Xylella fastidiosa

Xylella fastidiosa
Scientific classification
Domain: Bacteria
Kingdom: Eubacteria
Phylum: Proteobacteria
Class: Gammaproteobacteria
Order: Xanthomonadales
Family: Xanthomonadaceae
Genus: Xylella
Species: X. fastidiosa
Binomial name
Xylella fastidiosa
Wells et al., 1987

Xylella fastidiosa is an aerobic, Gram-negative bacteria of the monophyletic genus Xylella. It is a plant pathogen, and is transmitted exclusively by xylem fluid feeding sap insects.[1] Many plant diseases are due to symptomatic infections of X. fastidiosa, including bacterial leaf scorch, oleander leaf scorch, coffee leaf scorch (CLS), alfalfa dwarf, phony peach disease, and the economically important Pierce’s disease of grapes (PD) and citrus variegated chlorosis (CVC). In Europe it has attacked olive trees in the Salento area of Southern Italy causing the olive quick decline syndrome[2] (OQDS). While distributions of X. fastidiosa-related diseases are mostly limited to the Americas, outbreaks have occurred in Taiwan, Slovakia, and other countries worldwide.

Many plants are asymptomatic carriers of the bacteria, which can contribute to its spread. Pathogenicity of the bacterium only occurs when a large proportion of xylem vessels in a plant are colonized; often, the colonies of bacteria themselves are not large enough to completely block the vessels, and the mechanism of pathogenesis is largely unknown.[3] A subspecies of X. fastidiosa responsible for citrus variegated chlorosis was the first non-viral plant pathogen to have its genome sequenced, in part because of its potential to devastate affected crops.[4]

Pathogen anatomy and disease cycle

X. fastidiosa is rod-shaped and at least one subspecies has two types of pili on only one pole; longer type IV pili are used for locomotion while shorter type I pili assists in biofilm formation inside its hosts. As demonstrated using a PD-related strain, the bacterium has a characteristic twitching motion that allows groups of bacteria to travel upstream against heavy flow, such as that found in xylem vessels.[5] It is obligately insect vector transmitted from xylem-feeding insects directly into the xylem, but infected plant material for vegetative propagation (e.g. grafting) can produce mature plants that also have a X. fastidiosa disease.[6] In the wild, infections tend to occur during warmer seasons, when insect vector populations are at their highest. The bacterium is not seed transmitted and has been historically difficult to culture.[7][8]

X. fastidiosa can be divided into four subspecies that affect different plants and have separate origins. X. fastidiosa subsp. fastidiosa is the most studied subspecies, as it is the causal agent of PD; it is thought to have originated in southern Central America and also affects other varieties of plants. X. fastidiosa subsp. multiplex affects many trees, including stone fruits such as peaches and plums, and is thought to originate in temperate and southern North America. X. fastidiosa subsp. pauca is believed to originate in South America. It is the causal agent of CVC in Brazil, and also affects South American coffee crops in the form of coffee leaf scorch. X. fastidiosa subsp. sandyi is thought to originate in the southern part of the United States of America, and is notable for causing oleander leaf scorch.[9]

The bacterium has a two-part life cycle: inside an insect vector, and inside a susceptible plant. While the bacterium has been found across the globe, only once the bacterium reaches systemic levels do symptoms present themselves. Within susceptible plant hosts, X. fastidiosa forms a biofilm-like layer within xylem cells and tracheary elements that can completely block the water transport in affected vessels.[3]

Symptoms

There is significant variation in symptoms between diseases, though some symptoms are expressed across species. On a macroscopic scale, plants infected with a X. fastidiosa-related disease exhibit symptoms of water deficiencies, manifesting as leaf scorching, stunting in leaves, fruit, and overall plant height. As the bacterium progressively colonizes xylem tissues, affected plants often try to block off their xylem in an attempt to limit the spread of the pathogen; this can occur in the form of polysaccharide rich gels and/or tyloses. These plant defenses do not seem to hinder the movement of X. fastidiosa. Occlusion of vascular tissue, while a normal plant response to infection, makes symptoms significantly worse: as the bacteria itself also reduces vascular function, a 90% reduction of vascular hydraulic function was seen in susceptible Vitis vinifera.[10] Though it is possible for the bacterium itself to completely block vascular tissue, this tends to be rare; instead, smaller colonies are found throughout a high proportion of xylem vessels in symptomatic plants.

Pierce's disease

Severe PD symptoms include shriveled fruit, leaf scorching, and premature abscission of leaves, with bare petioles remaining on the stem.[4]

Citrus variegated chlorosis

The disease is named after the characteristic spotty chlorosis on the top sides of leaves. Fruits of infected plants are small and hard.

Leaf scorches

In coffee, premature abscission of leaves and fruits is of bigger concern than scorching.

Environment

X. fastidiosa can be found worldwide, though its diseases are most prominent in riparian habitats including the southeastern United States, California, and South America.

Symptoms of X. fastidiosa diseases worsen during hot, dry periods in the summer: lack of water and maximum demand from a full canopy of leaves combined with symptoms due to disease stress infected plants to a breaking point. Cold winters can limit the spread of the disease;[8] this has shown to be effective in California, but is useless in regions with milder winters, such as Brazil. Additionally, dry summers seem to delay symptom development of PD in California.[6]

Any conditions that increase vector populations can increase disease incidence, such as seasonal rainfall and forests or tree cover adjacent to crops, which serve as alternate food sources and overwintering locations for leafhoppers.[6]

Alexander Purcell, an expert on the bacterium, hypothesizes that plants foreign to X. fastidiosa’s area of origin, Holarctic-neotropical regions, are more susceptible to development of symptoms. Thus, plants from warmer climates are more resistant to disease development, while plants from areas with harsher winters, such as grapes, are more severely affected by disease.[8]

Hosts

X. fastidiosa has an incredibly wide host range: as of 2015, 309 species were reported as hosts for the bacterium.[11] Most host plants are dicots, but X. fastidiosa has also been reported in monocots and ginkgo, a gymnosperm. However, the vast majority of host plants remain asymptomatic, making them reservoirs for infection.

Due to the temperate climates of South America and the southeastern and western coast of the United States, X. fastidiosa can be a limiting factor in fruit crop production, particularly for stone fruits in northern Florida and grapes in California.[3] In South America, X. fastidiosa can cause significant losses in the citrus and coffee industries; 1/3 of today's citrus crops in Brazil have CVC symptoms.[4]

The bacterium also colonizes the foregut of insect vectors, which can be any xylem-feeding insects, often sharpshooters in Cicadellidae subfamily Cicadellinae.[1][8] Once the bacterium is acquired, X. fastidiosa has a short latent period of about 2 hours, then is transmissible for a period of a few months up to the lifetime of the insect. The bacterium multiplies within its vectors, forming a “bacterial carpet” within the foregut of its host. If the foregut is shed, as during molting, the vector is no longer infected but may reacquire the pathogen. At present, there is no evidence that the bacterium has any detrimental effect on its insect hosts.

List of Subspecies fastidiosa Susceptible Plants (recreated from EFSA Panel) [11]
Subspecies Plant Family Plant Genus
fastidiosa Adoxaceae Sambucus
Amaranthaceae Alternanthera, Chenopodium
Anacardiaceae Rhus, Toxicodendron
Apiaceae Conium, Datura, Daucus, Oenanthe
Apocynaceae Nerium, Vinca
Araliaceae Hedera
Asteraceae Ambrosia, Artemisia, Baccharis, Callistephus, Conyza, Franseria, Helianthus, Latuca, Solidago, Sonchus, Xanthium
Betulaceae Alnus
Boraginaceae Amsinckia
Brassicaceae Brassica
Cannaceae Canna
Caprifoliaceae Lonicera, Symphoricarpos
Convolvulaceae Convolvulus, Ipomoea
Cyperaceae Cyperus
Fabaceae Acacia, Chamaecrista, Cytisus, Genista, Lathyrus, Lupinus, Medicago, Melilotus, Spartium, Trifolium, Vicia
Fagaceae Quercus
Geraniaceae Erodium, Pelargonium
Juglandaceae Juglans
Lamiaceae Callicarpa, Majorana, Melissa, Mentha, Rosmarinus, Salvia
Lauraceae Persea, Umbellularia
Magnoliaceae Magnolia
Malvaceae Malva
Myrtaceae Eucalyptus, Eugenia, Metrosideros
Oleaceae Fraxinus, Syringa
Onagraceae Epilobium, Fuchsia, Godetia, Oenothera
Pittosporaceae Pittosporum
Platanaceae Platanus
Poaceae Avena, Bromus, Cynodon, Digitaria, Echinochloa, Eragrostis, Eriochola, Festuca, Holcus, Hordeum, Lolium, Paspalum, Pennisetum, Phalaris, Phleum, Poa, Setaria, Sorghum
Polygonaceae Persicaria, Polygonum, Rheum, Rumex
Portulacaceae Montia, Portulaca
Resedaceae Reseda
Rhamnaceae Rhamnus
Rosaceae Cotoneaster, Fragaria, Photinia, Prunus, Rosa, Rubus
Rubiaceae Coffea, Coprosma
Rutaceae Citrus
Salicaceae Populus, Salix
Sapindaceae Acer, Aesculus
Scrophulariaceae Veronica
Simmondsiaceae Simmondsia
Solanaceae Datura, Lycopersicon, Nicotiana, Solanum
Urticaceae Urtica
Verbenaceae Duranta
Vitaceae Ampelopsis, Parthenocissus, Vitis

Grape

Pierce's disease (PD) was discovered in 1892 by Newton B. Pierce (1856–1916; California's first professional plant pathologist) on grapes in California near Anaheim, where it was known as "Anaheim disease".[12] The disease is endemic in northern California, being spread by the blue-green sharpshooter, which only attacks grapevines that are adjacent to riparian habitats. It became a real threat to California's wine industry when the glassy-winged sharpshooter (GWSS), native to the southeast United States, was discovered in the Temecula Valley in California in 1996. The GWSS spreads PD much more extensively than other vectors do.

Symptoms of infection

When a vine becomes infected, the bacterium causes a gel to form in the xylem tissue of the vine, preventing water from being drawn through the vine. Leaves on vines with Pierce's disease will turn yellow and brown, and eventually drop off the vine. Shoots will also die. After one to five years, the vine itself will die. The proximity of vineyards to citrus orchards compounds the threat, because citrus is not only a host for the sharpshooter eggs, but it is also a popular overwintering site for the insect. Likewise, oleander, a common landscaping plant in California, serves as a reservoir for Xylella.

Collaborative efforts for solutions

It triggered a unique effort from growers, administrators, policy makers and researchers to work together in finding a solution for this immense threat. No cure has yet been found,[13] but the understanding of Xylella fastidiosa and glassy-winged sharpshooter biology has increased much since 2000, when the California Department of Food and Agriculture, in collaboration with different universities, such as University of California, Davis (UC Davis); University of California, Berkeley; University of California, Riverside, and the University of Houston–Downtown started to focus their research on this pest. The research explores the different aspects of the disease propagation from the vector to the host plant and within the host plant, to the impact of the disease on California's economy. All researchers working on Pierce's disease meet annually in San Diego in mid-December to discuss the progress in their field. All proceedings from this symposium can be found on the Pierce's disease website,[14] developed and managed by the Public Intellectual Property Resource for Agriculture (PIPRA).[15]

There are no resistant Vitis vinifera varieties, and Chardonnay and Pinot noir are especially sensitive, but muscadine grapes (Vitis rotundifolia) have a natural resistance.[13] Pierce's disease is found in the southeastern United States and Mexico. Also it was reported by Luis G. Jiménez-Arias in Costa Rica, and Venezuela,[16] and possibly in other parts of Central and South America. There are isolated hot spots of the disease near creeks in Napa and Sonoma in northern California.[13] Work is underway at UC Davis to breed PD resistance from Vitis rotundifolia into Vitis vinifera. The first generation was 50% high quality vinifera genes, the next 75%, the third 87% and the fourth 94%. In the spring of 2007, seedlings that are 94% vinifera were planted.[17]

Nerium oleander infected with Xylella fastidiosa in Phoenix, Arizona

Oleander

Oleander leaf scorch is a disease of landscape oleanders (Nerium oleander) caused by a strain of X. fastidiosa which has become prevalent in California and Arizona, USA starting in the mid 1990s. This disease is transmitted by a type of leafhopper (insect) called the Glassy-winged sharpshooter (Homalodisca coagulata).

Olive

In October 2013 the bacterium was found to be infecting olive trees in the region of Apulia in southern Italy.[18] The disease was causing a rapid decline in olive plantations and by April 2015 it was affecting the whole Province of Lecce and other zones of Apulia.[2][19] The bacterium had never previously been confirmed in Europe.[20] Almond and oleander plants in the region have also tested positive for the pathogen.[18] The sub-species involved in Italy is Xylella fastidiosa subsp. pauca. This shows a marked preference for olive trees and warm conditions and is thought unlikely to spread into Northern Europe.[21]

The disease has been called olive quick decline syndrome (OQDS; in Italian: complesso del disseccamento rapido dell'olivo).[20][22] The disease causes withering and desiccation of terminal shoots, distributed randomly at first but which then expands to the rest of the canopy.[22] This results in the collapse and death of the trees.[22] In the affected groves, all of the plants show symptoms.[22]

Spread of syndrome

By the beginning of 2015 it had infected up to a million trees in the southern region of Apulia.[23] By July 2015, Xylella fastidiosa had reached Corsica,[24] by October 2015, it had reached Mainland France, near Nice, in Provence-Alpes-Côte d'Azur, affecting the myrtle-leaf milkwort (Polygala myrtifolia). This is the subspecies X. fastidiosa subsp. multiplex which is considered to be a new genetic variant of the bacterium, different to that found in Italy.[25][26] On 18 August 2016 in Corsica, 279 focuses of the infection have been detected, concentrated mostly in the south and the west of the island.[27] In August 2016, the bacterium was detected in Germany in an oleander plant.[28] In January 2017 it was detected in Majorca and Ibiza.[29] In June 2017, it was detected in the Iberian peninsula, specifically in Guadalest, Alicante.[30] In April 2018 it was detected in Madrid.[31]

Genome sequencing

The genome sequencing of X. fastidiosa was realized by a pool of over 30 research labs in the State of São Paulo, Brazil, and funded by this State's Science Foundation (FAPESP).[32]

See also

Notes

  1. 1 2 Redak, Richard A.; Purcell, Alexander H.; Lopes, João R.S.; Blua, Matthew J.; Mizell III, Russell F.; Andersen, Peter C. (2003-12-03). "The biology of xylem fluid–feeding insect vectors of xylella fastidiosa and their relation to disease epidemiology". Annual Review of Entomology. 49 (1): 243–270. doi:10.1146/annurev.ento.49.061802.123403. ISSN 0066-4170.
  2. 1 2 "Minimizing the Spread of Disease in Italy's Famous Olive Trees". Our Environment at Berkeley. University of California at Berkeley, Department of Environmental Science, Policy, and Management (ESPM). 9 February 2015. Retrieved 5 May 2015.
  3. 1 2 3 Chatterjee, Subhadeep; Almeida, Rodrigo P. P; Lindow, Steven (2008-08-04). "Living in two Worlds: The Plant and Insect Lifestyles of Xylella fastidiosa". Annual Review of Phytopathology. 46 (1): 243–271. doi:10.1146/annurev.phyto.45.062806.094342. ISSN 0066-4286.
  4. 1 2 3 Hopkins, D. L.; Purcell, A. H. (2002-10-01). "Xylella fastidiosa: Cause of Pierce's Disease of Grapevine and Other Emergent Diseases". Plant Disease. 86 (10): 1056–1066. doi:10.1094/pdis.2002.86.10.1056. ISSN 0191-2917.
  5. ↑ Meng, Yizhi; Li, Yaxin; Galvani, Cheryl D.; Hao, Guixia; Turner, James N.; Burr, Thomas J.; Hoch, H. C. (2005-08-15). "Upstream Migration of Xylella fastidiosa via Pilus-Driven Twitching Motility". Journal of Bacteriology. 187 (16): 5560–5567. doi:10.1128/jb.187.16.5560-5567.2005. ISSN 0021-9193. PMC 1196070. PMID 16077100.
  6. 1 2 3 Mizell, Russell F.; Andersen; Tipping (January 2003). "Xylella Fastidiosa Diseases and Their Leafhopper Vectors" (PDF). University of Florida IFAS Extension. Retrieved November 30, 2017.
  7. ↑ Coletta-Filho, Helvécio Della; Carvalho, Sérgio Alves; Silva, Luis Fernando Carvalho; Machado, Marcos Antonio (2014-07-01). "Seven years of negative detection results confirm that Xylella fastidiosa, the causal agent of CVC, is not transmitted from seeds to seedlings". European Journal of Plant Pathology. 139 (3): 593–596. doi:10.1007/s10658-014-0415-8. ISSN 0929-1873.
  8. 1 2 3 4 Purcell, Alexander (2013-08-04). "Paradigms: Examples from the Bacterium Xylella fastidiosa". Annual Review of Phytopathology. 51 (1): 339–356. doi:10.1146/annurev-phyto-082712-102325. ISSN 0066-4286.
  9. ↑ "Xylella fastidiosa (Pierce's disease of grapevines)". www.cabi.org. Retrieved 2017-11-06.
  10. ↑ Sun, Qiang; Sun, Yuliang; Walker, M. Andrew; Labavitch, John M. (2013-03-01). "Vascular Occlusions in Grapevines with Pierce's Disease Make Disease Symptom Development Worse". Plant Physiology. 161 (3): 1529–1541. doi:10.1104/pp.112.208157. ISSN 0032-0889. PMC 3585614. PMID 23292789.
  11. 1 2 EFSA Panel on Plant Health (PLH) (2015-01-01). "Scientific Opinion on the risks to plant health posed by Xylella fastidiosa in the EU territory, with the identification and evaluation of risk reduction options". EFSA Journal. 13 (1): n/a–n/a. doi:10.2903/j.efsa.2015.3989. ISSN 1831-4732.
  12. ↑ Pinney, Thomas (1989). A History of Wine in America from the Beginnings to Prohibition. University of California Press. p. 27. ISBN 0520062248.
  13. 1 2 3 winepros.com.au. Oxford Companion to Wine. "Pierce's disease".
  14. ↑ PIPRA Pierce's Disease website. "Pierce's disease".
  15. ↑ Public Intellectual Property Resource for Agriculture. "PIPRA".
  16. ↑ Jiménez A., L.G. (July–September 1985). "Evidencia inmunológica del mal de pierce de la vid en Venezuela". Turrialba. 35 (3): 243–247.
  17. ↑ PD/GWSS Board bulletin, California Department of Food & Agriculture, Spring 2007 (p. 2)
  18. 1 2 "'Major consequences' if olive disease spreads across EU". BBC News. 9 January 2015. Retrieved 1 March 2015.
  19. ↑ Spagnolo, Chiara. "Xylella, allarme nuovi focolai, per la Ue interessata tutta la Puglia". repubblica.it. La Repubblica. Retrieved 8 May 2015.
  20. 1 2 "First report of Xylella fastidiosa in the EPPO region". European and Mediterranean Plant Protection Organization (EPPO). Retrieved 1 March 2015.
  21. ↑ "Xylella fastidiosa". Plant Health Portal. Department for Environment, Food and Rural Affairs. Retrieved 24 June 2017.
  22. 1 2 3 4 "Expert Says Eradication of New Olive Tree Disease in Europe Unlikely". Olive Oil Times. 29 March 2014. Retrieved 1 March 2015.
  23. ↑ "Italy warns deadly olive tree bacteria could spread across Europe". The Telegraph. 27 February 2015. Retrieved 1 March 2015.
  24. ↑ "Olive oil dries up". The Economist. 31 July 2015. Retrieved 2015-07-31.
  25. ↑ "Xylella fastidiosa". Plants. European Commission. Retrieved 24 June 2017.
  26. ↑ "Un premier cas de la bactérie tueuse de végétaux découvert à Nice". Nice Matin. 9 October 2015. Retrieved 2015-10-09.
  27. ↑ "Xylella : carte et liste des communes en zones délimitées en Corse au 18 août 2016". Direction régionale de l'alimentation, de l'agriculture et de la forêt de Corse (in French). Retrieved 23 August 2016.
  28. ↑ "Pflanzen-Killerbakterium: Teile von Zeulenroda-Triebes zur Sperrzone erklärt". Antenne Thueringen (in German). Retrieved 23 August 2016.
  29. ↑ "La plaga vegetal más peligrosa de Europa invade las Baleares". La Vanguardia (in Spanish). Retrieved 24 January 2017.
  30. ↑ "Tala preventiva de árboles ante el primer caso de 'Xylella fastidiosa' en la península". La Vanguardia (in Spanish). Retrieved 4 July 2017.
  31. ↑ "Detectada en Madrid la presencia de una bacteria que obligó a arrancar un millón de olivos en Italia". 20 Minutos (in Spanish). Retrieved 12 April 2018.
  32. ↑ Simpson, AJG; Reinach, FC; Arruda, P; Abreu, FA; et al. (July 2000). "The genome sequence of the plant pathogen Xylella fastidiosa". Nature. 406 (6792): 151–159. doi:10.1038/35018003. PMID 10910347.

References

  • Public Intellectual Property Resource for Agriculture Pierce's Disease Website
  • APHIS. 2002. Glassy-winged Sharpshooter and Pierce's Disease in California
  • CDFA PD/GWSS Board Website PD/GWSS Interactive Forum
  • Univ. of Arizona. 2006 Oleander leaf scorch
  • Wells, J. M., B. C. Raju, H. Y. Hung, W. G. Weisburg, L. M. Parl and D. Beemer (1987). "Xylella fastidiosa gen. nov., sp. nov.: Gram-negative, xylem-limited, fastidious plant bacteria related to Xanthomonas spp". International Journal of Systematic Bacteriology. 37 (2): 136–143. doi:10.1099/00207713-37-2-136.
  • Catalano, Luigi (2015). "Xylella fastidiosa la più grave minaccia dell'olivicoltura italiana" (PDF). L'Informatore Agrario (in Italian) (16): 36–42.
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