Necrotic rachis resulting from PSS. Image courtesy Adrian Utter   

By Dr Andrea Roberts-Davison

Background and favoured conditions

Pseudomonas syringae is a familiar global pathogen, with 57 pathovars responsible for symptoms from spots on foliage to blights, cankers and necrosis, on hundreds of different cultivated plants (Gerin et al., 2019). Of those pathovars, Pseudomonas syringae pv. syringae (PSS), distributed throughout Australia, is responsible for bacterial inflorescence rot (BIR) in grapevines, although it was originally isolated from lilac blight (Syringa vulgaris), and can cause disease in other species (S. J. Hall et al., 2019).

PSS, the cause of BIR, was once considered to be a weak pathogen, (Klingner et al., 1976), but along with other bacterial vine diseases like crown gall disease, is now being recognised as causing extensive financial losses to the Australian wine industry (Gerin et al., 2019; S. J. Hall et al., 2016; Whitelaw-Weckert et al., 2011). An increase in short but heavy rain events during spring, and frost events exacerbated by climate change, will likely enhance the spread of such pathogens. BIR was first documented in Australia in 2000, from the Adelaide Hills, SA (Hall et al., 2002), then much of the current research was undertaken on vines from Tumbarumba, NSW between 2006 and 2011 (Whitelaw-Weckert et al., 2011). There has been little research undertaken in recent years. BIR has since been reported in other cool-climate regions including the Yarra Valley and Mornington Peninsula, Victoria, and Tasmania (personal correspondence), some of which utilise overhead sprinkler systems for frost prevention, but others do not. Many different varieties are affected.

PSS is a motile bacterium that can exist on the surface of plant tissues and can travel systemically through the plant, in the vascular tissue, once forcibly accessed via the stomata (Hall et al., 2002; Hall, 2015; SHall et al., 2019; Whitelaw-Weckert et al., 2011). It needs moisture on the surface of the plant to spread and (in stone fruit) prefers temperatures between 19 and 25 °C (Wimalajeewa & Flett, 1985). So, any abiotic factors that increase the moisture on the surface of the leaves in spring and autumn (including rain events, heavy dews, frost, overhead sprinklers to prevent frost and perhaps even early season spraying) could potentially lead to increased incidence of infection. Nearly all the pathogenic and non-pathogenic strains of this bacterium have been demonstrated to produce a protein (IN – ice nucleating) that is frost nucleating (de Araujo et al., 2019), exacerbating the damage caused by frost events.

Symptoms of BIR caused by PSS (Figure 1), fist appear at flowering (approximately 60 days after bud burst) but foliar symptoms can appear shortly after budburst (especially following a frost) and include (Whitelaw-Weckert et al., 2011):

• Brown, longitudinal striations on shoots, rachises, petioles and veins of leaves (Figure 5)
• Necrotic rachises and abscission of up to 50% of inflorescences
• Initial small back spots on leaves with yellow halos
• Necrotic patches expand, become less regular in shape, bound by leaf veins
• Affected necrotic tissue dries and splits
• Leaf eventually senesced
• Drops of bacterial ooze sometimes visible near lesions

Diagnosis and spread

Currently confirmation of Pseudomonas syringae pv. syringae infection is slow, and it is easily mistaken for other pathogens like downy mildew (AWRI, 2023). According to Adrian Utter of E.E. Muir & Sons (personal communication), once symptoms are seen on the leaves of the vine then the infection is severe. There is evidence that disease severity increases in subsequent years if conditions are favourable (AWRI, 2023; Hall et al., 2016; Whitelaw-Weckert et al., 2011).

Early detection and diagnosis are essential to enable growers to mitigate the effects of PSS and prevent the spread, though options are limited. Currently in Victoria, fresh, aseptically collected samples of leaves, petioles, stems or necrotic inflorescences are sent to Crop Health Services, a division of Agriculture Victoria. An early indication, via PCR is possible in days, but to avoid false positives, culture plates are subjected to biochemical tests for confirmation. This can take between three and four weeks (CHS, 2024, personal communication), and the tests cost the same as other bacterial biosecurity tests (approximately $250 each). Faster detection, in the field, is possible using LAMP or qPCR technology, but this is unfortunately not yet available for BIR in Australia (Yang et al., 2023), though it is being developed for the detection of phylloxera.

With symptoms common to other pathogens, particularly downy mildew, BIR caused by PSS could be more widespread than is known. It is important for growers to be made aware of the threat that it poses, have a rapid way to detect it, and confirm that they have an infection in their vineyard, to be able to effectively mitigate it.

Mitigation

There are no viticultural agrichemicals registered for use in preventing or treating BIR caused by PSS in Australia (AWRI, 2023), although the use of copper, primarily as an antifungal agent for downy mildew, does seem to have some effect. Soil copper chelate drenches, post-harvest, maybe the most effective way to use copper to access the plant systemically (AWRI, 2023). However, although copper is an extensively used fungicide in agriculture, even permitted for use in organic farming systems, attitudes towards its use are changing. Copper itself is a non-degradable, heavy metal micronutrient, with low mobility, so it accumulates in soils and can leach into water systems (Ballabio et al., 2018; Cornu et al., 2022; MacKie et al., 2012). Excessive copper levels in soils maybe detrimental to human health, negatively impact the health of the soil microbiome and cause toxicity to the grapevines (Widmer & Norgrove, 2023). Copper resistant PSS has been long observed in mango (Cazorla et al., 2002) and cherry (Sundin, 1989), amongst many other agricultural plants. Although there have been anecdotal observations that PSS strains in some grapevines are becoming resistant, there is no current published research. More research is needed into how other agricultural sectors are dealing with copper resistance in managing PSS, and to find some innovative alternatives including biological control.

Conclusion

BIR caused by PSS can cause significant revenue loss to those affected, compounding year on year after the first infection, which is often mistaken for other pathogens. The extent of the spread is unknown, so growers may be at risk and unprepared to prevent and mitigate the disease. The climate is set to get hotter and drier, but increased heavy rain events during spring, coupled with frost risk, will likely increase the spread of bacterial vine diseases like BIR and crown gall. There are no licenced agrichemicals for the treatment of BIR in grapevines, with only unsustainable copper preparations showing any effectiveness, to which resistant strains maybe emerging.

Greater attention must be given to current and emerging bacterial vine diseases. Innovative and sustainable solutions, including biological control methods, are urgently needed to address these infections. While certain viticultural practices may offer some mitigation of disease spread, further research is essential to equip the industry to tackle the potentially significant financial losses that may arise in the future.

What growers need to know about BIR/PSS:

• What BIR is, what it looks like (compared to downy mildew and Phomopsis) and how they can confirm they have it quickly (they need a faster in-field diagnostic capacity)
• The exact conditions that favour a potentially bad year; exactly how much rain and when can cause the worst infections? Can the pathogen be spread post-flowering and cause major symptoms the following year? Is the pathogen knocked back in hot dry conditions?
• What to do if those conditions are forecast
• Are they unknowingly doing anything that is making the chance of major infection worse?
• What to do in the vineyard to prevent even worse infections in subsequent years, beyond common sense – what is most important if they must pick their battles?
• The best current ways to mitigate it including sprays and pruning practices etc.
• New, more sustainable ways to mitigate, especially for resistant strains. Can you ever get rid of it completely?
• What effect a major yield loss might have on the quality of the wine made from the remaining fruit
• Is it potentially harmful to other crops, livestock or humans?

Where do we start?

How widespread is bacterial inflorescence rot, caused by PSS? Initially, this is the most important question to answer. A survey has been produced (link below) that will give the first indication of grower awareness, the spread (either from confirmed or suspected cases), and the associated loss in yield/revenue. This, followed by the development of some LAMP or qPCR technology to rapidly diagnose the disease in the field, will paint the best picture of where this pathogen is currently, the speed it is spreading and the financial impact to the industry. Funding is required for the development of this technology.

The survey will also include several questions about current vineyard practices in general and those being employed to try and mitigate or prevent infections by PSS and other bacterial vine diseases. These questions will be used to look for patterns in the data that link management to disease, or indeed, disease prevention. It will also highlight the current, most effective forms of mitigation or prevention, so that best practice can be shared, and further research can be directed in ways that are most helpful to growers.

Beyond the survey, funding for more grass-roots research is needed to provide answers to the questions in the section above. Most importantly, innovative and more sustainable ways to mitigate BIR and other bacterial vine diseases need to be researched, including biological control. When faced with a changing climate and rapidly adapting pathogens, action is needed now to prevent potential devastating losses in the future.

You can access the anonymous survey here: https://qualtricsxmwhbsr5qs6.qualtrics.com/jfe/form/SV_eb2YQs827NCQHqu

Please direct any questions to [email protected]

References

AWRI. (2023, April). Recognizing and Understanding Bacterial Inflorescence Rot – Fact Sheet. Australian Wine Research Institute.

Ballabio, C., Panagos, P., Lugato, E., Huang, J. H., Orgiazzi, A., Jones, A., Fernández-Ugalde, O., Borrelli, P., & Montanarella, L. (2018). Copper distribution in European topsoils: An assessment based on LUCAS soil survey. Science of the Total Environment, 636. https://doi.org/10.1016/j.scitotenv.2018.04.268

Cazorla, F. M., Arrebola, E., Sesma, A., Pérez-García, A., Codina, J. C., Murillo, J., & De Vicente, A. (2002). Copper resistance in Pseudomonas syringae strains isolated from mango is encoded mainly by plasmids. Phytopathology, 92(8). https://doi.org/10.1094/PHYTO.2002.92.8.909

Cornu, J. Y., Waterlot, C., & Lebeau, T. (2022). Advantages and limits to copper phytoextraction in vineyards. Environmental Science and Pollution Research, 29(20). https://doi.org/10.1007/s11356-021-13450-3

de Araujo, G. G., Rodrigues, F., Gonçalves, F. L. T., & Galante, D. (2019). Survival and ice nucleation activity of Pseudomonas syringae strains exposed to simulated high-altitude atmospheric conditions. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-44283-3

Gerin, D., Cariddi, C., de Miccolis Angelini, R. M., Rotolo, C., Dongiovanni, C., Faretra, F., & Pollastro, S. (2019). First report of pseudomonas grapevine bunch rot caused by pseudomonas syringae pv. syringae. Plant Disease, 103(8). https://doi.org/10.1094/PDIS-11-18-1992-RE

Hall, B. H., McMahon, R. L., Noble, D., Cother, E. J., & McLintock, D. (2002). First report of Pseudomonas syringae on grapevines (Vitis vinifera) in South Australia. Australasian Plant Pathology, 31(4). https://doi.org/10.1071/AP02048

Hall, S. (2015). Effects of the Plant Pathogen Pseudomonas Syringae on Vitis Vinifera. Charles Sturt University.

Hall, S. J., Dry, I. B., Blanchard, C. L., & Whitelaw-Weckert, M. A. (2016). Phylogenetic relationships of Pseudomonas syringae pv. Syringae isolates associated with bacterial inflorescence rot in Grapevine. Plant Disease, 100(3). https://doi.org/10.1094/PDIS-07-15-0806-RE

Hall, S. J., Dry, I. B., Gopurenko, D., & Whitelaw-Weckert, M. A. (2019). Pseudomonas syringae pv. syringae from cool climate Australian grapevine vineyards: new phylogroup PG02f associated with bacterial inflorescence rot. Plant Pathology, 68(2). https://doi.org/10.1111/ppa.12936

Klingner, A. E., Palleroni, N. J., & Pontis, R. E. (1976). Isolation of Pseudomonas syringae from Lesions on Vitis vinifera. Journal of Phytopathology, 86(2). https://doi.org/10.1111/j.1439-0434.1976.tb01682.x

MacKie, K. A., Müller, T., & Kandeler, E. (2012). Remediation of copper in vineyards – A mini review. In Environmental Pollution (Vol. 167). https://doi.org/10.1016/j.envpol.2012.03.023

Sundin, G. W. (1989). Copper Resistance in Pseudomonas syringae pv. syringae from Cherry Orchards and its Associated Transfer in Vitro and in Planta with a Plasmid . Phytopathology, 79(8). https://doi.org/10.1094/phyto-79-861

Whitelaw-Weckert, M. A., Whitelaw, E. S., Rogiers, S. Y., Quirk, L., Clark, A. C., & Huang, C. X. (2011). Bacterial inflorescence rot of grapevine caused by Pseudomonas syringae pv. syringae. Plant Pathology, 60(2). https://doi.org/10.1111/j.1365-3059.2010.02377.x

Widmer, J., & Norgrove, L. (2023). Identifying candidates for the phytoremediation of copper in viticultural soils: A systematic review. Environmental Research, 216. https://doi.org/10.1016/j.envres.2022.114518

Wimalajeewa, D. L. S., & Flett, J. D. (1985). A study of populations of Pseudomonas syringae pv. syringae on stonefruits in Victoria. Plant Pathology, 34(2). https://doi.org/10.1111/j.1365-3059.1985.tb01356.x

Yang, P., Zhao, L., Gao, Y. G., & Xia, Y. (2023). Detection, Diagnosis, and Preventive Management of the Bacterial Plant Pathogen Pseudomonas syringae. In Plants (Vol. 12, Issue 9). https://doi.org/10.3390/plants12091765