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3 Plant Viruses Transmitted by Mealybugs

3 Plant Viruses Transmitted by Mealybugs

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10



a



Mealybugs as Vectors



125



b



c



d



e



f



g



h



i



j



Fig. 10.1 (a) Electron micrograph of BSV; (b) Ferrisia

virgata feeding on banana; (c) Pink pineapple mealybug,

Dysmicoccus brevipes; (d) Gray pineapple mealybug, D.

neobrevipes; (e) Electron micrograph of GLRaV; (f)



Electron micrograph of GVB; (g) Vine mealybug; (h)

Symptoms of BSV in banana; (i) GLRaV infected grapevine; (j) Symptoms of mealybug wilt of pineapple



the low numbers survived the inoculation access

period; the virus was transmitted from the TC-5

to the William banana. However, no episomal

BSGFV could be transmitted by D. brevipes from

the FH-4 donor to the recipient plants (Meyer



et al. 2008). The fact that none of the mealybug

species were able to transmit integrated BSOLV

from the FHIA-4 to Williams proves that the integrated form of BSV is not likely to be transmitted

by mealybugs; even highly efficient mealybugs



R. Selvarajan et al.



126



such as P. citri were unable to transfer any integrated viral sequences to the receptor plants.

Episomal BSV in tissue culture-derived tetraploids is highly transmissible by efficient mealybug vectors to Cavendish varieties.

Cocoa swollen shoot virus (CSSV), a badnavirus, is transmitted by at least 14 species of

mealybugs of the family Pseudococcidae within

the Coccoidae (Roivainen 1976), but

Planococcoides njalensis and Planococcus citri

are the most important vectors (Dongo and

Orisajo 2007). Piper Yellow Mottle Virus

(PYMV) is transmitted by the citrus mealybug,

Planococcus citri (Lockhart et al. 1997). Bhat

et al. (2003) reported that PYMV could easily be

transmitted by the mealybugs (Ferrisia virgata)

from naturally diseased black pepper to healthy

seedlings of black pepper. The initial symptoms

of the disease, like vein clearing and chlorotic

mottle, could be seen in 14 of the 20 test plants in

5 weeks after inoculation. Macanawai et al.

(2005) reported that the Taro bacilliform virus

(TaBV) is transmitted by Pseudococcus

solomonensis.



10.4



Viruses Belonging

to Closteroviridae



Mealybug-vectored viruses often exist as a complex of viruses, such as the mealybug wilt of

pineapple complex, which is made up of three

pineapple mealybug wilt-associated viruses

(PMWaV) (Sether et al. 1998, 2005; Sether and

Hu 2002a, b) and Grapevine leafroll-associated

viruses. Mealybug wilt of pineapple is a major

constraint in the global production of pineapple

(Carter 1934, 1942; Rohrbach et al. 1988;

Wakman et al. 1995). Carter (1934, 1942, 1949,

1962) found an association between mealybugs,

particularly the pink pineapple mealybug,

Dysmicoccus brevipes (Cockerell), (Fig. 10.1c)

and the gray pineapple mealybug, D. neobrevipes

(Beardsley) (Fig. 10.1d), and wilt throughout the

pineapple-growing regions of the world.

PMWaV-1 infections are correlated with growth

reductions of the plant crop (Sether and Hu

1998), and yield reductions in the ratoon crop.



PMWaV-2 infection and mealybug feeding are

necessary for the development of mealybug wilt

disease (Hu and Sether 1999a, b; Sether and Hu

2002a, b). All pineapple plants with wilt disease

have PMWaV-2 infections, but not necessarily

PMWaV-1 infections (Hu et al. 1997; Sether and

Hu 2002a). Several species of ants are associated

with mealybugs (Beardsley et al. 1982; Carter

1963). These ants assist in the establishment of

mealybug colonies, consuming the honeydew

produced by the mealybugs (Petty and Tustin

1993), and can have a suppressive effect on the

natural enemies of mealybugs (Jahn 1992).

Sether et al. (1998) reported that presence of ants

was correlated with an increased rate of virus

spread when caged with D. brevipes. All stages

of D. neobrevipes acquire PMWaV, although

vector efficiency decreased significantly in older

adult females; the probability of a single thirdinstar immature transmitting the virus was 0.04.

Both the species of the mealybugs acquired and

transmitted the PMWaV from infected pineapple

material.

The Grapevine leafroll disease is caused by

grapevine leafroll-associated viruses (GLRaVs)

(Fig. 10.1e). These viruses are common in vineyards worldwide, and are often associated with

vitiviruses that are involved in the rugose wood

complex of grapevines. Ten mealybug species are

known as vectors of one or several of these grapevine viruses, including the apple mealybug

Phenacoccus aceris, which is widespread, and is

able to transmit the Grapevine leafroll-associated

virus-1 and -3 (GLRaV-1 and -3). Vitiviruses,

namely Grapevine virus A (GVA), Grapevine

virus B (GVB) (Fig. 10.1f), Grapevine virus D

(GVD) and Grapevine virus E (GVD), infect

grape vines, and these are transmitted by the

members of several insect genera (Pseudococcus,

Planococcus,

Phenacoccus,

Heliococcus,

Neopulvinaria, Parthenolecanium, Cavariella

and Ovatus) in a semi-persistent manner (La

Notte et al. 1997; Rosciglione et al. 1983; Garau

et al. 1995). Tsai et al. (2010; Le Maguet et al.

2012) studied the virus–vector specificity analysis for mealybug transmission of GLRaVs. Plants

infected with several GLRaVs virus species were

screened for vector transmission by the mealybug



10



127



Mealybugs as Vectors



Table 10.1 Mealybug transmitted plant viruses

Virus, genus and family

Banana streak virus sps,

Badnavirus, Caulimoviridae



Sugarcane bacilliform virus

sp. Badnavirus,

Caulimoviridae

Piper yellow mottle virus;

Badnavirus, Caulimoviridae

Taro bacilliform Badnavirus,

Caulimoviridae

Schefflera ringspot virus

(SRV)

Cacoa swollen shoot virus,

Badnavirus, Caulimoviridae

Pineapple mealybug wilt

associated virus-1–3;

Closterovirus; Closteroviridae

GLRaV-1, 3–9; Ampelovirus,

Closteroviridae



Grapevine virus A, B, D and

E, Vitivirus, Betaflexiviridae,

Little Cherry Virus 2

Closterovirus, Closteroviridae



Vector species

Dysmicoccus brevipes,

Planococcus citri, Pl. ficus,

Pseudococcus longispinus,

Ferrisia virgata

Saccharicoccus sacchari



Mode of transmission

Semi-persistent



Reference

Meyer et al. (2008),

Kubiriba et al. (2001),

Selvarajan et al. (2006)



Semi-persistent



Lockhart et al. (1997)



Planococcus citri

Pseudococcus elisae

F. virgata

Pseudococcus solomonensis



Semi-persistent



Lockhart et al. (1997),

Bhat et al. (2003)



Semi-persistent



Planococcus citri



Semi-persistent



Planococcoides njalensis, Pl.

citri, F. virgata

Dysmicoccus brevipes

(Cockerell)

D. neobrevipes

Heliococcus bohemicus,

Phenacoccus aceris Signoret,

Planococcus ficus

Pseudococcus longispinus,

Pseudococcus viburni,

Pseudococcus calceolariae,

Pseudococcus maritimus, Pl.

citri

Pseudococcus, Planococcus,

Phenacoccus, Heliococcus

Phenacoccus aceris



Semi persistent



Macanawai et al.

(2005)

Lockhart and

Olszewski (1996)

Roivainen (1976)



Semi-persistent



Sether et al. (1998)



Semi-persistent



Tsai et al. (2012)



Semi-persistent



Garau et al. (1995), Le

Maguet et al. (2012)

Raine et al. (1986)



species Planococcus ficus and Pseudococoucus

longispinus. The results revealed that P. longispinus had transmitted the GLRaV-9 to the inoculated plants, and showed that 18 % of the

inoculated plats were positive for GLRaV-9, but

none of the inoculated plants were found positive

for GLRaV-5, tested 9 months after the inoculation. Planococcus ficus transmitted the GLRaV1,3,4,5,9 and GVA. This study showed that there

was no evidence of mealybug–GLRaV specificity. Tsai et al. (2008) reported that the vine

mealybug (Planococcus ficus) (Fig. 10.1g) transmits GLRaV- 3 in a semi-persistent manner. First

instars were more efficient vectors than adult

mealybugs, but the GLRaV-3 transmission lacked

a latent period in the vector. Virus transmission

occurred with a 1-h acquisition access period



Semi-persistent



(AAP) and peaked with a 24-h AAP, after which

the transmission rate remained constant. In addition, the GLRaV-3 was found not to have been

transovarially transmitted from infected females

to their progeny (Table 10.1).

Mealybugs are less mobile on the plant compared with groups of vectors such as aphids and

leaf hoppers, a feature that makes them relatively

inefficient as virus vectors. Mostly, the mealybugtransmitted viruses appear to have a semipersistent mode of transmission based on

retention times. Mealybug-transmitted viruses

appear to have a high rate of acquisition and low

rate of inoculation. Mealybug-vectored viruses

often exist as a complex of viruses, such as the

mealybug-associated viruses. Badnaviruses such

as PYMV, BSV’s TaBV and CSSV have been



R. Selvarajan et al.



128



shown to transmit by different mealybug species.

In all of these studies, the interaction of the

mealybug vector with the virus and the host is

lacking; hence it is necessary to generate fundamental knowledge about the interaction of the

vector, the host and the virus system to develop

effective disease management strategies for viral

diseases. Epidemiological studies are also

required to predict the spread of the plant viruses

through mealybugs, and the changing climatic

conditions need to be considered while developing forecasting models of disease spread.



3–4 years (Fig. 10.1j) (Crowdy and Posnette

1947). The impact of mealybug feeding and

Pineapple mealybug wilt associated virus-1

(PMWaV-1), PMWaV-2 infection on pineapple

yield and the spread of PMWaV-1 and mealybug

wilt of pineapple (MWP) were evaluated under

field conditions; the results showed a 35 % reduction in yield when compared with PMWaV-free

plants (Sether and Hu 2002b). If MWP develops

during the first 3 months of the plant crop, it can

lead to a 55 % reduction in average fruit weight,

compared with fruits from PMWaV-free plants.



10.5



10.6



Loss Due to MealybugTransmitted Virus Diseases



Comprehensive analysis of yield loss due to

mealybug infection has not been carried out in

many of the crops, however, the infection of

mealybug-transmitted viruses leads to drastic

yield losses have been reported. Estimated yield

losses of between 7 % and 90 % have been attributed to the banana streak disease in different

parts of the world (Harper et al. 2004; Lockhart

et al. 1998; Davis et al. 2000; Daniells et al.

2001). In India, a yield loss of 49.48 % has been

recorded in cv. Poovan (Mysore, AAB) due to

BSV (Fig. 10.1h) (Thangavelu et al. 2000). In

banana, the yield loss due to BSV is influenced

by the cultivar, the virus species infecting, and

environmental conditions. Grapevine leafroll disease occurs in all the major grape-growing

regions of the world, causing reductions in productivity and quality of both wine and table

grapes.

Infected grapevines (Fig. 10.1i) result in

reduced berry yields, delayed maturity and poor

pigmentation. Estimated yield losses of as much

as 30–40 % due to Grapevine leafroll disease has

been recorded (Maree et al. 2013). In addition,

the disease agent has been implicated in certain

types of graft incompatibility and young vine

failure. Cacao swollen-shoot virus (CSSV)

infects cacao trees and has a major effect on crop

yields. Within 1 year of infection by CSSV, the

yield decreases by 25 % and by 50 % within 2

years. The infected trees are usually killed within



Management



The best way to manage the virus diseases transmitted by mealybugs is to ensure that purchase of

planting material is from virus-tested and virusfree mother plants, and the control of

vectors – mealybugs.



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