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um"-screened (Venture Textiles, MA, USA) cages, two plants per cage, and aphids were .... Bird cherry-oat aphid (Rhopalosiphum padi. (L.)), like soybean aphid, ...

Amer J of Potato Res (2005) 82:197-201


Soybean Aphid, Aphis glycines Matsumura, a N e w Vector of P o t a t o Virus Y in P o t a t o J e f f r e y A. Davis*, E d w a r d B. R a d c l i f f e , a n d D a v i d W. R a g s d a l e Department of Entomology, University of Minnesota, 219 Hodson Hail, 1980 Folwell Ave., St. Paul, MN 55108, USA *Corresponding author: Tel: (612) 624-2751; Fax: (612) 625-5299; Email: [email protected]

ABSTRACT S o y b e a n aphid (Aphis glycines Matsumura),


Since its discovery in the North Central region of the

e x o t i c s p e c i e s first d i s c o v e r e d in t h e N o r t h Central

United States in 2000, soybean aphid (Aphis glycines Mat-

region o f t h e U n i t e d S t a t e s in 2000, is a c o m p e t e n t vec-

sumura) has spread to 21 states (Venette and Ragsdale 2004).

tor o f s e v e r a l Potyviridae. S o y b e a n aphid has high

This aphid can directly damage soybean (Glycine m a x L.), cans-

f e c u n d i t y and p r o d u c e s alatae ( w i n g e d m o r p h s ) readily,

ing early leaf senescence and reducing pod set, seed quality, and

characteristics typical o f p r o f i c i e n t virus vectors. W h e n

yield (Xibei et al. 1994; Wang et al. 1996, 1998; Wu et al. 1999).

s o y b e a n aphids w e r e e x p o s e d t o Potato virus Y (PVY)-

In addition to direct feeding damage to soybean, soybean

i n f e c t e d p o t a t o p l a n t s and t h e n clip-caged o n h e a l t h y

aphid transmits several plant viruses including Alfalfa mosaic

p o t a t o p l a n t s in groups o f five or as single aphids, PVY

.virus (AMV), Cucumber mosaic virus (CMV), Peanut mottle

t r a n s m i s s i o n ranged f r o m 14% to 75% across all experi-

virus (PMV), Soybean mosaic virus (SMV), Tobacco ringspot

m e n t s . PVY°, PVYN, and PVYNTNstrains w e r e t r a n s m i t t e d

v i r u s (TRSV), and Tobacco vein-banding mosaic virus (TBMV) (Fang et al. 1985; Alleman et al. 2002; Clark and Perry

by s o y b e a n aphid.

2002; Wang and Ghabrial 2002). Soybean aphid is a proficient


vector of nonpersistent viruses in part because of its high fecundity, short generation time (McCornack et al. 2004), and

E1 ~Lfido de la s o y a (Aphid glycines Matsumura),

propensity to form alatae (winged morphs) (Voegtlin and

e s p e c i e e x 6 t i c a que f u e r a d e s c u b i e r t a e n la regi6n nor-

Onstad 2003). Soybean aphid is congeneric with two known

central de los E s t a d o s U n i d o s e n el afio 2000 es un vec-

Potato virus Y (PVY) vectors: buckthorn aphid (Aphis nas-

tor de varios Potyviridae. E1 ~fido de la s o y a t i e n e una

turtii Kaltenbach) and cotton aphid (Aphis gossypii Glover).

alta f e c u n d i d a d y produce r ~ p i d a m e n t e f o r m a s aladas,

Aphis glycines and A. gossypii have been reported to produce

caracterlstica tipica de los v e c t o r e s de virus. C u a n d o los

hybrids which, while viable, have reduced fecundity (Zhang

~fidos de la s o y a se p u s i e r o n e n c o n t a c t o con el virus Y

and Zhong 1982). For these reasons, we hypothesized that soy-

(PVY) e n plantas de papa i n f e c t a d a s y l u e g o se inser-

bean aphid could be a vector of PVY.

taron en p l a n t a s sanas en grupos de cinco o c o m o ~fidos

PVY exists as several strains that have been placed into

solitarios, la trasmisi(in de PVY fue de 14% a 75% en

groups based on their symptomology in potato (Solanum

t o d o s los e x p e r i m e n t o s . Las v a r i a n t e s PVY °, PVYN y

tuberosum L.) and tobacco (Nicotiana tabaccum L.) (de Bokx

PVYNTNf u e r o n t r a s m i t i d a s por el ~fido de la soya.

and Huttinga 1981; Kerlan et al. 1999). The common strain, PVY°, produces mosaic and leaf drop in potato and tobacco. A strain designated as tobacco veinal necrotic strain, PVYN, produces mottling and necrosis in potato (Chachulska et al. 1997; Kerlan et al. 1999) and severe necrosis in tobacco (de Bokx

Accepted for publication 12 October 2004. ADDITIONAL KEY WORDS: Solanum tuberosum, virus transmission efficiency

and Huttinga 1981). In potato, PVYN tends to cause a milder mosaic than does PVY° and in some cultivars is essentially asymptomatic (de Bokx and Huttinga 1981). A variant of PVYN



can produce tuber necrosis in potato and has been designated as PVYNTN.This variant causes typical mosaic symptoms on

Vol. 82

A p h i d Colonies Aphid colonies maintained in the laboratory were used in

potato leaves, sunken necrotic rings on tubers, and leaf necrosis

all transmission experiments. The soybean aphid colony was

in tobacco (Le Romancer et al. 1994). Tubers may be infected

founded from aphids collected from soybean at UMore Park in

with PVYNv~ but not show symptoms due to cultivar differ-

2001 and reared on soybean (cv M96-133151) in an environmen-

ences or lack of permissive environmental conditions. In addi-

tal growth chamber held at 25 ± 2 C, 75 ± 3% RH, and a pho-

tion, there are specific strains detected serologically as PVY°

toperiod of 16:8 (L:D). Colonies of green peach aphid and potato

that cause necrosis in tobacco (McDonald and Singh 1996;

aphid were founded from aphids collected from potato at

Chrzanowska 2001). These strains have been designated PVYN:°

UMore Park in 1996 and 2002, respectively, and reared on virus-

and are recombinants between PVY° and PVYN(Nie and Singh

free potato (various cultivars have been used) in a greenhouse

2002, 2003; Singh et al. 2003).

held at 20 ± 2 C, 50 ± 5% RH and a photoperiod of 16:8 (L:D). The

Preliminary experiments using a mass inoculation proce-

corn leaf aphid (Rhopalosiphum maidis (Fitch)) colony was

dure similar to the arena tests described by Irwin and Ruesink

founded from aphids collected from wheat (Triticum aestivum

(1986) suggested that soybean aphid can acquire and transmit

L.) at the St. Paul campus of the University of Minnesota in 2003

PVY (Davis et al. 2004). Objectives of this study were (i) to

and reared on barley (Hordeum vuLgare L.) in a greenhouse

confirm that soybean aphid can transmit PVY from potato to

held at 20 ± 2 C, 50 ± 5% RH and a photoperiod of 16:8 (L:D).

potato and (ii) to measure transmission efficiency.

Virus D e t e c t i o n


Virus detection was performed by double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) using

Virus S t r a i n s a n d M a i n t e n a n c e

polyclonal and monoclonal kits according to the manufac-

The PVY inoculum source used in these experiments orig-

turer's protocols (Agdia, Elkhart, IN, USA). Absorbance was

inated from PVY-infected tubers (cvs Red La Soda and Chief-

measured at 405 nm with a BioRad 450 Plate Reader (Her-

tain) harvested at the University of Minnesota Outreach,

cules, CA, USA). Plants were considered PVY positive if the

Research and Education Park (UMore Park), Rosemount, MN,

OD405 reading was three times negative controls (noninfected

from field plots used to screen potato breeding lines for PVY

plants). Viral RNA was extracted using a Qiagen (Valencia, CA,

resistance. In the field, this PVY source is maintained by annual

USA) RNeasy Plant Mini Kit. RT-PCR was performed with a

harvesting of tubers from the "infector rows," which are

Qiagen OneStep RT-PCR Kit using a competitive multiplex

blended with certified seed and planted as inoculum the next

approach with five primers based on nucleotide differences in

year. Thus, this source is representative of aphid-transmitted

the P1 gene of PVY to discriminate among strains (Nie and

PVY strains found in Minnesota, a characteristic considered

Singh 2002) and a six primer competitive multiplex to discrim-

desirable in transmission efficiency trials (Irwin and Ruesink

inate recombinant PVYN:° (Nie and Singh 2003). Primers spe-

1986; Power and Gray 1995; Gray et al. 1998; Lucio-Zavaleta et

cific to the coat protein and nuclear inclusion protein b region

al. 2001). All three PVY strains and recombinant PVYN:° were

created by Moravec et al. (2003) were also used to confirm

shown by reverse transcriptase polymerase chain reaction

strain type. This allowed simultaneous identification of all PVY

(RT-PCR) to be present in the inoculum source, but titer levels

strains present in plants having multiple strain infections.

for each strain were not determined. In the greenhouse, trans-

Bioassays to confirm PVYN detection involved rubbing leaves

missions to maintain the PVY source were by green peach

of tobacco, cv Samsun NN, with carborundum (silicon car-

aphid (Myz~v persicae (Sulzer)), and potato aphid (Macrosi-

bide, 600 grit) and plant sap or with water (control).

phum euphorbiaz (Thomas)). Aphids were allowed to move freely from infected to healthy potatoes, transmitting PVY. This ensured that freshly infected plants were available to

P o t a t o Test P l a n t s Potato plants were grown from minitubers, cv Katadhin

serve as virus sources for all experiments and that all PVY

(provided courtesy of J. P. Helgeson, Univ. Wisconsin, Madi-

strains maintained were aphid transmitted.

son), or true potato seed, cv GS-201 (from National Research Support Project-6, United States Potato Genebank, Sturgeon




Bay, WI, USA), planted in 10-cm-diameter plastic pots contain-

ciency, single aphid experiments included three k n o w n PVY

ing sterile potting mix (Sun Gro Horticulture, Elma, Manitoba,

vectors, green p e a c h aphid, potato aphid, and corn leaf aphid.

Canada) and 5 g O s m o c o t e (14-14-14), a slow-release fertilizer

Transmission efficiency was estimated as n u m b e r of

(The Scotts Company, Marysville, OH, USA). Plants were held

infected test plants divided by total n u m b e r of test plants,

in a greenhouse at 20 _+ 2 C, 50 + 5% RH and a photoperiod of

expressed as a percentage. For groups of five aphids, the max-

16:8 (L:D). Prior to use in transmission experiments, test

i m u m likelihood estimator (MLE) was also used (Gibbs and

plants were serologically tested by DAS-ELISA to confirm that

G o w e r 1960; Venette et al. 2002). MLE was calculated as 1-(1-

they w e r e PVY-free.

x/m) ~/k,where x was the n u m b e r of test plants positive for PVY, m was the total n u m b e r of test plants, and k was the n u m b e r

Transmission Efficiency Tests

of aphids used per test plant. Differences in infection rates b e t w e e n test plants and

Adult apterae (wingless aphids) w e r e used in all transmission tests. Transmission efficiencies w e r e measured using

controls w e r e calculated by PROC NPARIWAY using the

aphids in groups of five or individually and virus-free potato

Wilcoxon score (SAS Institute, Cary, NC, USA). Wilcoxon

test plants grown from either minitubers (greenhouse-grown

score is a signed rank test, substituting for the paired t-test, in

prenuclear seed potatoes) or true potato seed. Soybean aphids

which treatments are ranked (positive or negative in this case)

were given a 4-h pre-acquisition fast after which they were

and c o m p a r e d (Snedecor and Cochran 1989). Tiffs test is used

placed on detached PVY-infected potato leaves in closed petri

w h e n assumptions for normality are not met, i.e., variance is

dishes and allowed an acquisition access period of 10 min. All

not constant (Snedecor and Cochran 1989).

excised leaves used as inoculum sources w e r e later tested by RT-PCR to identify PVY strains present. Aphids w e r e then


placed into 1.2-mm-diameter circular clip cages on PVY-free test plants. Test plants and aphids w e r e held in 0.2 m 3 "no-see-

In four experiments w h e r e test plants w e r e exposed to

um"-screened (Venture Textiles, MA, USA) cages, two plants

groups of five aphids, PVY was detected in 50% of the test plants

per cage, and aphids w e r e given an tmlimited inoculation

(range 37.5% to 75%) (Table 1). After exposure to a single aphid

access period. Surviving aphids were r e m o v e d manually after

in five experiments, PVY was detected in 33.3% of test plants

5 days. Plants w e r e retested for PVY by RT-PCR 2 w k after

(range 14.3°/5 to 50%) (Table 1). PVY infection was detected in

aphids w e r e removed. To provide comparisons of vector effi-

one of the control plants (1/16) grown from cv Katahdin mini-

TABLE 1--Soybean aphid transmission of PVY : ...


:" r--

Test cultivax~


PVY strains in inoculum



PVY transmission to test plants Control Source (not PVY(PVY inoculated) inoculated)

Strain frequency in test plants where transmission occurred ~ PVY° PVYN P ~ PVYN:°

Five aphid experiments 1 2 3 4

Katahdin Katahdin Katahdin Katahdin

O, N, NTN, N:O O, N, NTN, N:O O, N, NTN, N:O O, N, NTN, N:O

0/4 0/4 0/4 1/4 1/16(

6/8 4/8 3/8 3/8 16/32¢

6 4 2 2 14

6 4 1 2 13

0 4 1 2 7

0 0 0 0 0

O, N, NTN, N:O O O O O, N, NTN, N:O

0/8 0/3 0/8 0/7 0/5 0/31~

3/8 1/7 1/4 2/4 5/13 12/36¢

3 1 1 2 4 11




0 l

1 1

0 0

Single aphid exper~ments 1 2 3 4 5

GS 201 GS 201 GS 201 GS 201 GS 201

~Multiple PVY strains were often detected in infected plants so cumulative strain numbers can exceed total infected plants. bGrown from minitubers and true potato seed. cPVY transmission between control and inoculum sources in five aphid experiments and in single aphid experiments differed significantly, Wilcoxon Signed Rank Test, P = 0.03, and P = 0.013, respectively.



Vol. 82

tubers, but in none of the plants (0/31) grown from cv GS201

the PVY° and PVYTM strains in this study were similar to that

true seed. Differences in infection incidence between test

reported by other authors (Katis and Gibson 1985; Harrington et

plants and controls were significantly different in both the five

al. 1986; Fereres et al. 1993), all of whom found that green peach

aphid and single aphid experiments; P -- 0.03, and P = 0.013,

aphid transmitted PVY° more efficiently than PVYN. If PVYN were to become abundant in the North Central

respectively. Efficiency of PVY transmission by soybean aphid ranged

region, this could force potato seed certification programs to rely

from 14% to 75% across all experiments. Calculated MLE for

to a much greater extent on serological testing because PVYN

groups of five aphids was 13.8%. In single aphid experiments,

infections tend to be more difficult to recognize visually. Soybean

PVY transmission by green peach aphid was 100°/0(8/8) and by

aphid appeared to transmit PVYN:°in preliminarymass inoculation

potato aphid 87.5% (7/8). There was no transmission of PVY by

experiments (Davis et al. 2004), but this recombinant was not

corn leaf aphid (0/8). The results for vectors other than A.

transmitted in experiments with groups of five or single aphids.

glycines were similar to efficiencies reported for these species in the literature (Ragsdale et al. 2001).

Soybean is not a host of PVY and even when soybean aphid had access to PVY inoculmu, its efficiency of transmis-

Soybean aphid transmitted strains PVY°, PVYN, and

sion was less than that of green peach aphid and potato aphid.

PVYNTNto potato (Table 1). Among the test plants positive for

However, potatoes are frequently rotated with soybean in the

PVY in the groups of five aphids and single aphid experiments,

North Central region, so this crop is often grown in close prox-

89°/0 (25/28) test plants were positive for PVY°, 58% (14/24)

imity to potatoes. Bird cherry-oat aphid (Rhopalosiphum padi

were positive for PVYN, and 33% (8/24) were positive for PVYm~.

(L.)), like soybean aphid, is an inefficient PVY vector (11.5%)

This indicates that soybean aphid can transmit either single or

compared to M. persicae, but has been implicated as a key vec-

multiple strains of PVY. There was no detectable transmission

tor of that virus in our region (DiFonzo et al. 1997). What soy-

of p\~N:~) in any experiment.

bean aphid lacks in transmission efficiency, it makes up in

Bioassays indicated that PVY~ was present in the inoculum.

sheer numbers. In 2003, 2.8 million ha of soybeans in Minnesota

Typical tuber symptoms of PVYm~, raised rings or arches that

were hffested with soybean aphid, with nearly 1.4 million ha

become cracks or sunken pits, were observed in the inoculum

treated to prevent yield losses. Voegtlin and Onstad (2003) esti-

tubers, but in the transmission experiments, test plants were

mated that -400 million soybean aphid alatae emigrated from

not grown to tuber bulking.

one 32-ha Illinois soybean field in a single day. Given this aphid's propensity to form alatae, its high fecundity, and rela-


tive transmission efficiency, soybean aphid appears to have the potential to be an important vector of PVY. This is the first

The role soybean aphid may play in PVY epidemiology in

confirmation of soybean aphid transmitting PVY.

the North Central region is uncertain, but there is cause for concern. In this study, soybean aphid had PVY-transmission


efficiencies similar to other Aphis spp. considered important vectors of PVY. For example, Aphis nasturtii transmits PVY at

The authors acknowledge Dr. Roger Moon for his statistical

19°/0 to 50% and A. gossypii at 12% to 31% (Ragsdale et al.

advice. We also thank Dr. Philip Berger, USDA-APHIS-PPQ-

2001). Green peach aphid is considered to be the most efficient

CPHST, Raleigh, NC, Dr. Jeffrey Wyman, University of Wiscon-

PVY vector, whereas potato aphid is intermediate (Harrington

sin, Madison, WI, and anonymous peer reviewers for their

et al. 1986; Piton 1986; Harrington and Gibson 1989) and corn

constructive comments on a previous draft of this manuscript.

leaf aphid is inefficient (Halbert et al. 2003). Placed on this continuum, soybean aphid would fall between potato aphid


and corn leaf aphid in PVY vector efficiency. Relative titer levels of PVY strains in the inoculum source used in this study were not measured, so it is not possible to draw conclusions as to relative efficiency of transmission of various strains. However, comparative transmission efficiencies for

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