Xylella: the greatest threat to Australian agriculture?

Keywords: biosecurity, climate change, devastating, economic impact, insect vectors, olive quick decline syndrome, sharp shooter, Xylella fastidiosa.

Xylella fastidiosa is a bacterial plant pathogen like no other and if not already could become one of the world’s most important bacterial plant pathogens in history. Distantly related to the more familiar Xanthomonas group of plant pathogens it was voted in the top ten most important plant pathogenic bacteria by the international community in 2012¹ and that was before it made the 4500 mile journey from America to Europe. It is now firmly established in Italy where it has become a major threat to the olive industry and there are numerous other well documented reports of it being elsewhere in Europe, namely: France, Spain, Germany, the Czech Republic, Kosovo and further afield in Israel, Taiwan, and Iran.²

Fig. 1.  Transmission electron micrograph; the cells of Xylella fastidiosa are clearly seen as dark bodies within the xylem vessel and lodged within the bordered pit (left) of an oak tree. Photo credit: Ulla Jarlfors, University of Kentucky, Bugwood.org.

Despite this recent surge in interest the pathogen is nothing new. The diseases it causes were originally studied by the world’s first professional plant pathologist Newton B. Pierce who stated that he was going to work on the problem (originally called Anaheim disease after the town in California where it was first observed) and not move onto any other disease until he had cracked it.³ This pathogen was a particularly poor choice for Pierce’s career: unlike almost every other plant pathogenic bacterium it cannot be directly inoculated from one plant to another and as it requires extremely exacting culture media, it was first cultured in the early 1980s and was awarded the name Xylella fastidiosa in 1987.^4,5

X. fastidiosa proliferates only in xylem vessels, of roots, stems and leaves (Fig. 1). The vessels are ultimately blocked by bacterial aggregates and by tyloses and gums formed by the plant, although disease induction may not be due simply to water blockage.⁶ It appears to be able to move against the transpiration stream moving down into the roots as well as up into the leaves in many hosts whereas in others it will multiply but not leave the site of infection.⁷ These findings have considerable implications for plants where grafting between scions and rootstocks is commonplace.

Over a century since Pierce’s death we still have not ‘cracked it’, and it is cruel irony that one of the most environmentally important, but least understood plant diseases, bears his name; ‘Pierce’s disease of grapevine’.

However, Pierce’s disease is not the only named disease caused by X. fastidiosa. Using molecular means, the species has been split into at least five subspecies, which have evolved in distinct geographical regions:⁸

1. X. fastidiosa subsp. fastidiosa, thought to be native to southern Central America,⁹ is associated primarily with Pierce’s disease of grapevines and almond leaf scorch.

2. X. fastidiosa subsp. multiplex, thought to be native to temperate and subtropical North America, is associated with scorch disease in a wide range of trees, including phony peach disease and plum leaf scorch.¹⁰

3. X. fastidiosa subsp. pauca, thought to be native to South America, is associated with strains causing disease in citrus and coffee.¹¹

4. X. fastidiosa subsp. sandyi, believed to originate from the southern region of the USA, is associated with oleander leaf scorch.¹²

5. X. fastidiosa subsp. taiwanensis believe to be isolated in Taiwan and is mostly affecting pear trees.¹³

The cases of X. fastidiosa within Europe are not all of one subspecies, which strongly indicates several recent introductions rather than one introduction followed by subsequent spread within Europe especially so as there is considerable specificity between sub-species and vector.^8,14

Unlike almost all other bacterial plant pathogens X. fastidiosa requires an insect vector to transmit the disease in a manner analogous to many insect vectored viruses. The glassy-winged sharpshooter, Homalodisca vitripennis (Fig. 2) is the most common vector of Pierce’s disease of grapevine but this species is only found in North America and other xylem-feeding insects including froghoppers and spittlebugs are vectors of other subspecies in other regions.¹⁵

Fig. 2.  Glassy winged sharpshooter (Homalodisca vitripennis), a Californian vector of Pierce’s disease of grapevine. Photo credit: Johnny N. Dell, Bugwood.org.

On arrival in a new region it is difficult to predict which potential vectors (which will never have encountered the bacterium previously) will spread the recently arrived subspecies. Additionally, the spectre of climate change which may increase the range of potential vectors make predictions as to the pathogen spread very difficult. Bosso et al. using modelling methods, predicts that the disease could spread much further than its current location in Italy.¹⁶

The success of X. fastidiosa is reflected in its host range. Many hosts are woody trees and bushes both ornamental and fruit crops. However, other hosts include fodder crops (clover, lucerne and ryegrass), vegetable crops such as brassicas, herbs (e.g. rosemary) and weeds such as dandelion, wild oat and chickweed.²

Due to continued observation in the field and laboratory research the number of recorded hosts is rising on an almost weekly basis, 11 new species were added to the list of susceptible hosts between May 2021 and the end of that year taking the total number of hosts to 664 plant species, 299 genera and 88 families.¹⁷

What makes the long range spread of X. fastidiosa particularly insidious is that many hosts are asymptomatic. Perfectly ‘healthy’ plants could be imported in good faith while bringing the pathogen into a new area. The tests for Xylella are not cheap and often it is not feasible to test every plant.¹⁸ To avoid testing, hot water treatment to kill the pathogen has been used in some cases.

The most well documented attempts to contain spread within a region is that of the outbreak in Italy. Believed to have arrived on coffee plants in 2008 the pathogen has wiped out vast swathes of olives.¹⁹ In desperate attempts to save their trees farmers have come up with their own control measures: sprays containing zinc, copper and citric acid are claimed to reduce the severity of the disease,²⁰ but these claims are disputed by the scientific community.²¹ The only effective way to limit spread of the disease is through vector control, coupled with a cordon sanitaire whereby all known hosts of the pathogen are removed around the affected area – something not easy due to the vast host range. Despite the best efforts of the Italian authorities the pathogen is spreading at approximately 10 km per year.²²

Each of the subspecies causes different symptoms on their respective hosts; however, the most familiar and dramatic symptom is leaf scorch. On grapes particularly, an early sign is sudden drying of part of a green leaf, which then turns brown while adjacent tissues turn yellow or red reminiscent of an autumnal display (Fig. 3). The desiccation spreads and the whole leaf may shrivel and drop, leaving only the petiole attached. Once infected, grapevines rarely survive more than 2–3 years.²³

Fig. 3.  Appearance of grapevine leaf affected by Xylella fastidiosa. Photo credit: John Hartman, University of Kentucky, Bugwood.org.

The disease of citrus takes a different course; initially trees show interveinal chlorosis on young leaves as they mature. This variegation spreads throughout the canopy and to mature leaves with time. As the leaves mature, small, light-brown, slightly raised gummy lesions (becoming dark-brown or even necrotic) appear on the underside, directly opposite the yellow chlorotic areas on the upper side. Affected trees show stunting and slow growth rate; twigs and branches die back and the canopy thins, but affected trees do not die.²⁴ Timing of blossom and fruit set are unaffected, but natural fruit thinning does not occur. Therefore, on infected trees the fruits remain small; however, as more fruits remain on the tree, total production is not hugely reduced.

The threat to Australian native flora and crops is significant. Hafi et al. make the point that the economic impact would depend on which subspecies arrived²⁵ (the arrival of X. fastidiosa subsp. fastidiosa would be by far the most economically damaging subspecies but in combination with other subspecies the situation would be worse).

Crops under threat include high value Australian horticultural crops; avocados, citrus, grapes, nuts, olives and stone fruits are all susceptible. Together these crops contribute to around 9% of the Australia’s total agricultural GVP.²⁶ The effects on the downstream processing industries would also be significant. Victoria and South Australia would suffer the greatest economic losses were the pathogen to become established.

The pathogen affects amenity trees and shrubs, native Australian shrubs are affected in North America and North American and European amenity trees common in Australia are similarly affected.

The Department of Agriculture, Fisheries and Forestry has estimated that if a single subspecies were to establish in Australia it would cost between $1.2 billion and $8.9 billion in 2017–18 over 50 years at a 3% discount rate, and of course more if multiple subspecies established.²⁵

Departments of Agriculture from all over the world are deeply troubled by this relatively new threat of an old pathogen, as can be seen by the size of the conferences dedicated to this pathogen. In 2015, 100 plant health specialists met in Brussels, whereas in April 2021, 900 interested stakeholders from more than 60 countries met online to discuss this threat to world agriculture.²⁷ Australia has world class biosecurity and is taking the threat very seriously. In 2019, the Department of Agriculture, Fisheries and Forestry produced the National Xylella Action Plan, detailing prevention, detection, response, cross-cutting issues such as coordination of stakeholders.²⁸ In addition to this document the Inspector-General of Biosecurity commissioned a document on the effectiveness of the biosecurity arrangements already in place.²⁹ While the threat is real, no other country is doing more to prevent the arrival of this pest or deal with it should it arrive.

It is ironic that after all this time, the first pathogen studied by the first professional plant pathologist is still causing the world the most headaches.

Data sharing is not applicable as no new data were generated or analysed during this study.

The author declares that he has no conflicts of interest.

This research did not receive any specific funding.