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10.1146/annurev.ento.51.110104.151039
Annu. Rev. Entomol. 2006. 51:91–111
doi: 10.1146/annurev.ento.51.110104.151039
Copyright
c
2006 by Annual Reviews. All rights reserved
First published online as a Review in Advance on September 22, 2005
INSECT VECTORS OF PHYTOPLASMAS
Phyllis G. Weintraub
1
and LeAnn Beanland
2
1
Agricultural Research Organization, Department of Entomology,
Gilat Research Center, Israel 85280; email: phyllisw@volcani.agri.gov.il
2
Alson H. Smith, Jr., Agriculture Research and Extension Center,
Winchester, Virginia 22602; email: lbeanlan@vt.edu
KeyWords leafhopper, planthopper, mollicute, pathogen transmission
■ Abstract Plant diseases caused by, or associated with, phytoplasmas occur in
hundreds of commercial and native plants, causing minor to extensive damage. In-
sect vectors, primarily leafhoppers, planthoppers, and psyllids, have been identified
for relatively few phytoplasma diseases, limiting the capacity of managers to make
informed decisions to protect crops and endangered indigenous plants. In the past two
decades our knowledge of insect vector–phytoplasma interactions has increased dra-
matically, allowing researchers to make more accurate predictions about the nature and
epidemiology of phytoplasma diseases. These better-characterized systems also may
provide clues to the identity of insect vectors of other phytoplasma-associated diseases.
We review the literature addressing the ecology of insect vectors, phytoplasma-insect
ecological and molecular interactions, vector movement and dispersal, and possible
management strategies with an emphasis on research from the past 20 years.
INTRODUCTION
Phytoplasmas (originally called mycoplasma-like organisms) are important insect-
transmitted pathogenic agents causing more than 700 diseases, many of which are
lethal, in hundreds of plant species. Phytoplasmas are nonculturable degenerate
gram-positive prokaryotes closely related to mycoplasmas and spiroplasmas. A
large body of research has accumulated in the past 20 years that addresses the
biology, ecology, vector relationships, and epidemiology of crop diseases caused
by phytoplasmas. Despite the effort that has gone into understanding individual
diseases and phytoplasmas, a synthesis of the published information on the range
of studied systems has not appeared since Purcell’s (82) work, which raised and
addressed many questions about bacterial plant disease-vector relationships. In
this review, we provide an overview of the more recent developments regarding
the interactions between insect vectors and phytoplasmas and their plant hosts,
and the principles and mechanisms that govern them. In a comprehensive re-
view of phytoplasmas, Lee et al. (46) describe the 12 main groups of phytoplas-
mas (designated 16SrI–XII) and their subgroups (designated with a letter suffix,
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e.g., 16SrI-A). Note that there are many more described phytoplasmas than there
are identified vector species.
Three known mechanisms introduce phytoplasmas into the vulnerable tissue
of host plants: (a) vegetative propagation or grafting of infected plant material,
(b)vascular connections made between infected and noninfected host plants by
parasitic plants such as dodder (Cuscuta spp.) (22, 32), and (c)vector insects feed-
ing on noninfected host plants. Recent reports suggest a fourth possible source of
phytoplasma: seed transmission. Because phloem sieve elements lack any direct
connection to seeds, this form of transmission was assumed to be unlikely; how-
ever, lethal yellows phytoplasma has been detected in coconut fruit embryos from
infected trees (20) and alfalfa witches’ broom has been detected in alfalfa seeds
from phytoplasma-infected parent plants (40). We limit our discussion to the third,
the insect-phytoplasma relationship.
TAXONOMIC GROUPS OF PHYTOPLASMA VECTORS
The single most successful order of insect phytoplasma vectors is the Hemiptera.
This group collectively possesses several characteristics that make its members ef-
ficient vectors of phytoplasmas: (a) They are hemimetabolous; thus, nymphs and
adults feed similarly and are in the same physical location—often both immatures
and adults can transmit phytoplasmas. (b) They feed specifically and selectively on
certain plant tissues, which makes them efficient vectors of pathogens residing in
those tissues. Furthermore, their feeding is nondestructive, promoting successful
inoculation of the plant vascular system without damaging conductive tissues and
eliciting defensive responses. (c) They have a propagative and persistent relation-
ship with phytoplasmas. (d) They have obligate symbiotic prokaryotes that are
passed to the offspring by transovarial transmission, the same mechanisms that
allow the transovarial transmission of phytoplasmas.
Phytoplasmas are phloem-limited; therefore, only phloem-feeding insects can
potentially acquire and transmit the pathogen. However, within the groups of
phloem-feeding insects only a small number, primarily in three taxonomic groups,
have been confirmed as vectors of phytoplasmas (Table 1; follow the Supplemental
Material link from the Annual Reviews home page at http://www.annualreviews.
org). The superfamily containing the largest number of vector species is the Mem-
bracoidea, within which all known vectors to date are confined to Cicadellidae.
The second largest group is the Fulgoromorpha, in which four families of vector
species are found. The smallest suborder is Sternorrhyncha, in which only two
genera in the Psyllidae are confirmed vectors.
Morphological and molecular evidence indicates that the Membracoidea are
a monophyletic superfamily (24); however, the phylogenetic status and relation-
ships of the families, subfamilies, and tribes are poorly understood. The most
recent analyses, based on conservative 28S ribosomal subunit DNA sequences
(see figure 3 in Reference 24), and in agreement with morphological analysis (73),
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INSECT VECTORS OF PHYTOPLASMAS 93
place the subfamily Deltocephalinae as the most highly derived lineage. More than
75% of all confirmed phytoplasma vector species are found in this subfamily. The
feeding habits of species within the Deltocephalinae range from monophagous to
polyphagous, and members of this group can transmit one or more different phy-
toplasma taxa. The subfamily containing the second largest number of confirmed
vector species is the Macropsinae. Vector members of the Macropsinae can be
monophagous or oligophagous, but most feed primarily on woody plants. This
subfamily is more highly derived (following the molecular scheme) than all of the
remaining genera; the more basal genera of the Deltocephalinae have only one or
two vector species. However, in a comparison of the number of competent vectors
as a percentage of the total known species for a group, 10% of the Aphrodinae (a
less derived subfamily) are phytoplasma vectors, opposed to the Deltocephalinae,
which have only 0.8%.
On the basis of analysis of ribosomal DNA, the morphologically distinct mem-
bracids are part of the Cicadellidae; however, to date, no membracids have been
confirmed as or are suspected of transmitting phytoplasmas. Although membracids
are relatively poor transmitters of viruses compared with leafhoppers, it is unknown
whether researchers have not considered membracids for use in phytoplasma vec-
tor studies because they appear to be a group distinct from the leafhoppers (which
are known vectors) or because membracids actually do not transmit phytoplasmas.
Because membracids tend to feed on woody hosts, it would not be surprising to find
that they transmit phytoplasmas in the groups found primarily in woody plants:
Western-X (WX), Pear Decline (PD), Apple Proliferation (AP), or European Stone
Fruit Yellows (ESFY).
Vector species are found in four families of fulgorids: Cixiidae, Delphacidae,
Derbidae, and one species in the Flatidae. The first three families all have at
least one species that transmits a phytoplasma in the coconut lethal yellows group
(16SrIV). Several species in these families also transmit phytoplasmas from the
stolbur (Sr16XII) group. The one flatid vector, Metcalfa pruinosa (Say), transmits
aster yellows (AY) (group Sr16I).
Two genera of psyllids are vectors. Cacopsylla spp. transmit AP group (16SrX)
phytoplasmas to pome and stone fruit trees. AP phytoplasmas are the smallest,
with a genome size of 630 to 690 kbp (58), and it may be the case that psyllids
can transmit only smaller phytoplasmas. The same types of trees susceptible to AP
and ESFY are also susceptible to WX, which has a similar small genome size, but
to date psyllids have not been implicated in WX transmission. The other psyllid
genus has one vector species, Bactericera trigonica Hodkinson, which transmits
a stolbur (Sr16XII) phytoplasma to carrots (27).
It was once believed that, in order for an insect to transmit phytoplasma, it must
feed in the phloem in a nondestructive manner, but there are heteropteran vectors
that have a more destructive feeding pattern (64, 74). Two heteropteran families,
Pentatomidae and Tingidae, have confirmed vector species. Adults and nymphs
of the brown marmorated stink bug, Halyomorpha halys Stål (=H. mista Uhler),
can transmit witches’ broom phytoplasma to Paulownia spp. trees in Asia (33).
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The tingid Stephanitis typica (Distant) transmits a root wilt to coconut palms in
Southeast Asia (60).
IDENTIFYING VECTOR SPECIES OF PHYTOPLASMAS
Typically, when new phytoplasma diseases are discovered little is known about
the disease epidemiology. The first step in identifying the species of insects that
inoculate crops is to determine the suite of insects found in the vicinity of diseased
plants. Season-long monitoring must be conducted. The most common method to
monitor the insect population in and near crops is the use of sticky traps (100),
but sweep netting (79) and vacuum sampling (100), especially in field crops, are
effective survey techniques that yield live insects. To acquire live insects from trees,
shaking branches over collection trays will capture falling insects (13). Another
technique useful in phytoplasma vector studies is malaise trapping, which can
capture insects recalcitrant to other trapping methods. In addition, when placed at
the interface of two habitats, bidirectional malaise traps allow the determination
of net movement patterns of trapped insects (37) or movement between forest
vegetation and crops (3).
The relationship of species incidence and abundance with the incidence of dis-
ease can provide clues to the identity of vector species. Individual insects or groups
of insects can also be tested for the presence of phytoplasmas by molecular tech-
niques (56). Last, transmission experiments provide the most convincing evidence
of vector capacity of tested candidate vector species (89).
PHYTOPLASMA INSECT VECTOR INTERACTIONS
Insect Acquisition and Transmission of Phytoplasmas
Phloem-feeding insects acquire phytoplasmas passively during feeding in the
phloem of infected plants. The feeding duration necessary to acquire a sufficient
titer of phytoplasma is the acquisition access period (AAP). The AAP can be as
short as a few minutes but is generally measured in hours, and the longer the
AAP, the greater the chance of acquisition (82). The AAP may also depend on
the titer of phytoplasmas in the plants. Wei et al. (99) determined that there was
a sixfold increase in onion yellows phytoplasma per week in the plant after inoc-
ulation; however, they did not examine this effect on phytoplasma acquisition by
leafhoppers. Therefore, even though the phytoplasma titer could be quantified, it
is unknown how its titer in plants affects the AAP.
The time that elapses from initial acquisition to the ability to transmit the
phytoplasmas is known as the latent period (LP) and is sometimes called the
incubation period. The LP is temperature dependent and ranges from a few to
80 days (67, 70). During the LP the phytoplasmas move through and replicate
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INSECT VECTORS OF PHYTOPLASMAS 95
in the competent vector’s body. Phytoplasmas can pass intracellularly through the
epithelial cells of the midgut and replicate within a vesicle, or they can pass between
two midgut cells (49) and through the basement membrane to enter the hemocoel.
Phytoplasmas circulate in the hemolymph, where they may infect other tissues
such as the Malpighian tubules (53), fat bodies and brain (49, 71), or reproductive
organs (39); replication in these tissues, albeit not essential for transmission, may
be indicative of a longer coevolutionary relationship between host and pathogen.
Lefol et al. (48) demonstrated surface protein involvement, and some level of
specificity, in attachment of phytoplasma particles to insect host cells. Using double
dot blot DNA hybridization assays, they demonstrated that Flavescence dor´ee
phytoplasma acquired from infected broad bean (Vicia faba) strongly binds to the
alimentary tract tissues, hemolymph, and salivary glands but not to muscles or
genital organs of its insect hosts, Scaphoideus titanus and Euscelidius variegatus.
Other nonvector species also showed strong phytoplasma-insect tissue binding;
however, the tissues of nonhemipteran species did not react. The molecular factors
related to the movement of phytoplasmas through the various insect tissues are
unknown; however, Oshima et al. (76) developed a non-insect-transmissible onion
yellows phytoplasma and have shown that its gemone size (870 kbp) is smaller than
that of the wild-type phytoplasma (1000 kbp), which suggests that the mechanism
of binding to insect cells has been lost.
To be transmitted to plants, phytoplasmas must penetrate specific cells of the
salivary glands and high levels must accumulate in the posterior acinar cells of the
salivary gland before they can be transmitted (42). At each point in this process,
should the phytoplasmas fail to enter or exit a tissue, the insect would become
a dead-end host and would be unable to transmit the phytoplasmas. To illustrate
this point, Wayadande et al. (96) showed that in the salivary glands alone there
are three barriers that pathogens must traverse before they can be ejected with
the saliva: the basal lamina, the basal plasmalemma, and the apical plasmalemma.
Leafhoppers can be infected with a phytoplasma and yet be unable to transmit it
to healthy plants (48, 93, 94), perhaps because of the salivary gland barriers.
Phytoplasma transmission from a competent host during feeding can be indi-
rectly “observed” and separated into its component stages by electrical penetration
graph monitoring (5). In this technique, the monitor introduces a low-voltage cur-
rent into the test plant, and the insect is connected to the monitor via a gold wire.
When the insect’s stylets penetrate the leaf, the electrical circuit is closed. The
insect’s resistance to the applied signal (or biopotentials within the insect or plant)
varies with different feeding behaviors. Therefore, as the stylets perform different
activities, or penetrate different plant tissues, changes in voltage can be detected
and quantified. Types of stylet movements, salivation, ingestion, and egestion ap-
pear as different waveforms (5). For instance, as leafhoppers or planthoppers feed,
they constantly secrete a small amount of sheath saliva into the leaf environment
that encases and protects the delicate stylets when it solidifies. The release of sheath
saliva can be monitored (4, 12, 52). Phytoplasmas (or other circulative pathogens)
are introduced into the phloem probably via watery saliva as the leafhopper stylets
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penetrate sieve element membranes (52). Researchers can rigorously quantify both
the duration and frequencies of this particular behavior, and other behaviors, us-
ing electrical penetration graph monitoring (5). This technique allows the detailed
study of all elements of insect transmission of phytoplasmas as well as other plant
pathogens.
Some of the same leafhopper species that are competent to transmit phytoplas-
mas can also transmit viruses, rickettsia-like organisms, and spiroplasmas. For
example, Circulifer tenellus transmits beet curly top hybrigeminivirus (95), phy-
toplasma (101), and Spiroplasma citri (43). It is unknown whether the receptors
that allow penetration of these different pathogens into insect midgut cells are the
same. Phytoplasmas cannot be cultured in vitro (58), but the closely related group
spiroplasmas can; hence, more is known about the biology of spiroplasma–insect
vector interactions (10, 26).
Is the Vector-Phytoplasma Relationship Specific?
The interaction between insects and phytoplasmas is complex and variable. The
complex sequence of events required for an insect to acquire and subsequently
transmit phytoplasmas to plants suggests a high degree of fidelity between insect
vector species and the phytoplasmas that they transmit. However, numerous phyto-
plasmas, such as AY and WX strains in North America, are transmitted by several
different insect species (25, 45). In addition, a single vector species may transmit
two or more phytoplasmas, and an individual vector can be infected with dual or
multiple phytoplasma strains (45; L. Beanland, unpublished data).
Vector–host plant interactions also play an important role in determining the
spread of phytoplasmas. Polyphagous vectors have the potential to inoculate a
wider range of plant species, depending on the resistance to infection of each host
plant. Several studies (9, 59) have shown that insects that normally do not feed on
certain plant species can acquire and transmit phytoplasmas to those plants under
laboratory conditions. Hence, in many cases, the host range of a vector, rather
than lack of phytoplasma-specific cell membrane receptors, limits the spread of
phytoplasmas by that species
Bosco et al. (9) found that leafhoppers are not able to acquire equally phy-
toplasmas from different infected plant species. Chrysanthemum yellows (CY)
phytoplasma is successfully transmitted by three leafhoppers: Euscelidius varie-
gatus, Macrosteles quadripunctulatus, and Euscelis incisus. All three leafhopper
species acquire from and transmit to CY-infected chrysanthemum and uninfected
chrysanthemum, respectively. However, only M. quadripunctulatus and E. varie-
gatus acquire CY after feeding on CY-infected periwinkle and subsequently trans-
mit CY to uninfected plants. None of the leafhoppers acquire the phytoplasma
from CY-infected celery, a dead-end host. Dead-end hosts are plants that can be
inoculated and subsequently become infected with phytoplasma, but from which
insects can not acquire phytoplasma. Several other dead-end hosts have been iden-
tified (e.g., AY from Cyclamen persicum L.) (2). Grapevine is a dead-end host for
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INSECT VECTORS OF PHYTOPLASMAS 97
the stolbur (Stol) phytoplasma associated with bois noir and vergilbungskrankheit
grapevine yellows (GY) transmitted by the planthopper Hyalesthes obsoletus
(E. Boudon-Padieu & M. Maixner, personal communication).
The mechanisms that prevent phytoplasma acquisition from dead-end plant
hosts are not well understood. One factor may be the absence of phytoplasmas
in some plant parts. Wei et al. (99) demonstrated that when a leafhopper inocu-
lated a middle leaf of an eight-leafed garland chrysanthemum, the phytoplasmas
migrated into the main stem, apex, and roots quickly (2 days) but required about
3 weeks to infect all leaves. Conversely, Siddique et al. (87) found that phyto-
plasma was never detected in papaya leaves that were mature before the plant was
infected. Behavioral studies may also provide an explanation. Leafhoppers alter
feeding patterns depending on the plant host (5), and changes in feeding behavior
may influence the titer of ingested phytoplasmas (or whether the phytoplasmas
are ingested at all). The phytoplasma and virus vector Nephotettix virescens feeds
primarily from phloem in rice but occasionally consumes some xylem sap; how-
ever, in virus-resistant cultivars, it switches to feeding primarily from xylem (41).
Leafhoppers do not feed as readily in the phloem of nonpreferred host plants (16),
which suggests a mechanism to explain why only some plants are phytoplasma ac-
quisition hosts. Finally, phytoplasma symptoms are correlated with plant hormonal
imbalances (78) and altered carbohydrate and amino acid movement in plants (17,
50); hence, the infection may cause systemic changes but phytoplasma may not be
present in symptomatic plant parts. Alternatively, biochemical imbalances caused
by phytoplasma infection may impede phytoplasma acquisition.
Although there are no reports of vectors selectively acquiring one phytoplasma
from a host plant infected with more than one phytoplasma strain, when given
short AAPs on lettuce infected by more than one strain of phytoplasma, Macroste-
les quadrilineatus Forbes could acquire and subsequently transmit a single strain
(104), the result of short feeding periods rather than selective acquisition or trans-
mission. Multiple phytoplasma infections in plants can complicate transmission
studies performed to determine vector identity. Zhang et al. (104) provide a useful
methodology to compensate for confounding dual or multiple infections.
Transovarial Transmission
Although plant pathogenic viruses and symbiotic prokaryotes can be transovarially
transmitted, phytoplasmas were not thought to be directly transmitted from female
vector to progeny. However, in recent years several investigators have reported
instances of transovarial transmission of phytoplasma. Phytoplasma-infected S. ti-
tanus Ball (a vector of GY in Europe) females were allowed to lay eggs on healthy
host plants and hatched nymphs were transferred to healthy host plants. All devel-
opmental stages, including adults, were infected and transmitted phytoplasma (1).
Kawakitaet al. (39) used electron microscopy to observe phytoplasma in the ovaries
and other tissues of Hishimonoides sellatiformis and confirmed their presence by
PCR. They also found phytoplasmas in eggs laid on mulberry shoots by inoculative
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leafhoppers and in first-instar nymphs hatched from these eggs. Working with the
same leafhopper, Mitsuhashi et al. (65) found Wolbachia coexisting in all tissues
with the phytoplasma, suggesting that this other prokaryote may have mediated
infection by the phytoplasma. Infective Matsumuratettix hiroglyphicus have been
reared for two generations on phytoplasma-free sugarcane grown from tissue cul-
ture (31). In all of these cases there is absolute fidelity between insect vector and
the phytoplasmas; these species do not transmit any additional phytoplasmas.
Effects of Phytoplasma on the Vector
The phytoplasma-insect relationship can be beneficial, deleterious, or neutral in
terms of its impact on the fitness of the insect host. Early reports suggested that
infection by phytoplasmas was harmful to insect hosts (85). More recent reports
suggest that phytoplasmas may confer some increased fitness to their insect hosts.
Beanland et al. (7) determined that exposure to one strain of AY increases both
the lifespan and fecundity of female M. quadrilineatus;however, exposure to
another strain of AY increases the lifespan of test insects but not the number of
offspring produced. The corn leafhopper, Dalbulus maidis,isaspecialist of corn
that cannot live on unrelated hosts such as healthy aster (Callistephus chinensis
Nees). However, when reared on several strains of AY-infected aster, its lifespan is
increased. Once exposed to AY-infected asters, D. maidis can feed and survive on
healthy aster as well (83). The effects of phytoplasma infection on the insect hosts
have implications for the incidence and spread of disease. Longer lived vectors
have the opportunity to infect more plants and produce more offspring.
Phytoplasma infection can have different effects on different species of vec-
tors. Madden et al. (55) reported that maize bushy stunt phytoplasma had a less
deleterious effect on its primary vector, B. elimatus, than on a secondary vector,
D. maidis.Environmental factors, such as temperature, can also mediate the effects
of phytoplasma infection on the insect host. Garcia-Salazar et al. (28) reported that
X-disease phytoplasma infection can be deleterious to the vector Paraphlepsius
irroratus at low temperatures but not at temperatures ranging from 25 to 30
◦
C.
Those phytoplasmas that reduce the fitness of their host insects may have had a
shorter evolutionary relationship with that insect species, as selection would re-
duce the deleterious effects on insect hosts. Only those phytoplasmas that do not
kill their hosts would survive to be introduced into a plant host and subsequently
acquired by another vector.
It can be difficult to separate the effects of phytoplasma on the food quality of
the plant host from the direct effects on the insect vector. However, if phytoplasma-
infected insects are transferred to uninfected plants at frequent intervals (i.e., be-
fore phytoplasma infection alters the host plant), the effects of phytoplasmas on
insect survival and fecundity can be observed. Phytoplasma infection may al-
ter the infected plant in such a way as to make it a more suitable host for the
insect, for example, reduction of the plant’s chemical defenses which would other-
wise repel phloem-feeders or reduce the fitness of insect herbivores. Alternatively,
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INSECT VECTORS OF PHYTOPLASMAS 99
phytoplasma infection may increase the titer of easy-to-digest nutrients such as
free amino acids and sugars in plant hosts that are available to vector species.
Fitness benefits may increase the relative attraction of infected plant hosts. Todd
et al. (90) reported a higher attraction to yellow plants by leafhoppers; because
symptoms of phytoplasma infection in plants usually include chlorosis, infected
plants are likely more attractive to insects, including vector species.
Factors Mediating Vector Capacity
For years investigators have found that leafhopper gender can influence the ac-
quisition and transmission dynamics of phytoplasma (14, 15, 88). At three scales
of investigation, Beanland et al. (6) reported that female M. quadrilineatus were
more efficient at transmitting AY to lettuce than were males. When test insects were
tested in three arenas of increasing scale—(a) confined in leaf cages, (b) placed
in larger cages with four lettuce plants, or (c) introduced into greenhouse sections
housing dozens of plants—results were consistent.
Beanland et al. (6) also determined that female leafhoppers were less likely than
males to acquire phytoplasma during feeding. The male and female leafhoppers
used in these trials may have transmitted at an equal rate if they had been tested
at an older age, as Lefol et al. (49) observed phytoplasma at an earlier age and
at a higher titer in male E. variegatus salivary glands than in those of female
E. variegatus. Behavioral differences between male and female vector insects can
account for observed gender differences and can affect plant disease dynamics
(36). Males move around more on each plant, and also more frequently from plant
to plant, in search of females.
Although early reports suggested that vector age did not influence vector ca-
pacity (16), more recent investigations suggest that age is an important factor.
Newly hatched nymphs of E. variegatus do not acquire CY with the same effi-
ciency as fifth-instar nymphs (77). In some cases, transmission is increased when
phytoplasmas are acquired by nymphs than by adults (66, 67). Phytoplasma strain
and environmental conditions are factors that may interact with vector age in the
capacity of leafhoppers to transmit phytoplasmas (67).
PHYTOPLASMA VECTOR DISPERSAL
Landscape and Local Vector Dispersal and Distribution
Spatial ecology is a science in its infancy; the movement of insect vectors, and
the complexities of the impact of the agrolandscape on that movement, are slowly
being teased into their component parts (91). As with any tritrophic relationship,
the components of a phytoplasma disease system must overlap: vulnerable host
plant in time (season) and space (geography), pathogen, and vector. Environmental
conditions mediate the activity and contribution of each of the three components.
It is axiomatic that an insect would not simply leave suitable host plants and
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disperse unless constrained by biotic (e.g., crowding, developmental stage, a ge-
netic tendency to engage in migratory behavior) or abiotic factors. Brcak (11)
observed H. obsoletus to remain on bindweed (Convolvulus arvensis) until the
plants were spent; only then did they disperse to alternative host plants nearby. At
the field scale, movement of vectors can be influenced by the dispersion of host
plants. According to Power (81), shorter distances between preferred plants in-
crease the likelihood that an insect moves from one to the other. Vector movement
and dispersal also influence the insect-pathogen interaction. Hoy et al. (35) docu-
mented the migration of M. quadrilineatus from northern Mexico/southern Texas,
acquiring phytoplasma en route, to infect crops in the Great Lakes area of Canada
and the midwestern United States. As an additional layer to this complex system,
there are primary and minor insect vectors; the primary vector transmits the phy-
toplasma to the economic crop, whereas the minor vector(s) inoculates noncrop
plant hosts that serve as reservoirs of the phytoplasma. Although these two classes
of vectors have seldom been identified for any crop-phytoplasma system, they are
likely important in most plant diseases.
Habitat Components of Phytoplasma Disease Epidemiology
Vegetation composition, habitat diversity, and the nature of ecotones in and near a
phytoplasma-vulnerable crop can have profound effects on the presence and dis-
persal of vectors, their natural enemies, and other insects. For instance, in aged
Chardonnay vineyards bordering a riparian forest, Nicholls et al. (72) found that
a corridor of plants and forest edge affected the distribution of the nonvector
leafhopper Erythroneura elegantula Osborn and generalist insect predators. The
proximity to corridors of forest vegetation had a positive influence on the number
of predator species that moved into the vineyards. Malaise trap captures in tropical
areas revealed that leafhoppers move into pasture land from nearby forest veg-
etation (37). Furthermore, Langer et al. (44) showed that the weed composition
around a field affected the level of phytoplasma-infected H. obsoletus, the vector
of GY in grapes; 30% to 60% of the planthoppers were infected when there was a
prevalence of Convolvulus arvensis,1%to7%when Ranunculus bulbosus was the
predominant weed, and 1% to 10% when Urtica dioica was the predominant weed.
While forests and plant corridors may increase predatory species and biodiversity,
they also augment the movement of phytoplasma vector species into nearby vine-
yards. In Virginia, a study of the movement of phloem-feeding insects across a
forest vineyard ecotone suggests which species may be responsible for infecting
wine grapes with GY phytoplasmas. Scaphoideus titanus, Osbornellus auronitens
Provancher, and Jikradia olitorius Say exhibit seasonal movement into the vine-
yard from nearby forest vegetation, which could account for the high incidence of
diseased vines observed near the vineyard edge (L. Beanland, unpublished data).
In North America, S. titanus is found primarily on native Vitis spp. (57) that often
harbor both S. titanus and the phytoplasmas found in diseased cultivated vines
(23). Because wild-collected S. titanus has tested positive for phytoplasma in PCR
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INSECT VECTORS OF PHYTOPLASMAS 101
assays, this species is likely one vector of GY in North America (L. Beanland, un-
published data). Lessio & Alma (51) recently examined the movement of S. titanus,
within an Italian vineyard and reported that planting densities and canopy density
affect vector movement. Furthermore, they found that S. titanus did not disperse
significantly beyond 24 m from the vineyard. Their findings suggest that increas-
ing the distance between wild hosts of S. titanus and vineyards may reduce the
movement of this insect to cultivated vines.
The movement of vectors from forest habitat to crop is important in the in-
cidence and spread of phytoplasma diseases in other cropping systems as well.
In Connecticut, vector leafhoppers of Peach X-disease move into orchards from
wild plant hosts in the spring (61, 62). Within-crop vegetation, such as the types
of plants found in an orchard floor, can also influence the entry and tenure of
vector species. During the summer the species of plants found under peach trees
influenced the abundance of leafhopper vectors that colonized trees (63). In North
Carolina, Scaphytopius magdalensis (Provancher), a vector of blueberry stunt dis-
ease, shows seasonal migration patterns between wild blueberry hosts in forests
and cultivated blueberries, although the role of wild blueberry in the epidemiology
of blueberry stunt is not clear (102).
Unlike weather conditions in North America and Europe, the desert climate of
Israel mitigates against the abundance of weeds in the vicinity of vineyards, so
vectors must disperse or migrate over large areas to find suitable plant hosts. Spatial
autocorrelation analysis of the distribution in Israeli vineyards of the phytoplasma
vector species Neoaliturus fenestratus and the suspected vector species Megoph-
thalmus scabripennis showed significant clustering of leafhoppers captured on
sticky traps. Analyses also revealed the seasonal movement of these species from
various locations around the vineyard to the north-east boundary (75).
Spatial Characteristics of Phytoplasma-Infected Crops
Spatial patterns of phytoplasma-infected vines within vineyards have been inves-
tigated by several groups, and a clustered pattern of GY-infected plants has been
observed (19, 103). In each system, insects are the suspected agents of spread-
ing the disease-causing phytoplasmas. Clustering is also observed in AY-infected
lettuce plants in the Midwest of North America. The plants inoculated by the
vector M. quadrilineatus are often clustered, and their distribution follows a beta-
binomial distribution (8, 56). In this case, inoculative leafhoppers move into a
lettuce field, feed upon and subsequently inoculate a lettuce plant, engage in
small-scale movement to adjacent plants, and feed and infect them before en-
gaging in more long-range movement out of the immediate area. The distribution
of phytoplasma-infected plants can give clues to the identity, behavior, and source
of vector insects. For instance, Jarausch et al. (38) predicted that aerial vectors were
responsible for the spatial distribution of ESFY-infected Prunus trees in France
because the disease was initially found in various locations in the orchard with no
apparent border effects.
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102 WEINTRAUB
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Human-Mediated Spread of Phytoplasmas
Human activities have introduced vector species into previously unoccupied areas,
resulting in devastating phytoplasma-caused plant diseases. There is no question
that phytoplasmas have been present in France for decades, and the phytoplasma
causing Flavescence dor´ee is probably endemic to Europe. When the eggs of the
monovoltine Vitis specialist S. titanus were unintentionally brought to Europe on
imported grapevine canes from North America, GY became an epidemic disease in
France—and is spreading as the leafhopper disperses. Although S. titanus transo-
varially transmits phytoplasma (see above), it is doubtful that a phytoplasma new
to Europe was transmitted from North America with the leafhopper. S. titanus
likely acquired phytoplasma from infected plants in the vicinity of vineyards to
initiate the epidemic, or perhaps vines were infected at very low levels before S.
titanus arrived. Species in the genera Euscelis and Eusclidius can also transmit
GY and may serve as the minor vectors in this disease system.
DEVELOPING TECHNOLOGIES
Recently Developed Detection Tools
Because phytoplasmas are unculturable, Koch’s postulates cannot be satisfied and,
as a result, many aspects of their biology are poorly known. To circumvent these
problems, in the past 15 years numerous molecular techniques have been devel-
oped and applied to phytoplasma research; foremost among them is PCR. Based on
the conservative nature of ribosomal DNA across all prokaryotic organisms, total
DNA from plants or insects is used as a template for short synthetic primers. Uni-
versal primers amplify sequences common to all phytoplasmas and can be used to
determine if phytoplasma DNA is present (47). Specific primers amplify some of
the variable regions and have been developed for most of the phytoplasma groups
(54). With restriction fragment length polymorphism analysis, enzymatic digests
of amplified DNA products of PCR assays can be electrophoretically separated to
reveal patterns specific to different groups of phytoplasmas and even differences
in a specific phytoplasma isolated from different plant sources (44). To increase
specificity, nested PCR, in which amplification by one primer is followed by ampli-
fication with a second more specific primer or one that amplifies a smaller sequence
within the first product, has been developed to multiplex nested PCR, in which
multiple primers are used (21). Real-time PCR is a technique researchers are only
beginning to use; it has so far been employed to quantify the movement and multi-
plication of phytoplasma in plants (18, 98) and could be applied to insect vectors.
Although PCR is a specific and relatively quick method for detecting and char-
acterizing phytoplasmas, there are several problems: Any insect feeding on an in-
fected plant can test positive because of the phytoplasma present anywhere along
its digestive tract, and neither a dead-end host nor a vector in a latent period (LP)
can be distinguished from an infective or inoculative vector. In addition, remnants
of phytoplasma DNA remaining after the phytoplasma is no longer viable may be
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INSECT VECTORS OF PHYTOPLASMAS 103
amplified as well. Webb et al. (97) developed in situ PCR (on fixed and sectioned
plants and on whole insects) using 20- to 24-mer oligonucleotide primers. Their
findings from studies using in situ PCR were in strong agreement with previous
electron microscopic and immunochemical studies. This technique allows for a
more efficient and effective study of the biology and epidemiology of multiple
infections in a single host and of the events leading to transovarial transmission.
It is unclear why a technique widely used by microbiologists (68) has yet to be
embraced by phytoplasma researchers. Individual bands of amplified PCR products
are separated by denaturing gradient gel electrophoresis (DGGE) in a technique
also known as genetic fingerprinting. DNA fragments are separated on the basis of
their decreasing electrophoretic mobility in a linear urea/formamide gel gradient
or by a linear temperature gradient. With this technique, oligonucleotide probes
for detecting specific phytoplasma groups or PCR primers could be synthesized
on the basis of the sequences of the DNA fragments. Researchers have used this
procedure in investigations on the many bacteria-type symbionts and pathogens
found in ticks (84) and it should be equally useful to phytoplasma researchers.
Well-established serological techniques have been used in phytoplasma inves-
tigations often without success. The low phytoplasma titer in insects and plants,
and the presence of host-derived antigens, resulted in the production of polyclonal
antibodies with insufficient titer and low specificity and/or cross-reactivity with
hosts. The use of monoclonal antibodies, specific to phytoplasma groups, has
overcome some of the problems associated with the use of polyclonal antibodies.
Unfortunately, monoclonal antibodies can cross-react with other phytoplasmas
(30). A new technique based on putting a phytoplasma gene fragment into a bacte-
ria vector (Escherichia coli) that subsequently expresses the genes that produce an
abundance of pure proteins from which antibodies are made has proven successful
(98). The authors developed antibodies to the SecA membrane protein, which is
unique to bacteria (prokaryotes) and central to the process of protein secretion
from cell membranes. Because the SecA antibodies react to phytoplasma, their
use in assays allowed the investigators to detect and trace the progress of a phyto-
plasma infection in plants. This technique could also be used to develop specific
and high-titer antibodies for specific phytoplasmas.
Before the vector competence of an insect species is established, it is necessary
to perform biological transmission studies on test plants under natural conditions.
Test plants must be receptive or vulnerable to phytoplasma infection when the test
insect species is in the field. Even under controlled conditions, transmission assays
are time-consuming because symptom development in the plant may take weeks
or months. Zhang et al. (105) developed a rapid, nondestructive method of identi-
fying inoculative insect species by allowing them to feed through a membrane on
buffered sucrose media and then using PCR to test the media for presence of phy-
toplasmas. Recently, Ge & Maixner (29) tested a number of vector and nonvector
species using both membrane-feeding assays and traditional transmission assays.
The transmission rate for two vectors of grape phytoplasmas was more than four
times higher in the artificial medium. Differences between the two methodologies
must be taken into account when analyzing results of artificial media assays.
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104 WEINTRAUB
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Phytoplasma/Vector Management
Until recently, management of plant diseases caused by phytoplasma has focused
on controlling the vector by insecticides. A method to reduce alternative vector
host plants and/or reservoirs of phytoplasma-infected crop plants and weeds is by
roguing. Uyemoto et al. (92) found that by spraying WX-infected trees with insec-
ticide before roguing, the incidence of disease spread was significantly reduced.
Chemical control of vectors likely will continue for the foreseeable future, but
vector management or management of phytoplasma spread within the plant is now
slowly shifting to habitat management and the use of genetically modified crops.
Habitat management can reduce pest incidence. The type of mulching materials
used around coconut trees influences the abundance of the planthopper vector of
lethal yellows, Myndus crudus. Fewer nymphs are found around trees mulched
with coarse materials such as pine bark nuggets (34). Although some parasitoids
of leafhoppers have been identified, no studies have investigated the use of these
natural enemies to effectively manage pest species. Unfortunately, the vegetation
that can increase the incidence and abundance of natural enemies of vectors can
also be favorable to those taxa that transmit phytoplasmas. More effort should be
made to determine those elements of the cropping environment that enhance the
survival of natural enemies but do not increase vector numbers.
Genetic modifications may include enhancement of genes naturally present
within the plant that code for defensive compounds or the introduction of alien
genes into crop plants. The enhanced or introduced genes provide protection from
the vector insect or the pathogenic phytoplasma. We limit our discussion to genetic
modifications that have direct effects on vector insects.
Rice is attacked by two planthoppers (Sogatella furcifera and Nilaparvata lu-
gens) and one leafhopper (Nephotettix cinciteps) that cause direct feeding dam-
age and transmit viruses, phytoplasmas, or both. Powell et al. (80) demonstrated
that plant lectins, in particular Galanthus nivalis agglutinin (GNA, or snowdrop
lectin), are highly toxic to planthoppers. Nagadhara et al. (69) have shown that
GNA-expressing transgenic rice significantly reduced the survival, development,
and fecundity of the planthopper Sogatella furcifera and had substantial resistance
against the other two planthoppers. Reduction of the planthopper populations re-
duces not only the spread of pathogens but also the production by planthoppers
of honeydew, which enhances the growth of mold and fungus. The expression
of GNA was stable throughout the growth and development of the plants, which
grew to maturity with normal vigor and seed fertility. This research has far-reaching
implications for almost half the world’s population, who depend on rice as their
dietary staple. The insertion of this gene into other crop plants could have similarly
significant effects.
There is evidence that rootstock may affect vector response to plants. Annual
mapping of phytoplasma infections in a vineyard in Israel led to the discovery that
plants on Richter 110 rootstock had less phytoplasma incidence than did plants on
Castel 216 (P.G. Weintraub, unpublished data). Detached H. obsoletus antennae
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INSECT VECTORS OF PHYTOPLASMAS 105
stimulated by volatiles isolated from cabernet sauvignon on these two rootstocks
revealed that there was less reaction to Richter 110 than to Castel 216 (86). This is
an avenue that bears further exploration, since most woody crop plants are grafted
on rootstocks.
CONCLUSIONS
There is much to be learned from compiling and synthesizing research results on
phytoplasmas. Most phytoplasma vectors are members of the Cicadellidae; how-
ever, this is one of the largest insect families, with ∼25,000 species, and taxonomic
relationships of subfamilies and tribes are not at all clear. Unfortunately, this con-
fusion hinders the ability to predict which species are likely to be vectors. Focus
on vector species usually occurs when economic crops are affected, which may
skew our understanding of the true range of vector species. Work on noneconomic
plants, other than those weeds associated with crops, is seldom if ever performed;
hence, untold vector species may be overlooked. Vector studies must be expanded
to include a variety of plant phloem-feeders, including the Membracidae. The
vector-pathogen relationship is complex, and the inability to culture phytoplasmas
hinders rapid advancement. However, not only should new tools be applied to the
insect vectors to quantify and follow phytoplasma development in plants, but these
studies should determine how phytoplasma titers in the plant affect acquisition by
leafhoppers and subsequent development in the vector. The primary means of con-
trolling phytoplasma vectors is by insecticides; however, increasing pressure to
find less toxic and more biologically based techniques to control, or at least man-
age, insect vectors necessitates an even greater reliance on solid understandings
of the biology of insect vectors from the cellular to the ecological level.
ACKNOWLEDGMENTS
The authors thank Elaine Backus (USDA-ARS, Parlier, CA) for help with EPG
monitoring, Michael Wilson (National Museums & Galleries of Wales, Cardiff,
United Kingdom) for reviewing the taxonomic section, and Janis Yoseph (ARO,
Israel) for reviewing the references and producing the supplemental table. We
apologize to authors whose work we could not cite because of page limitations.
The Annual Review of Entomology is online at http://ento.annualreviews.org
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Annual Review of Entomology
Volume 51, 2006
CONTENTS
SIGNALING AND FUNCTION OF INSULIN-LIKE PEPTIDES IN INSECTS,
Qi Wu and Mark R. Brown 1
PROSTAGLANDINS AND OTHER EICOSANOIDS IN INSECTS:BIOLOGICAL
SIGNIFICANCE, David Stanley 25
BOTANICAL INSECTICIDES,DETERRENTS, AND REPELLENTS IN
MODERN AGRICULTURE AND AN INCREASINGLY REGULATED
WORLD, Murray B. Isman 45
INVASION BIOLOGY OF THRIPS, Joseph G. Morse and Mark S. Hoddle 67
INSECT VECTORS OF PHYTOPLASMAS, Phyllis G. Weintraub
and LeAnn Beanland 91
INSECT ODOR AND TASTE RECEPTORS, Elissa A. Hallem, Anupama
Dahanukar, and John R. Carlson 113
INSECT BIODIVERSITY OF BOREAL PEAT BOGS, Karel Spitzer
and Hugh V. Danks 137
PLANT CHEMISTRY AND NATURAL ENEMY FITNESS:EFFECTS ON
HERBIVORE AND NATURAL ENEMY INTERACTIONS, Paul J. Ode 163
APPARENT COMPETITION,QUANTITATIVE FOOD WEBS, AND THE
STRUCTURE OF PHYTOPHAGOUS INSECT COMMUNITIES,
F. J. Frank van Veen, Rebecca J. Morris, and H. Charles J. Godfray 187
STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN,
Susan E. Fahrbach 209
EVOLUTION OF DEVELOPMENTAL STRATEGIES IN PARASITIC
HYMENOPTERA, Francesco Pennacchio and Michael R. Strand 233
DOPA DECARBOXYLASE:AMODEL GENE-ENZYME SYSTEM FOR
STUDYING DEVELOPMENT,BEHAVIOR, AND SYSTEMATICS,
Ross B. Hodgetts and Sandra L. O’Keefe 259
CONCEPTS AND APPLICATIONS OF TRAP CROPPING IN PEST
MANAGEMENT, A.M. Shelton and F.R. Badenes-Perez 285
HOST PLANT SELECTION BY APHIDS:BEHAVIORAL,EVOLUTIONARY,
AND APPLIED PERSPECTIVES, Glen Powell, Colin R. Tosh,
and Jim Hardie 309
vii
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November 2, 2005 13:47 Annual Reviews AR263-FM
viii CONTENTS
BIZARRE INTERACTIONS AND ENDGAMES:ENTOMOPATHOGENIC
FUNGI AND THEIR ARTHROPOD HOSTS, H.E. Roy,
D.C. Steinkraus, J. Eilenberg, A.E. Hajek, and J.K. Pell 331
CURRENT TRENDS IN QUARANTINE ENTOMOLOGY, Peter A. Follett
and Lisa G. Neven 359
THE ECOLOGICAL SIGNIFICANCE OF TALLGRASS PRAIRIE
ARTHROPODS, Matt R. Whiles and Ralph E. Charlton 387
MATING SYSTEMS OF BLOOD-FEEDING FLIES, Boaz Yuval 413
CANNIBALISM,FOOD LIMITATION,INTRASPECIFIC COMPETITION, AND
THE
REGULATION OF SPIDER POPULATIONS, David H. Wise 441
BIOGEOGRAPHIC AREAS AND TRANSITION ZONES OF LATIN AMERICA
AND THE
CARIBBEAN ISLANDS BASED ON PANBIOGEOGRAPHIC AND
CLADISTIC ANALYSES OF THE ENTOMOFAUNA, Juan J. Morrone 467
DEVELOPMENTS IN AQUATIC INSECT BIOMONITORING:A
C
OMPARATIVE ANALYSIS OF RECENT APPROACHES, N
´
uria Bonada,
Narc
´
ıs Prat, Vincent H. Resh, and Bernhard Statzner 495
TACHINIDAE:EVOLUTION,BEHAVIOR, AND ECOLOGY,
John O. Stireman, III, James E. O’Hara, and D. Monty Wood 525
TICK PHEROMONES AND THEIR USE IN TICK CONTROL,
Daniel E. Sonenshine 557
CONFLICT RESOLUTION IN INSECT SOCIETIES, Francis L.W. Ratnieks,
Kevin R. Foster, and Tom Wenseleers 581
ASSESSING RISKS OF RELEASING EXOTIC BIOLOGICAL CONTROL
AGENTS OF ARTHROPOD PESTS, J.C. van Lenteren, J. Bale, F. Bigler,
H.M.T. Hokkanen, and A.J.M. Loomans 609
DEFECATION BEHAVIOR AND ECOLOGY OF INSECTS, Martha R. Weiss 635
PLANT-MEDIATED INTERACTIONS BETWEEN PATHOGENIC
MICROORGANISMS AND HERBIVOROUS ARTHROPODS,
Michael J. Stout, Jennifer S. Thaler, and Bart P.H.J. Thomma 663
INDEXES
Subject Index 691
Cumulative Index of Contributing Authors, Volumes 42–51 717
Cumulative Index of Chapter Titles, Volumes 42–51 722
ERRATA
An online log of corrections to Annual Review of Entomology
chapters may be found at http://ento.annualreviews.org/errata.shtml
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