

A mating pair of the spittlebug Philaenus spumarius on oleander. The color patterns of this species are very variable. (Photo by author.) A mass of foam surrounds the immature spittlebug on this vetch plant (Vicia sativa) [note to editor: You could crop the photograph of the spittle mass and combine with the photo of the mating pair of adult spittlebugs, as best fits your needs.]

The European species of spittlebug Philaenus spumarius is the most important vector for spreading OQDS in olives in the Salento region of Puglia in Italy
^32-33. In the region severely affected by OQDS P. spumarius can be extremely abundant in weeds in olive orchards; from 10 to over 100 nymphs of P. spumarius per square meter would not be unusual. Adults move to olive trees after weeds decline in summer dry periods (May-August), and over 50% of the spittlebugs collected from olive trees tested positive for the presence of X. fastidiosa in late summer or autumn³². The lowest number of bacteria required for the insect to infect a plant by feeding is below the limit for detection tests (typically about 100 bacteria per sampled head), so actual percentage of infective spittlebugs can be even higher than estimated by the most sensitive methods^35-36. P. spumarius transmits to olive in lab tests within the range of about 5 to 15% per insect per day. Without complicated math, you can easily imagine the difficulty of protecting large trees for many years from a single infection by an infectious spittlebug. At least a few spittlebugs will survive insecticide treatments, and others may fly in from adjacent untreated areas.
In all Mediterranean regions, many millions of spittlebugs every year for centuries have fed on olives with no significant adverse effects on olive production. But the introduction of a genotype of X. fastidiosa that can infect and kill an olive tree radically changed the status of P. spumarius³⁶. Reducing the number of spittlebugs capable of transmitting X. fastidiosa to a very low number should be the objective of methods to reduce the chance of infecting a tree. The exponential rate at which OQDS spreads within an olive orchard point to olive as the main source from which spittlebugs acquire X. fastidiosa. The CVC disease in Brazilian citrus has the same exponential spread, and the regular inspection of citrus orchards followed by removing symptomatic trees greatly reduces the spread of CVC³⁷. The similarities between CVC and OQDS reinforces the logical conclusion that removing diseased trees is an essential part of slowing the spread of OQDS. However, the pruning methods for control of CVC in Brazilian citrus does not offer much hope that pruning alone will be of benefit to reduce the spread of OQDS. In summary, a combination of control techniques against the vector and the rapid removal of infected trees has the best chance of slowing the spread of OQDS. The most effective remedy for managing OQDS will be OQDS-resistant varieties or effective new preventive or curative treatment methods that may be developed in the future.
Invasive insect vectors of X. fastidiosa pose anther threat to European agriculture and forests. The tropical and subtropical Americas have a huge diversity of xylem sap-feeders, both spittlebugs and sharpshooter leafhoppers. Most leafhoppers insert their eggs into plant tissues; spittlebugs commonly glue their eggs to living or dead plants but also soil. Importing plants that have vectors’ eggs provides an entry to invade new territories. The sharpshooter Homalodisca vitripennis (glassy-winged sharpshooter) caused a major panic for wine grape growers in southern California after 1998³⁸. This insect is native to the southeastern United states and northeast Mexico but was not seen in California until the early 1990s. Until then, Pierce’s disease of gape was a minor problem except for a few vineyards located near habitats of native sharpshooters. The Temecula Valley is a patchwork of its two major crops: citrus and grapes. This set the scene for a major problem with Pierce’s disease when the glassy-winged sharpshooter entered Temecula Valley and began to increase to very high populations in citrus groves then moved to nearby vineyards in spring months³⁹. The exponential increase in Pierce’s disease eliminated some vineyards within three years.

 

This Temecula Valley vineyard was lost to Pierce’s disease 3 years after appearance of the sharpshooter leafhopper, Homaladisa vitripennis. Adjacent to the vineyard is a citrus grove (upper right) that harbors this insect while grapevines are dormant. (Photo by author.)

Adult glassy-winged sharpshooter, Homalodisca vitripennis. [Editor: I suggest putting the photo of the adult Homalodisca as an inset at an upper part of the photo of the barren vineyard.]

The severity of this new problem with Pierces disease in Temecula Valley alerted all California grape growers as well as farmers in other crops like almonds that were also sensitive to diseases caused by to the new threat created by the invasion of glassy-winged sharpshooter. Beginning in 2000, grower organizations, along with the state and federal departments of agriculture, coordinated responses to control Pierce’s disease in Temecula by treating citrus just prior to grapes producing new foliage. A federal agency (APHIS) provided funding the insecticide applications. The citrus growers did not have to pay for the insecticide treatments, but the treatments complicated and raised the costs of controlling citrus pests by methods that minimized insecticide use. This was a generous move by citrus farmers to help their neighbors. Combinations of grape grower mandatory assessments and state and federal funding supported over five million dollars per year for research to develop control methods to prevent and cure Pierce’s disease. These research efforts have begun to produce results that will begin to return profits from these investments (2014). New grape varieties resistant to Pierce’s disease have are beginning to be released⁴⁰.

Needs for more knowledge of the genetic diversity of xylellas

Analyzing examples from diseases caused by xylellas provides some ideas on how to avoid further invasions by their many genetic variants (genotypes). We should expect that Olive Quick Decline Syndrome will not be the last new disease to suddenly appear because of a new combination of a unique xylella genotype and a different plant host. Pierce’s disease was been reported to occur in Kosovo in in the 1990s⁴¹, but only in 2018 was it found in Mallorca⁴². The eventual appearance of Pierce’s disease in Europe was considered to be inevitable and required advance plans to deal with it when it became established in new regions⁴³. Better management of OQDS would have benefitted from planning in advance to detect new xylella diseases early and to begin control measures. This will have to be adapted not only to different countries but to different regions within countries.
The current pandemic of the COVID-19 virus is best explained as an invasion of the COVID-19 virus originating from an animal source in China⁴⁴. Animal viruses are quite diverse in wild and domestic animals. Some of these viruses are the origins of “new encounters” for human virus diseases like COVID-19. Virologists search wild animals for as yet undescribed viruses that may be transmissible from human to human. This enables advance research on viruses that may become a problem in humans or domestic animals. By analogy, why don’t we do this for xylellas? Central America appears to be the “El Dorado” (the fabled city of gold sought by early Spanish explorers of the Americas) of xylellas, based on this region’s high diversity and common presence of X. fastidiosa *. Because of quarantine restrictions, research on most xylella genotypes can only be done with live bacteria in regions in which a particular genotype has been proven to occur. Two locations have both the likelihood that they have a variety of unknown xylella genotypes embedded in their territory and the scientific facilities to accommodate the needed research. Brazil hosts genotypes within the subspecies pauca, while Costa Rica harbors genotypes grouped in the subspecies fastidiosa, multiplex, and pauca. Costa Rica and Brazil are suitable choices for searches to identify genetic diversity in X. fastidiosa and evaluate the impacts of diverse xylella genotypes on plants of economic or ecological concerns. Both Costa Rica and Brazil are adjacent to other countries that may be accessible for shared research. The costs of this kind of research need not be expensive relative to the value of investing in gaining knowledge of potential threats of possible “new encounters” of now unknown genotypes that inhabit the American tropics. For example, experimental plantings of kiwi fruit plants in a variety of locations in Central and South America might reveal a Xylella genotype that causes disease in kiwi.
We should expect that locations with a high diversity of Xylella genotypes and also a great diversity of plant and vector species would also harbor a diversity of other microbes that can be antagonists to X. fastidiosa. Research with microbial antagonists have the potential to manage Pierce’s disease of grape with bacteriophages (viruses of bacteria)⁴⁵ or other bacteria that inhabit xylem and aid infected plants in recovering from xylella infections before causing disease⁴⁶ . Science has so far concentrated on bacteria associated with plant disease, so our scientific knowledge of the microbiota of xylem is shamefully sparse. Some unpredictable findings from basic searches may have the potential to develop into methods to prevent or manage the “new encounter diseases” caused by xylellas.

 

 

L'articolo è uscito in origine per "I TEMPI DELLA TERRA"

REFERENCES

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12.        Purcell, AH.1977. Cold therapy of Pierce's disease of grapevines. Plant Disease

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14.        Lieth, J. H., M. M. Meyer,   K.-H.Yeo, and , B. C. Kirkpatrick. 2011. Modeling cold curing of Pierce’s disease in Vitis vinifera ‘Pinot Noir’ and ‘Cabernet Sauvignon’ grapevines in California. Phytopathology 101: 1492-1500.

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17.        Turner, W. F. and H. N. Pollard. 1959. Insect transmission of phony peach disease. U.S. Dept. Agric. Tech. Bull. 1193:1–27.

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21.        Saponari, M., Loconsole, G., Cornara, D., Yokomi, R. K., Stradis, A., Boscia, D., Bosco, D., Martelli, G. P., Krugner, R., and Porcelli, F. 2014. Infectivity and transmission of Xylella fastidiosa by Philaenus spumarius (Hemiptera: Aphrophoridae) in Apulia, Italy. J. Econ. Entomol. 107:1316-1319.

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29.        International Symposium on Xylella fastidiosa. 2017. Brisbane Australia. https://www.agriculture.gov.au/pests-diseases-weeds/plant/xylella/international-symposium-xylella-fastidiosa  [videos of the symposium presentations on X. fastidiosa are available on Internet.]

30.        European Union web site for Xylella: https://ec.europa.eu/food/plant/plant_health_biosecurity/legislation/emergency_measures/xylella-fastidiosa/latest-developments_en

31.        Redak R., A. H. Purcell, J. R. S. Lopes, M. Blua, R. F. Mizell, and P. C. Andersen. 2004. The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annu. Rev. Entomol. 49: 243–270.

32.        Saponari, M., G. Loconsole, D. Cornara, R. K. Yokomi, and A. De Stradis. 2014. Infectivity and Transmission of Xylella fastidiosa by Philaenus spumarius (Hemiptera: Aphrophoridae) in Apulia, Italy. J. Econ. Entomol. 107:1316-1319.

33.        Cornara, D., D. Bosco, and A. Fereres. 2018. Philaenus spumarius: when an old acquaintance becomes a new threat to European agriculture. J. Pest Sci. 91:957–972.

34.        Roberto, S. R., P. R. S. Farias, A. B. Filho. 2002. Geostical analysis of spatial dynamics of citrus variegated chlorossis [sic]. Fitopatol. Bras. Vol. 27  http://dx.doi.org/10.1590/S0100-41582002000600007 

35.        Hill, B. L. and A. H. Purcell. 199. Populations of Xylella fastidiosa in plants required for transmission by an efficient vector. Phytopathology 87:1197–201. 


36.        Cornara, D., A. Sicard, A. R. Zeilinger, F. Porcelli, A. H. Purcell and R. P. P. Almeida. 20. Transmission of Xylella fastidiosa to grapevine by the meadow spittlebug. Phytopathology 106:1285-1290.

37.        Lopes, S. A. 2019. Scion Substitution: A new strategy to control citrus variegated chlorosis disease. Plant Dis. 104:

38.        Dauherty, M. 2014. History and Status of the Glassywinged Sharpshooter in California. UCNFA News https://ucanr.edu/sites/UCNFAnews/newsletters/Download_UCNFA_News_as_PDF53795.pdf   

39.        Perring, T. M., C. A. Farrar, M. J.  Blua. 2001. Glassy-winged sharpshooter host impacts Pierce's disease in Temecula Valley vineyards. Calif. Agric.

40.        Anonymous. 2020. Wine Industry Advisor (Internet). https://wineindustryadvisor.com/2020/06/02/pierces-disease-resistant-vines-now-reality [many Internet news releases on “Pierce’s disease resistant varieties”]

41.        Moralejo, E., D. Borràs, M. Gomila, M. Montesinos, F. Adrover, et al. 2018. Insights into the epidemiology of Pierce's disease in vineyards of Mallorca, Spain. Plant Pathol.  https://doi.org/10.1111/ppa.13076

42.        Berisha, B., Y.D. Chen, G.Y. Zhang, B.Y. Xu and T.A. Chen. 1998. Isolation of Pierce’s disease bacteria from grapevines in Europe. Eur. J. Plant Pathol. 104:427–433.
[symptoms of PD in cermjan region of Kosovo in mid-1990s.]

43.        Purcell, A. H. 1997. A regional problem or a world threat? J. Plant Pathol. 79: 99-105.

44.        Guo, Y.-R., Q.-D. Cao, Z.-S. Hong, et al. 2020. The origin, transmission and clinical therapies on coronavirus disease 2019 (COVID-19) outbreak – an update on the status. Military Medical Research vol. 7, Article 11.  https://link.springer.com/article/10.1186/s40779-020-00240-0  [available on Internet]

45.        Das, M., T. S. Bhowmick, S. Ahern, R. Young, and C. Gonzales. 2015. Control of Pierce’s disease by phage. PLOS One 10(6): e0128902. https://doi.org/10.1371/journal.pone.0128902

46.        Baccari, C., E. Antonova, and S. Lindow. 2015. Biological control of Pierce’s disease by an endophytic bacterium. Phytopathology Vol. 103  https://doi.org/10.1094/PHYTO-07-18-0245-FI

 

 

ALEXANDER H. PURCELL III
Professor Emeritus at the University of California-Berkeley for the Department of Environmental Science, Policy and Management. His interests are bacterial diseases of plants spread by insect vectors. Another interest is insect-bacteria interactions.