Pathways of flower infection and pollen-mediated dispersion of Pseudomonas syringae pv. actinidiae, the causal agent of kiwifruit bacterial canker

Irene Donati , Antonio Cellini , Giampaolo Buriani , Sofia Mauri , Callum Kay , Gianni Tacconi , Francesco Spinelli

Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) : 56

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Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) :56 DOI: 10.1038/s41438-018-0058-6
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Pathways of flower infection and pollen-mediated dispersion of Pseudomonas syringae pv. actinidiae, the causal agent of kiwifruit bacterial canker
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Abstract

Flowers can provide a protected and nutrient-rich environment to the epiphytic microflora, thus representing a sensible entry point for pathogens such as Pseudomonas syringae pv. actinidiae (Psa). This bacterium can colonize both male and female Actinidia flowers, causing flower browning and fall, and systemic invasion of the host plant, eventually leading to its death. However, the process of flower colonization and penetration into the host tissues has not yet been fully elucidated. In addition, the presence of Psa in the pollen from infected flowers, and the role of pollination in the spread of Psa requires confirmation. The present study employed a Psa strain constitutively expressing the fluorescent GFPuv protein, to visualize in vivo flower colonization. Microscopy observations were performed by means of confocal laser scanning and wide-field fluorescent microscopy, and were coupled with the study of Psa population dynamics by quantitative PCR (q-PCR). The pathogen was shown to colonize stigmata, move along the stylar furrow, and penetrate the receptacles via the style or nectarhodes. Once the receptacle was invaded, the pathogen migrated along the flower pedicel and became systemic. Psa was also able to colonize the anthers epiphytically and endophytically. Infected male flowers produced contaminated pollen, which could transmit Psa to healthy plants. Finally, pollinators (Apis mellifera and Bombus terrestris) were studied in natural conditions, showing that, although they can be contaminated with Psa, the pathogen’s transmission via pollinators is contrasted by its short survival in the hive.

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Irene Donati, Antonio Cellini, Giampaolo Buriani, Sofia Mauri, Callum Kay, Gianni Tacconi, Francesco Spinelli. Pathways of flower infection and pollen-mediated dispersion of Pseudomonas syringae pv. actinidiae, the causal agent of kiwifruit bacterial canker. Horticulture Research, 2018, 5 (1) : 56 DOI:10.1038/s41438-018-0058-6

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References

[1]

Vanneste, J. L. Recent progress on detecting, understanding and controlling Pseudomonas syringae pv. actinidiae: a short review. N. Z. Plant Prot. 66, 170-177 (2013).

[2]

Donati, I. et al. New insights on the bacterial canker of kiwifruit (Pseudomonas syringae pv. actinidiae). J. Berry Res. 4, 53-67 (2014).

[3]

Greer, G. & Saunders, C. The costs of Psa-V to the New Zealand kiwifruit industry and the wider community. In: Report to kiwifruit VineHealth. Lincoln University press, New Zealand: Agribusiness and Economics Research Unit, 2-9 (2012).

[4]

Balestra, G. M., Renzi, M. & Mazzaglia, A. First report of bacterial canker of Actinidia deliciosa caused by Pseudomonas syringae pv. actinidiae in Portugal. New Dis. Rep. 22, 10 (2010).

[5]

Koh, Y. J., Kim, G. H., Jung, J. S., Lee, Y. S. & Hur, J. S. Outbreak of bacterial canker on Hort16A (Actinidia chinensis Planchon) caused by Pseudomonas syringae pv. actinidiae in Korea. N. Z. J. Crop Hort. Sci. 38, 275-282 (2010).

[6]

Vanneste, J. L. et al. First report of Pseudomonas syringae pv. actinidiae, the causal agent of bacterial canker of kiwifruit in France. Plant Dis. 95, 1311 (2011).

[7]

Scortichini, M . Occurrence of Pseudomonas syringae pv. actinidiae on kiwifruit in Italy. Plant Pathol. 43, 1035-1038 (1994).

[8]

Balestra, G. M., Mazzaglia, A., Quattrucci, A., Renzi, M. & Rossetti, A. Current status of bacterial canker spread on kiwifruit in Italy. Aust. Plant Dis. Notes 4, 34-36 (2009).

[9]

Ferrante, P. & Scortichini, M. Identification of Pseudomonas syringae pv. actinidiae as causal agent of bacterial canker of yellow kiwifruit (Actinidia chinensis Planchon) in Central Italy. J. Phytopathol. 157, 768-770 (2009).

[10]

Spadaro, D. et al. [The arrival of kiwifruit canker in Piedmont]. Inf. Agrar. 66, 58-59 (2010).

[11]

Everett, K. R. et al. First report of Pseudomonas syringae pv. actinidiae causing kiwifruit bacterial canker in New Zealand. Australas. Plant Dis. Notes 6, 67-71 (2011).

[12]

Vanneste, J. L. The scientific, economic, and social impacts of the New Zealand outbreak of bacterial canker of kiwifruit (Pseudomonas syringae pv. actinidiae). Ann. Rev. Phytopatology 55, 377-399 (2017).

[13]

Spinelli, F., Donati, I., Vanneste, J. L., Costa, M. & Costa, G. Real time monitoring of the interactions between Pseudomonas syringae pv. actinidiae and Actinidia species. Acta Hortic. 913, 461-465 (2011).

[14]

Ferrante, P. et al. The importance of the main colonization and penetration sites of Pseudomonas syringae pv. actinidiae and prevailing weather conditions in the development of epidemics in yellow kiwifruit, recently observed in central Italy. J. Plant Pathol. 94, 455-461 (2012).

[15]

Young, J. M., Cheesmur, G. J., Welham, F. V. & Henshall, W. R. Bacterial blight of kiwifruit. Ann. Appl. Biol. 112, 91-105 (1988).

[16]

Everett, K. R. & Henshall, W. R. Epidemiology and population ecology of kiwifruit blossom blight. Plant Pathol. 43, 824-830 (1994).

[17]

Balestra, G. B. & Varvaro, L. Pseudomonas syringae pv. syringae causal agent of disease on floral buds of Actinidia deliciosa (A. Chev) Liang et Ferguson in Italy. J. Phytopathol. 145, 375-378 (1997).

[18]

Rossetti, A. & Balestra, G. M. Pseudomonas syringae pv. syringae on kiwifruit plants: epidemiological traits and its control. In: Fatmi M. et al. (eds) Pseudomonas syringae pathovars and related pathogens - Identification, Epidemiology and Genomics. Springer, Dordrecht, 65-68 (2008).

[19]

Ark, P. A. Further evidence of pollen dissemination of walnut blight. Phytopathology 34, 329-334 (1944).

[20]

Ercolani, G. L. [Individuazione di Xanthomonas juglandis (Pierce) Dowson in Emilia]. English, Abstract, Conclusion and Figure Captions. Phytopathol. Mediterr. 2, 1-10 (1962).

[21]

Wilson, M., Sigee, D. C. & Epton, H. A. S. Erwinia amylovora infection of hawthorn blossom: I. The anther. J. Phytopathol. 127, 1-14 (1989).

[22]

Mansvelt, E. L. & Hattingh, M. J. Scanning electron microscopy of pear blossom invasion by Pseudomonas syringae pv. syringae. Can. J. Bot. 65, 2523-2529 (1987).

[23]

Wilson, M., Sigee, D. C. & Epton, H. A. S. Erwinia amylovora infection of hawthorn blossom: II. The stigma. J. Phytopathol. 127, 15-28 (1989).

[24]

Spinelli, F., Ciampolini, F., Cresti, M., Geider, K. & Costa, G. Influence of stigmatic morphology on flower colonization by Erwinia amylovora and Pantoea agglomerans. Eur. J. Plant Pathol. 113, 395-405 (2005).

[25]

Johnson, K. B., Stockwell, V. O., Burgett, D. M., Sugar, D. & Loper, J. E. Dispersal of Erwinia amylovora and Pseudomonas fluorescens by honey bees from hives to apple and pear blossoms. Phytopathology 83, 478-484 (1993).

[26]

McArt, S. H., Koch, H., Irwin, R. E. & Adler, L. S. Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecol. Lett. 17, 624-636 (2014).

[27]

Howpage, D., Spooner-Hart, R. N. & Vithanage, V. Influence of honey bee (Apis mellifera) on kiwifruit pollination and fruit quality under Australian conditions. N.Z. J. Crop Hortic. Sci. 29, 51-59 (2001).

[28]

Testolin, R., Vizzotto, G. & Costa, G. Kiwifruit pollination by wind and insects in Italy. N.Z. J. Crop Hortic. Sci. 19, 381-384 (1991).

[29]

Howpage, D., Vithanage, V. & Spooner-Hart, R. Pollen tube distribution in the kiwifruit (Actinidia deliciosa A. Chev. C. F. Liang) pistil in relation to its reproductive process. Ann. Bot. (Lond.) 81, 697-703 (1998).

[30]

Gonzalez, M. V., Coque, M. & Herrero, M. Papillar integrity as an indicator of stigmatic receptivity in kiwifruit (Actinidia deliciosa). J. Exp. Bot. 46, 263-269 (1995).

[31]

Hopping, M. E. & Jerram, E. M. Supplementary pollination of tree fruits. II. Field trials on kiwifruit and Japanese plums. N.Z. J. Agric. Res. 23, 517-521 (1980).

[32]

Vanneste, J. L. et al. Detection of Pseudomonas syringae pv. actinidiae in kiwifruit pollen samples. N.Z. Plant Prot. 64, 246-251 (2011).

[33]

Stefani, E. & Giovanardi, D. Dissemination of Pseudomonas syringae pv. actinidiae through pollen and its epiphytic life on leaves and fruits. Phytopathol. Mediterr. 50, 489-496 (2011).

[34]

Everett, K. R. et al. Heat treatments to kill Pseudomonas syringae pv. actinidiae on contaminated pollen. N.Z. Plant Prot. 65, 8-18 (2012).

[35]

Biondi, E. et al. Pseudomonas syringae pv. actinidiae detection in kiwifruit plant tissue and bleeding sap. Ann. Appl. Biol. 162, 60-70 (2013).

[36]

Gallelli, A., Talocci, S., L’Aurora, A. & Loreti, S. Detection of Pseudomonas syringae pv. actinidiae, causal agent of bacterial canker of kiwifruit, from symptomless fruits and twigs, and from pollen. Phytopathol. Mediterr. 50, 462-472 (2011).

[37]

Tontou, R., Giovanardi, D. & Stefani, E. Pollen as a possible pathway for the dissemination of Pseudomonas syringae pv. actinidiae and bacterial canker of kiwifruit. Phytopathol. Mediterr. 53, 333-339 (2014).

[38]

Sigee, D. C. Bacteria as plant pathogens. In: Bacterial Plant Pathology: Cell and Molecular Aspects. D. C. Sigee, ed. Cambridge University Press, Cambridge. pp. 1-12.

[39]

Gallelli, A., Talocci, S., Pilotti, M. & Loreti, S. Real-time and qualitative PCR for detecting Pseudomonas syringae pv. actinidiae isolates causing recent outbreaks of kiwifruit bacterial canker. Plant Pathol. 63, 264-276 (2014).

[40]

Pusey, P. L. The role of water in epiphytic colonization and infection of pomaceous flowers by Erwinia amylovora. Phytopathology 90, 1352-1357 (2000).

[41]

Gimenez-Ibanez, S. & Rathjen, J. P. The case for defence: plant versus Pseudomonas syringae. Microbes Infect. 12, 428-437 (2010).

[42]

Balestra, G. M. [ Use of copper formulations to limit bacterial diseases in kiwifruit. (Speciale Actinidia)]. Riv. di Fruttic. e di Ortofloric. 66, 35-41 (2004).

[43]

Serizawa, S. & Ichikawa, T. Epidemiology of bacterial canker of kiwifruit. 2. The most suitable times and environments for infection on new canes. Ann. Phytopathol. Soc. Jpn. 59, 460-468 (1993).

[44]

Serizawa, S., Ichikawa, T., Takikawa, Y., Tsuyumu, S. & Goto, M. Occurrence of bacterial canker of kiwifruit in Japan: description of symptoms, isolation of the pathogen and screening of bactericides. Ann. Phytopathol. Soc. Jpn. 55, 427-436 (1989).

[45]

Pattemore, D. E., Goodwin, R. M., McBrydie, H. M., Hoyte, S. M. & Vanneste, J. L. Evidence of the role of honey bees (Apis mellifera) as vectors of the bacterial plant pathogen Pseudomonas syringae. Australas. Plant Pathol. 43, 571-575 (2014).

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