Plant Pathogen DispersalJonathan S West, Rothamsted Research, Harpenden, UK

Plant disease epidemics require plant pathogens to be

dispersed to infect new hosts. Understanding dispersal is

important for devising methods to improve detection and

control of plant pathogens. This is not straightforward, as

plant pathogens can be dispersed by air, rain, water or

soil, and by vectors such as animals, pollen, various

microbes, people and machinery and on infected plant

material including seeds. Epidemicsvary in timeandspace

as a result of complex processes affecting inoculum

availability and production, dispersal and survival pro-

cesses, andalsothe coincidenceof susceptiblecrop plants,

which each interact with the weather. To reduce disease,

exposure of crops to inoculum is often limited by separ-

ating crops in time and space, using crop rotation,

including different varieties. A wide range of diagnostic

methods are increasingly used to help with this by

detecting plant pathogens before infection occurs to

prevent introduction of exotic inoculum, or to improve

applications of crop protection products.

Introduction

Plant pathogens include fungi, protists (such as oomycetesand plasmodiophorids), bacteria, phytoplasmas, virusesand viroids. Dispersal is essential for plant pathogens toinfect new hosts and complete their life cycles, reproducingto cause plant disease epidemics. Dispersal is also essentialfor gene flow and diversification of pathogen populations.It is important for plant pathologists and epidemiologiststo understand dispersal mechanisms in order to devisebetter methods to detect plant pathogens and control the

diseases they cause. The challenge of plant disease controlis a key component of increasing food production and foodsecurity but requires knowledge of multiple factors affect-ing plant disease epidemics, which occur at different timesand locations. One of those factors is the method ofpathogendispersal,whether by air, rain,water or soil, or byvectors (Figure 1). Epidemics are directly influenced by thecomplexities of inoculum availability as a result of pro-duction, dispersal and survival processes, and also bygrowth stage of susceptible crop plants and weather(McCartney et al., 2006). One of the main methods used incrop protection is to limit exposure of susceptible crops toinoculum by separating crops in time and space, using croprotation. In addition to conventional crop rotation, the useof different diverse varieties in different fields is anothermethod to reduce the amount of inoculum dispersing toreach subsequent susceptible crops because certain races ofplant pathogens produced on one variety of a cropmay notbe able to infect a different variety (Aubertot et al., 2006;Marcroft et al., 2012). In addition, othermethods are used,such as good hygiene or management of inoculum, use ofcrop protection products, for example, biological agents,pesticides and fungicides and use of resistant plant vari-eties. A wide range of diagnostic methods are increasinglyused to help with biosecurity and crop protection either bypreventing introduction of exotic inoculum or by detectingendemic plant pathogens before infection occurs toimprove applications of crop protection products. Diag-nostic methods are also used to monitor changes in genetictraits of pathogen populations, such as fungicide resistanceand development of new races. One of themain reasons fornew introductions of plant pathogens to a completely newterritory is introduction by people, inadvertently as infec-ted plant material, infected seeds or as contamination insoil, on clothing, machinery, food or other importedmaterials. As a result, many regulations and plant healthinspection teams are used in an attempt to limit this type ofdispersal. However, a method of long-distance dispersalthat have no control over is by air. Somepathogens that aredispersed by air can cross oceans and continents (Brownand Hovmøller, 2002) and are adapted to survive freezingtemperatures, high ultra-violet (UV) light levels and

Advanced article

Article Contents

. Introduction

. Air Dispersal

. Dispersal by Rain and Water

. Soilborne Plant Pathogens

. Introductions by People (Vehicles, Seed)

. Dispersal by Vectors

. Conclusion and Future Perspectives

. Acknowledgements

Online posting date: 17th February 2014

eLS subject area: Plant Science

How to cite:West, Jonathan S (February 2014) Plant Pathogen Dispersal. In: eLS.

John Wiley & Sons, Ltd: Chichester.

DOI: 10.1002/9780470015902.a0021272

eLS & 2014, John Wiley & Sons, Ltd. www.els.net 1

desiccation (Gregory, 1952). Some of these airbornepathogens, such as the bacterium Pseudomonas syringaeand the fungus Puccinia striiformis may even induce icenucleation to ‘seed’ rainfall by inducing ice crystals to formin the air, which melts to form rain thereby returning thespores to plants on the ground (Huffman et al., 2013;Morris et al., 2013a, b). Meanwhile, others only remainviable for short periods or in certain less extreme condi-tions, so these are usually not dispersed far in air. Anotherimportant dispersal process is by rain-splash, whichusually occurs over short distances (51m) but occasion-ally intermediate distances such as several kilometres havebeen suggested to occur when an aerosol of droplets con-taining pathogens is produced by combinations of rain andstrong winds. Pathogens can also be dispersed in waterfilms, particularly in soil and groundwater or rivers. Soil-borne diseases tend to be relatively static but can be dis-persed to other parts of a field or new locations when soilparticles and crop debris are blown by strong winds ortransported on machinery. Insects and other invertebratesand other microbes may vector some pathogens, mainly

viruses, viroids and phytoplasmas and this can includevectoring over relatively long distances when flying insectvectors, such as aphids, undergo seasonal migrations.Pathogens move within plants by growing through tissuesand can be translocated from roots to upper parts in sap,but these processes are not considered here as part of dis-persal. In the case of ergot caused by the species of Clavi-ceps, the fungus encourages insects to vector its conidia toinfect new flowers by producing these spores in a sweetliquid, known as honeydew. Plant viruses may also bevectored by fungi, protists and in pollen. Whether patho-gens arrive by introduction, air or vector, their chance ofbecoming established in new territories, where they werepreviously absent, may be enhanced by climate change.This article aims to discuss the various dispersal processesintroduced above in relation to the biology of plantpathogens as key information required to enablemodellingof disease epidemics and to improve surveillance andcontrol of plant diseases. See also: Epidemiology of PlantDisease; Fungicides for Plant Diseases; Plant VirusMovement; Resistance Genes (R Genes) in Plants

Airborne spores, bacteriaand airborne vectors

(pollen, soil and plant debris)

Ballistic and aerosolisedrain-splash and water

Soilborne dispersal, enhancedby vehicles, wind and people

Vectors (insects, fungi,protists, pollen, peopleand imported products)

Figure 1 A summary of plant pathogen dispersal processes: soilborne pathogens that are also wind-blown or vectored, rain-splash and water, airborne

(various spores, cells and biological debris), and vectors (insects (aphids illustrated), fungi (ergots on wheat, which are transported in seed and produce

insect-vectored conidia in ‘honeydew’), pollen (grass and pine pollen shown, which can contain viruses), and people, who are responsible for introductions

in imported plants, food and other materials). The centre-left photo of rain is provided courtesy of Prof. John Lacey (Rothamsted Research).

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Air Dispersal

Wind- or air-dispersal has been attributed to local spreadwithinor next to thefieldwhere the pathogenwasproducedand also to long-distance dispersal of pathogens overcontinental scales often crossing oceans (Pady andKapica,1955; Gregory, 1973; Brown and Hovmøller, 2002).Pathogen propagules dispersed by wind are typicallyspores or sporangia of fungi and oomycetes and spores,cells or collections of cells in biofilms of bacteria. However,air, particularly in windy conditions, also contains smallparticles of soil and water droplets so to some extent, soil-and waterborne pathogens may also be dispersed in air.For the truly air-dispersed pathogens, individual fungalspores typically have aerodynamic diameters in the sizerange of 2–30 mm, whereas individual bacteria are usually1–4mm, although aggregations can be much bigger. Theaerobiology and deposition of airborne propagules mayaffect disease distributions, leading to disease gradientswhen the sources of inoculumare local, small foci of diseasewhen the inoculum is rare, or a uniform disease distribu-tion when the inoculum is ubiquitous. See also: Biofilms;Fungal SporesThe timing of airborne inoculummay be seasonal due to

the production of fruiting bodies only under certain con-ditions and additionally, spores are often released onlyafter specific weather events (Lacey andWest, 2006; West,2012). Many fungal spores are actively released (Ingold,1971; Lacey, 1996), which allows the spores to reach themore turbulent air above the laminar boundary layer(Gregory, 1973). Some spores are passively released inwindy conditions, particularly due to gusts of wind orsurfaces they are produced on being shaken. Typically,these are dry spores of rust fungi and powderymildews butstrong gusts can also remove bacterial cells, such as P.syringae and spores such as Bacillus subtilis from leaves(Lighthart et al., 1993). Wind dispersal of passivelyreleased particles occursmainly frommid-morning to earlyeveningwhenwind-speeds are at its greatest. Since thewindspeed and direction is very variable in space and time,epidemics of diseases initiated by wind-dispersed propa-gules may vary considerably. Forecasting can be assistedby using wind-trajectory models such as Hysplit, forexample, as used to assess wind direction associated risk ofBotryits cinerea in Avignon, France (Leyronas and Nicot,2013), which found that air masses originating from theNorth or the South, that is, up or down the Rhone valley,brought more viable inoculum with potential to infecthorticultural crops thanwind from theWest.Wind is also amethod for dispersal of pathogens that are normallythought of as soilborne. Bacteria and viruses can be carriedon relatively large soil particles and plant debris, blownhundereds of metres to disperse them around fields andinto new fields (Peccia and Hernandez, 2006). Evenmicrosclerotia of pathogens such as Verticillium long-isporum have been reported to be blown up to distances ofhundereds of metres. Plant debris and pollen can alsovector plant-infecting viruses (see section Dispersal by

Vectors). See also: Fungal Spores; Powdery Mildews; TheRust FungiNormally, for spores dispersed at the field scale from

relatively small point, line or area sources, turbulence anddiffusion causes spore concentrations in air to spread outand dilute as they go downwind, which causes spore con-centrations to decline with distance from the source. This isoften described by a negative exponential or power func-tion but other functions have been described, and thereduction in spore concentration with distance varieshourly according to atmospheric conditions and filteringby crop canopies (McCartney et al., 2006). Care should betaken to interpret thresholds of spore concentrations totrigger disease control operations because a relatively highconcentration of spores could be caused by a very largedistant source (releasing spores over an entire region) or asmall source of spores very close to the sampler. Therefore,ideally decisions should be based either on more than onesampler, or a sampler that is buffered frompotentially closebut minor spore sources by mounting air samplers wellabove the ground or even on the roof of a tall building. Forcommonplant pathogens, it is possible to infer the presenceof airborne inoculum over a regional scale from a single airsampler located at rooftop height (West, 2012). However,it is not usually possible to use most types of air samplersfor biosecurity purposes to detect very rare influx of anexotic species from a distant source (Jackson and Bayliss,2011).Spores that escape into higher layers of the atmo-

sphere are available to be dispersed over long distances,often crossing oceans and continents (Pady and Kapica,1955; Gregory, 1973; Brown and Hovmøller, 2002).Long-distance transport of particles may be enhancedby natural events such as bushfires, which were implicatedin the spread of viable bacteria and fungal spores formore than 1450 km from Yucatan to Texas and fromSoutheast Asia to Hawaii (Mims and Mims, 2004).To remain viable, some of these are adapted to survivefreezing temperatures, highUV light levels and desiccation(Gregory, 1952). Some fungal spores and bacteriaare associated with ice-nucleation or enhanced condensa-tion of water on their surfaces, leading to snow or rainformation, which returns the spores to ground from highaltitudes (Frohlich-Nowoisky et al., 2009; Morris et al.,2013a, b). Owing to the use of deoxyribonucleic acid(DNA)-based analyses, bacteria are now thought to bemore prevalent in air thanwas understoodwhen theirmainmethod of detection was based on culturing (51% ofbacteria are able to be cultured in general media) (Despreset al., 2012). Species such as P. syringae may be present inair in sufficient concentrations to affect the hydrologicalcycle, by ice nucleation activity to induce rainfall to aidtheir dispersal. Owing to the fact that rain is the main wayhigh-altitude airborne spores can return to the Earth’ssurface, rain sampling methods have been developed tosample for long-distance transported plant pathogens suchas those causing cereal and soybean rusts (Barnes et al.,2006).

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Dispersal by Rain and Water

Rain-splash-dispersed pathogens are typically dispersedrelatively short distances from the sources of inoculum.This short-distance dispersal is primarily as ballistic drops,which are approximately 1mm or more in diameter. Thedistance these small droplets disperse depends on the sizeand speed of the incident raindrop, the effect of suspendedmicrobes and their exudates on the surface tension of thewater film that the raindrop impacts on, and the surface thewater film is on.The orientation, absorbency and texture ofleaves and other surfaces influence the splash process(McCartney et al., 2006). Yang et al. (1991a) demonstratedthat soft surfaces (such as straw), by cushioning someof thekinetic energy of the incident raindrop, splashed ballisticdrops shorter distances than those from hard surfaces(such as plastic matting). From leaves, ballistic dropsmostly travel a few centimetres and at most, in still air, cantravel only up to 120 cm reaching splashed heights560 cm(Macdonald and McCartney, 1987). Consequently, dis-persal gradients for splash-dispersed spores are generallymuch shorter than those for wind-dispersed spores. How-ever, in addition to ballistic drops, an aerosol of fine dro-plets 51mm in diameter are also produced. Althoughthese do not carry many spores per drop, much greaternumbers of these small droplets are produced, particularlyas a fine spray in extreme weather events such as tropicalstorms. This aerosolised spray is thought to explain howthe Asiatic citrus canker bacterium, Xanthomonas axono-podis pv. citri could be dispersed for between 3.5 and 10 kmin severe rainstorms and tropical storms in Florida(Gottwald et al., 2001, 2002). Spores of plant pathogensthat are adapted for dispersal by water are often producedin, or have a surface covered by, mucilage, which preventsdispersal by wind and reduces the surface tension of sporesuspensions to make the spore suspension more easilysplashed (Gregory, 1973; Fitt et al., 1989; Lovell et al.,2002). In addition to rain, water drops from irrigation orrolling off leaves higher in the canopy can create rain-splash dispersal. As a rain event continues, spores, beingreleased from an infection source may become depletedand those already dispersed may become secondarily dis-persed longer distances by further splashes. Eventually,long periods of rain may wash away most spores(McCartney et al., 2006). Splash dispersal of pathogensacross fields has been modelled in crop canopies, forexample, Yang et al. (1991b) and Saint-Jean et al. (2004).For example, Saint-Jean et al. (2008) found that modelledinfection by spores of Mycosphaerela graminicola (Zymo-septoria tritici) was reduced in a plot of cultivar mixturesrather than a single cultivar because a proportion of spore-carrying droplets were intercepted by a less compatiblecultivar.For many plant pathogens dispersed by air or rain-

splash, being washed into soil or into watercourses, such asstreams and rivers, is the end to their chance of infecting ahost. In contrast, of course, some pathogens specialise ininfectingwater andmarginal plants. It is amazing that such

plants are no more heavily infected by plant pathogens asmost pathogens require wetness for infection, so waterplants are permanently in perfect conditions for infectionto occur. Clearly, there are other mechanisms of resistancein aquatic plants that help to keep them healthy – perhaps,something that deserve to be studied more. Certainly thereis a problem of waterborne pathogens in irrigation waterand water in hydroponic systems and this has been impli-cated in economic losses of crops grown on land. Zappiaet al. (2013) reported finding various oomycetes and fungalplant pathogens in irrigation water, which was sprayedonto fields in Australia, including species of Phytophthora,Pythium, Colletotrichum, Fusarium, Leptosphaeria, Mor-tierella, Saprolegnia, and Paecilomyces. Root mat oftomato and cucumber is caused by bacteria such as Agro-bacterium biovar 1 and alsoOchrobactrum,Rhizobium andSinorhizobium in some hydroponically grown crops in theUK and France (Weller et al., 2006).

Soilborne Plant Pathogens

Many plant pathogens survive in soil as thick-walled rest-ing spores, or specialised survival structures, such assclerotia, or saprophytically on plant debris and organicmatter in the soil. Some fungi produce a network ofmycelium and more aggregated structures, such as rhizo-morphs of Armillaria mellea and hyphal chords of fungi inthe genus Hypholoma. Some of these are plant pathogensand can spread as mycelium and rhizomorphs, or bygrowing along infected roots to infect other roots. Thefungus Armillaria solidipes (known previously as Armil-laria ostoyae) is reported to be one of the world’s largestorganisms as one isolate was found to have colonised alarge area of woodland in Oregon, USA (Chiu et al., 2001)over a period estimated to be 2400 years and covering anarea of woodland of approximately 8.8 km2.

In addition, soilborne fungi may survive short periods inwater or air, assisting in dispersal when freak weathercauses either flooding or wind-blown dust. Soil pathogenscan be mapped by optical detection of their symptoms,allowing targeted treatment with biological control agentsor pesticides. This approach works well because soilbornepathogens are relatively static, moving only short distancesby themselves, and only occasionally further by animalsandmachinery, andwater orwind.Crop rotation is usuallythemainway to reduce the impact of soilborne diseases butoften the most profitable crops are grown too frequentlyleading to a build-up of this kind of disease and decline inyields. Some soilborne viruses can survive long periods,during crop rotations, and are dispersed within fungi andprotists, such as the Polymyxa species (see section Dis-persal by Vectors). Some important soilborne diseases arethe target for measures to prevent long-distance dispersalon machinery and plant material. For example, off-roadvehicles are required to be cleaned to prevent spread of thesoilborne oomycete Phytophthora cinnamomi in Australia,as this pathogen is one of the world’s most invasive species,

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causing root rot or dieback of many trees and shrubs.See also: Plant Viruses: Soil-borne

Introductions by People (Vehicles,Seed)

Introduction is themost important driver for emergence ofnew diseases in different pathogen groups (fungi, bacteria,virus and phytoplasmas) (Anderson et al., 2004). The term‘pathogen pollution’ was introduced by Anderson et al.(2004), to describe the anthropogenic movement ofpathogens resulting in a pathogen crossing a boundary thatpreviously provided geographical or ecological separation.Theremay then be greater impact of introduced pathogenson crop plant that could be relatively susceptible havingnot previously been exposed to the pathogen. A solution isto increase biosecurity, surveillance and quarantine checksand also to begin to anticipate introductions and breedresistance into cultivars grown in areas where the disease iscurrently absent. Such an approach was advocated by Fittet al. (2008) to reduce the impact of an introduction ofLeptosphaeria maculans on seed imported into China,where the pathogen is currently absent. Leptosphaeriamaculans causes stem canker or blackleg of oilseed rape orcanola and is one of the most important pathogens of thiscrop globally (West et al., 2001). Given the predictedcontinued increase in global air travel and trade volume,the number of introduced emerging diseases is also likely toincrease. As climate change will enable plants and patho-gens to survive outside their historic ranges, Harvell et al.(2002) predicted an increase in the number of invasivepathogens. For example, range expansion of grey leafblight of maize, caused by the fungus Cercospora zeae-maydis, was first noted during the 1970s, and subsequentlybecame the major cause of maize yield loss in the USA.Brown and Hovmøller (2002) described instances whereintroduction of infected plant material (followed by localdispersal of spores) had spread diseases to new continents,e.g. potato late blight (Phytophthora infestans) was trans-ported on imported tubers from Central America to Eur-ope in the 1840s, where it spread causing the potato blightfamine. This was augmented by import of the A2 matingtype by the same route in the mid-1970s. Another exampleis the spread of wheat yellow rust (P. striiformis) fromEurope to Australia in 1979 (by a plant breeder) (Brownand Hovmøller, 2002) and the introduction of L. maculansto Canada in the mid-1970s (also by a plant breeder) (Fittet al., 2008). See also: Phytophthora

Dispersal by Vectors

Virus diseases such as barley yellow dwarf virus are vec-tored by plant-feeding insects such as aphids. These canspread the pathogens in short distances within fields butmore importantly, seasonal migrations can disperse these

pathogens to more than hundreds of kilometres (Har-rington and Stork, 1995). The rate of dispersal within fieldsor plantations depends on the feeding activity of the vector.Insect families, such as Cicadellidea (leafhoppers), Ful-goridea (planthoppers) and Psyllidae (jumping plant lice)are often associated with vectoring of phytoplasmas, par-ticularly in tropical and subtropical countries. They aretaken up when the vector feeds on the phloem of infectedplants, leading to the phytoplasma entering the vector fromthe intestine and passing to the salivary glands, aided by anantigenic coating to evade the insect’s immune response(Suzuki et al., 2006). One unusual case for a fungal plantpathogen is that of ergot caused byClaviceps purpurea andits closely related species. Although the fungus spreads bymovement of ergots (a type of sclerotia) in batches of seed,and as air-dispersed ascospores, the fungus also reproducesasexually as conidia, which are produced in a sweet liquid,known as honeydew. Various insect vectors have beenfound to feed on the honeydew and to infect new flowers innearby crops. New vectors or new crops may facilitaterecombination of new virus diseases onto crops as manyviruses are able to recombine to produce new types ofviruses. This process is likely to increase due to climatechange, which will increase the range of different insectvectors, which may encounter viruses from different hostplants for the first time. An example of this has occurredrecently in Brazil due to the introduction of the B-biotypeof whitefly (Bemisia tabaci), which facilitated the vectoringof viruses present in different native plants onto cultivatedtomato crops in which they recombined to produce newvirus diseases (Fernandes et al., 2008). Plant viruses mayalso be vectored into plants by colonising fungi, protistsand also dispersed in air within pollen. For example, spe-cies of Polymyxa infect roots of cereals and some crucifersglobally, transmitting at least 15 plant viruses that causeeconomic yield loss, such as soilborne cerealmosaic, barleyyellow mosaic and beet necrotic yellow vein virus (Smith,2008). Shiller et al. (2010) describe a method to detectplant-infecting viruses, such as Tobacco ringspot virusfrom samples of pollen using quantitative reverse tran-scription polymerase chain reaction. See also: Inverte-brates and Fungi in Plant Virus Diseases; Plant VirusTransmission by Insects; Viruses and Plant Disease

Conclusion and Future Perspectives

A wide range of dispersal methods are used by plant patho-gens. Disease control relies on preventing introductions ofnew diseases through effective biosecurity and on separatingcrops from sources of inoculum in established locations.Natural methods of dispersal in air, water and vectors cantransport plant pathogens over long distances. Direct detec-tionof inoculumdispersedbyair, soil,water andon importedplant products is becoming increasingly possible due to fan-tastic advancements indiagnostics, suchasbiosensors, lateralflow devices and isothermal DNA assays, which can detectpathogens rapidly and on site (West et al., 2013).

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Acknowledgements

The author thanks the funding bodies: Defra, HGCA,TSB,EFSA, theEuropeanUnion and theBBSRC.Centre-left photo of rain in Figure 1 is used with permission and ispart of a photo taken by Prof John Lacey (RothamstedResearch).

References

Anderson PK,CunninghamAA, Patel NG et al. (2004) Emerging

infectious diseases of plants: pathogen pollution, climate

change and agrotechnology drivers. Trends in Ecology and

Evolution 19: 535–544.

Aubertot JN, West JS, Bousset-Vaslin L et al. (2006) Improved

resistancemanagement for durable disease control: a case study

of phoma stem canker of oilseed rape (Brassica napus). Eur-

opean Journal of Plant Pathology 114: 91–106.

Barnes CW, Szabo LJ, Johnson JL et al. (2006) Detection of

Phakopsora pachyrhiziDNA in rain using qPCRand a portable

rain collector. Phytopathology 96(6) : S9.

Brown JKM and Hovmøller MS (2002) Aerial dispersal of

pathogenson the global and continental scales and its impact on

plant disease. Science 297: 537–541.

Chiu ShiauYen, Lu JenYenn, Su YaoChi , Wu YingChang and

Chang HsiHsung (2001) The largest biological item on this

earth. Asia Seasonly Report of Environmental Microbiology

10(1): 17–20.

Despres VR, Huffman JA, Burrows SM et al. (2012) Primary

biological aerosol particles in the atmosphere: a review. Tellus

Series B: Chemical and Physical Meteorology 64: 15598.

doi:10.3402/tellusb.v64i0.15598.

Fernandes FR, de Albuquerque LC, Giordano LDB et al. (2008)

Diversity and prevalence of Brazilian bipartite begomovirus

species associated to tomatoes. Virus Genes 36: 251–258.

Fitt BDL, Hu BC and Li ZQ et al. (2008) Strategies to prevent

spread of Leptosphaeria maculans (phoma stem canker) onto

oilseed rape crops in China; costs and benefits. Plant Pathology

57(4): 652–664.

Fitt BDL,McCartney HA andWalklate PJ (1989) Role of rain in

the dispersal of pathogen inoculum. Annual Review of Phyto-

pathology 27: 241–270.

Frohlich-Nowoisky J, Pickersgill DA, Despres VR and Poschl U

(2009) High diversity of fungi in air particulate matter. Pro-

ceedings of the National Academy of Sciences of the USA

106(31): 12814–12819.

Gottwald TR, Hughes G, Graham JH , Sun X and Riley T (2001)

The citrus canker epidemic in Florida: the scientific basis of

regulatory eradication policy for an invasive species. Phyto-

pathology 91: 30–34.

Gottwald TR, Sun X, Riley T et al. (2002) Geo-referenced spa-

tiotemporal analysis of the urban citrus canker epidemic in

Florida. Phytopathology 92: 361–377.

Gregory PH (1952) Spore content of the atmosphere near the

ground. Nature 170: 475.

GregoryPH (1973)TheMicrobiology of theAtmosphere, 2nd edn.,

p. 377. Aylesbury: Leonard Hill.

Harrington R and Stork NE (1995) Insects in a changing envir-

onment: 17th Symposium of the Royal Entomological Society,

7–10 September 1993 at Rothamsted Experimental Station,

Harpenden, 535 pp. London: Academic Press.

Harvell CD,Mitchell CE,Ward JR et al. (2002) Climate warming

and disease risks for terrestrial and marine biota. Science 296:

2158–2162.

Huffman JA, Prenni AJ, DeMott PJ et al. (2013) High con-

centrations of biological aerosol particles and ice nuclei during

and after rain. Atmospheric Chemistry and Physics 13: 6151–

6164.

Ingold CT (1971) Fungal Spores: Their Liberation and Dispersal,

302 pp. Oxford: Clarendon Press.

Jackson SL and Bayliss KL (2011) Spore traps need improvement

to fulfil plant biosecurity requirements. Plant Pathology 60:

801–810.

Lacey J (1996) Spore dispersal – its role in ecology and disease: the

British contribution to fungal aerobiology. Mycological

Research 100: 641–660.

LaceyME andWest JS (2006) The Air Spora, 156 pp. Dordrecht,

The Netherlands: Springer.

Leyronas C and Nicot PC (2013) Monitoring viable airborne

inoculum of Botrytis cinerea in the South-East of France over 3

years: relation with climatic parameters and the origin of air

masses. Aerobiologia 29(2): 291–299.

Lighthart B, Shaffer BT, Marthi B and Ganio LM (1993) Arti-

ficial wind-gust liberation of microbial bioaerosols previously

deposited on plants. Aerobiologia 9: 189–196.

Lovell DJ, Parker SR, Van Peteghem P, Webb DA and Welham

SJ (2002) Quantification of raindrop kinetic energy for

improved prediction of splash-dispersed pathogens. Phyto-

pathology 92: 497–503.

Macdonald OC andMcCartney HA (1987) Calculation of splash

droplet trajectories Ag. Forest Meteorology 39(2–3): 95–110.

Marcroft SJ, Van de Wouw AP, Salisbury PA, Potter TD and

Howlett BJ (2012) Effect of rotation of canola (Brassica napus)

cultivars with different complements of blackleg resistance

genes on disease severity. Plant Pathology 61: 934–944.

McCartney HA, Fitt BDL andWest JS (2006) Dispersal of foliar

fungal plant pathogens: mechanisms, gradients and spatial

patterns. In: Cooke BM, Jones DG and Kaye B (eds) The

Epidemiology of Plant Diseases, 2nd edn, pp. 159–192. Dor-

drecht: Springer.

Mims SA and Mims FM (2004) Fungal spores are transported

long distances in smoke from biomass fires. Atmospheric

Environment 38: 651–655.

Morris CE, Monteil CL and Berge O (2013a) Novel under-

standing of the water cycle as a link between unsuspected

habitats of airborne pathogens – what consequences for plant

disease management? Acta Phytopathologica Sinica 43(suppl.):

17. International Congress of Plant Pathology 2013 abstract

O01.004.

MorrisCE, SandsDC,GlauxC et al. (2013b)Urediospores of rust

fungi are ice nucleation active at 4210 8C and harbor ice

nucleation active bacteria. Atmospheric Chemistry and Physics

13: 4223–4233.

Pady SM and Kapica L (1955) Fungi in air over the Atlantic

Ocean.Mycologia 47: 34–50.

Peccia J and Hernandez M (2006) Incorporating polymerase

chain reaction-based identification, population characteriza-

tion, andquantificationofmicroorganisms into aerosol science:

a review. Atmospheric Environment 40: 3941–3961.

eLS & 2014, John Wiley & Sons, Ltd. www.els.net6

Plant Pathogen Dispersal

Saint-Jean S, Chelle M and Huber L (2004) Modelling water

transfer by rain-splash in a 3D canopy using Monte Carlo

integration Ag. Forest Meteorology 121(3–4): 183–196.

Saint-Jean S, Kerhornou B, Derbali F et al. (2008) Role of rain-

splash in the progress of Septoria leaf blotch within a winter

wheat variety mixture. In: West JS and Burt PJ (eds) Applied

Aspects of Aerobiology. Harpenden, UK: Rothamsted

Research, 19 November 2008. Aspects of Applied Biology 89:

49–54.

Shiller JB,LebasBSM,HornerM ,PearsonMNandCloverGRG

(2010) Sensitive detection of viruses in pollen using conven-

tional and real-time reverse transcription-polymerase chain

reaction. Journal of Phytopathology 158(11–12): 758–763.

SmithMJ (2008) The Biology andMolecular Biology of Polymyxa

Species and their Interactions with Plants and Viruses. PhD

thesis, University of Warwick.

Suzuki S, Oshima K, Kakizawa S et al. (2006) Interactions

between a membrane protein of a pathogen and insect micro-

filament complex determines insect vector specificity. Proceed-

ings of the National Academy of Sciences of the USA 103(11):

4252–4257.

Weller SA, Stead DE and Young JPW (2006) Recurrent out-

breaks of root mat in cucumber and tomato are associated with

a monomorphic, cucumopine, Ri-plasmid harboured by var-

ious Alphaproteobacteria. FEMSMicrobiology Letters 258(1):

136–143.

West JS (2012) Aerobiology and air sampling in plant pathology.

Alergologia Immunologia 9: 80–81.

West JS, Heard S, Canning GGM, Fraaije BA and Hammond-

Kosack K (2013) New developments in identification and

quantification of airborne inoculums. Acta Phytopathologica

Sinica 43(suppl.): 16. International Congress of Plant Pathol-

ogy 2013 abstract O01.002.

West JS, Kharbanda PD, Barbetti MJ and Fitt BDL (2001) Epi-

demiology and management of Leptosphaeria maculans

(phoma stem canker) on oilseed rape in Australia, Canada and

Europe. Plant Pathology 50: 10–27.

Yang X, Madden LV, Reichard DL, Fox RD and Ellis MA

(1991b) Motion analysis of drop impaction on a strawberry

surface. Agricultural and Forest Meteorology 5: 67–92.

Yang XS,Madden LV and Brazee RD (1991a) Application of the

diffusion equation for modeling splash dispersal of point-

source pathogens. New Phytology 118(2): 295–301.

Zappia RE, Huberli D, Hardy GE and Bayliss KL (2013) Biose-

curity implications of plant pathogens in irrigation water. Acta

Phytopathologica Sinica 43(suppl.): 83. International Congress

of Plant Pathology 2013 abstract O04.011.

Further Reading

Agrios GN (2005) Plant Pathology, 5th edn., p. 952. Amsterdam:

Elsevier.

Web Links

http://ready.arl.noaa.gov/HYSPLIT.php

http://www.ars.usda.gov/Main/docs.htm?docid=14549

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Plant Pathogen Dispersal