LETTERS
Toxin delivery by the coat protein of an aphid-vectored
plant virus provides plant resistance to aphids
Bryony C Bonning1, Narinder Pal1, Sijun Liu1, Zhaohui Wang2, S Sivakumar1, Philip M Dixon3, Glenn F King4 &
W Allen Miller2
The sap-sucking insects (order Hemiptera), including
aphids, planthoppers, whiteflies and stink bugs, present one
of the greatest challenges for pest management in global
agriculture. Insect neurotoxins offer an alternative to chemical
© 2014 Nature America, Inc. All rights reserved.
insecticides for controlling these pests, but require delivery
into the insect hemocoel. Here we use the coat protein of a
luteovirus, an aphid-vectored plant virus, to deliver a spider-
derived, insect-specific toxin that acts within the hemocoel.
The luteovirid coat protein is sufficient for delivery of fused
proteins into the hemocoel of pea aphids, Acyrthosiphon
pisum, without virion assembly. We show that when four
aphid pest species—A. pisum, Rhopalosiphum padi,
Aphis glycines and Myzus persicae—feed on a recombinant coat
protein–toxin fusion, either in an experimental membrane sachet
or in transgenic Arabidopsis plants, they experience significant
mortality. Aphids fed on these fusion proteins showed signs of
neurotoxin-induced paralysis. Luteovirid coat protein–insect
neurotoxin fusions represent a promising strategy for transgenic
control of aphids and potentially other hemipteran pests.
Arthropod pests pose a constant threat to agricultural yields both
npg
in the field and after harvest. The use of transgenic crops expressing
insecticidal proteins from Bacillus thuringiensis (Bt) has become the
primary approach for management of some pests1, which has ben-
efited both growers through crop protection and the environment
through a reduction in the use of chemical insecticides2. However, Bt
toxins are not typically effective against hemipteran pests with pierc-
ing and sucking mouthparts3,4, and populations of some species have
dramatically increased concurrent with the decrease in insecticide
use5,6. In addition to gut-active toxins, such as those derived from Bt,
many other insect-specific toxins act within the insect hemocoel (body
cavity). In contrast to Bt toxins, these toxins are not insecticidal when
acquired by feeding7,8, and thus far have not been exploited for insect
pest management because of the lack of an appropriate delivery sys-
tem. Here we demonstrate the use of a coat protein from a luteovirid
(a virus in the family Luteoviridae) for delivery of an intrahemocoelic,
insect-specific toxin, thereby creating an effective oral toxin.
Upon aphid feeding on a luteovirid-infected plant, virus particles
cross from the gut lumen into the hemocoel of their aphid vectors by
1Department of Entomology, Iowa State University, Ames, Iowa, USA. 2Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, USA.
3Department of Statistics, Iowa State University, Ames, Iowa, USA. 4Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Queensland,
Australia. *Correspondence should be addressed to B.C.B. (bbonning@iastate.edu) or W.A.M. (wamiller@iastate.edu).
Received 24 May; accepted 30 October; published online 8 December 2013; doi:10.1038/nbt.2753
102
means of receptor-mediated transcytosis (vesicular transport across a
cell)9,10. Some virions subsequently enter the accessory salivary gland,
from which they are released into a plant, completing the transmission
cycle. The luteovirid virion comprises two forms of structural protein,
the 22-kDa major coat protein and a C-terminally extended version
containing a read-through domain (RTD) that is added by translation
through the leaky coat protein open reading frame stop codon. Both
forms are necessary for aphid transmission but the RTD is unneces-
sary for uptake of the virion into the hemolymph11.
We sought to fuse the coat protein and a small portion of the RTD
of Pea enation mosaic virus (PEMV) to the highly insect-specific,
spider-derived, peptide -hexatoxin-Hv1a (Hv1a)12. Hv1a is aphi-
cidal when injected into the aphid hemocoel but not when adminis-
tered orally13. In contrast, we show that the PEMV coat protein–Hv1a
fusion is toxic upon feeding and thus has potential to confer trans-
genic aphid resistance to plants.
First, to determine whether PEMV coat protein fusions would enter
the hemocoel, we fused PEMV coat protein to green fluorescent pro-
tein (GFP) by replacing the coat protein stop codon with a sense
codon and by replacing all or most of the RTD sequence with the GFP
sequence (CP-GFP or CP-P-GFP, respectively; Fig. 1a). Only fusions
with the proline-rich (P) motif derived from the N-terminal portion
of the RTD retained solubility (Supplementary Fig. 1). The P motif is
thought to serve as a spacer between the coat protein and RTD, allow-
ing each to fold properly. In contrast to expression of coat protein
alone, which formed virus-like particles14, and similar to previous
work15, no virus-like particles accumulated in cells expressing coat
protein fusion proteins without the coat protein stop codon.
To determine the fate of recombinant GFP and CP-P-GFP in
the aphid, we injected purified, baculovirus-expressed proteins
(Supplementary Fig. 2) into pea aphids. Injected CP-P-GFP was
concentrated in the pericardial cells along the dorsal aorta (Fig. 1b).
This localization was confirmed by injection of trypan blue, which
is removed from the hemolymph by the pericardial cells in which
the dye accumulates16,17 (Fig. 1b). Fluorescence following injec-
tion of GFP alone was diffuse with some concentration in the dorsal
aorta and pericardial cell region (Fig. 1b). We then tested whether
GFP or CP-P-GFP would move into the aphid hemocoel after feed-
ing. Aphids fed GFP alone showed only background fluorescence.
VOLUME 32 NUMBER 1 JANUARY 2014 NATURE BIOTECHNOLOGY
 LETTERS

Figure 1 Constructs used to test for PEMV

CP-P–mediated delivery of GFP and Hv1a to
a Injection Feeding b
Trypan blue PBS
aphids. (a) Fusion protein constructs. Colored
boxes indicate functional domains: H, 6xHis tag H GFP
KHisGFP
(18 nt); K, optimal Kozak sequence flanking
CP-GFP CP GFP
the start codon (21 nt); CP, coat protein;
HisCP-GFP H CP GFP
GFP, green fluorescent protein; P, proline-rich
domain, the amino acid sequence of which KHisGFP KHisGFP
is shown, followed by the linker GAAG; KHisCP-P-GFP H CP P GFP

TGA TGG, mutation to remove stop codon; TGA TGG

gss, GNA secretory signal (23 amino acids)

gssHv1a gss Hv1a
sequence to enhance localization in phloem
sap; GST, glutathione S-transferase; N27A and CP-P-Hv1a GST CP P Hv1a
KHisCP-P-GFP KHisCP-P-GFP
R35A, mutations that inactivate Hv1a in CP-P-
Hv1am. (b) Uptake of KHisCP-P-GFP from the CP-P-Hv1am: N27A R35A

pea aphid gut, into the hemocoel. Images show

fluorescence of aphids following injection (left)
or feeding (right) on the indicated treatments.
Shown are dissected pea aphid with pericardial
cells (arrows) stained by uptake of injected Trypan blue; pea aphids 2 h after injection with 250 ng purified KHisGFP or KHisCP-P-GFP. Arrows indicate
fluorescence in the dorsal aorta (KHisGFP) and pericardial cells (KHisCP-P-GFP). Aphids fed on PBS or KHisGFP showed only background fluorescence
whereas intense fluorescence was seen along the dorsal aorta (arrows) of aphids fed on KHisCP-P-GFP. Scale bar, 0.2 mm.
© 2014 Nature America, Inc. All rights reserved.

In contrast, intense fluorescence was clearly visible in the pericardial
cells of aphids fed on CP-P-GFP (Fig. 1b). Accumulation of CP-P-GFP
in the pericardial cells demonstrates that the viral CP-P sequence
delivered the fused GFP from the aphid gut into the hemocoel, from
which it was subsequently removed by the pericardial cells. This result
reveals that PEMV coat protein is sufficient for peptide delivery into
the aphid hemocoel, without assembly into an intact virion.
To test whether PEMV coat protein can deliver an insect-specific
toxin into the aphid hemocoel, we replaced the RTD except for the
P domain with either Hv1a18 or a mutant protein (Hv1am), which has
two mutations in the pharmacophore of Hv1a (N27A and R35A) that
destroy toxin activity19 (Fig. 1a). These fusion proteins, CP-P-Hv1a
and CP-P-Hv1am, were expressed in Escherichia coli and purified
for aphid feeding assays (Supplementary Fig. 2b). Feeding of the
green peach aphid (M. persicae), the pea aphid (A. pisum), the bird
cherry-oat aphid (R. padi) and the soybean aphid (A. glycines) with
150 ng/ l of either CP-P-Hv1a or CP-P-Hv1am or 200 ng/ l of Hv1a
resulted in significantly higher mortality in aphids fed with
npg
CP-P-Hv1a in the aphid hemocoel was confirmed by isolating hemo-
lymph from aphids fed on CP-P-Hv1a or diet alone by a membrane
feeding assay, and conducting western blot analysis with Hv1a antise-
rum (Fig. 2). Taken together these results demonstrate that PEMV
CP-P-Hv1a is aphicidal. In contrast, no mortality was seen in larvae
of Heliothis virescens, order Lepidoptera (0/30 for all treatments, ten
larvae per treatment, replicated three times), feeding on CP-P-Hv1a
or controls in droplet feeding assays.
To assess the aphicidal efficacy of CP-P-Hv1a when expressed
in transgenic plants, we transformed Arabidopsis thaliana to sta-
bly express CP-P-GFP, CP-P-Hv1a, CP-P-Hv1am or Hv1a (Fig. 1a).
Second-generation progeny (T2) plants from 19 CP-P-Hv1a,
15 CP-P-Hv1am, ten Hv1a and five CP-P-GFP lines, each representing
an independent transformation event, were screened by full-length
and real-time RT-PCR to confirm transcription from the trans-
gene (Supplementary Table 2). Protein expression in T2 plants was
detected by western blot analyses (Supplementary Fig. 3a) and by flu-
orescence microscopy for GFP constructs (Supplementary Fig. 3b).

CP-P-Hv1a compared to aphids fed with CP-P-Hv1am, Hvla or diet
alone (P < 0.0001, Fisher’s exact test with Bonferroni correction; Fig. 2
and Supplementary Table 1). The concentration at which 50% of
aphids die (LC50) for CP-P-Hv1a in M. persicae after oral ingestion was
80 ng/ l diet (95% CI = 60–98 g/ l diet; slope = 4.6 1.1;
natural response = 0.2 0.06; heterogeneity = 0.18). Concentrations
>180 ng/ l resulted in 100% mortality by day 5. The presence of
The presence of fusion proteins in the phloem sap was confirmed for
lines expressing CP-P-Hv1a and CP-P-GFP by western blot analy-
sis (Supplementary Fig. 3c). Among the T2 lines, CP-P-Hv1a and
CP-P-Hv1am accumulated to 0.45% of total soluble protein, CP-P-GFP
to levels ranging from 0.10% to 0.68% of total soluble protein and
Hv1a ranged from 0.51% (line gssHv5-6) to 0.12% (lines gssHv2-1
and gssHv4-1) of total soluble protein (Supplementary Fig. 3a).

90 CP-P-Hv1a Figure 2 Mortality of four species of aphid fed on CP-P-Hv1a or control

a CP-P-Hv1am treatments (CP-P-Hv1am, Hv1a or mock) in membrane feeding assays.
80
a Hv1a Percent mortality ( s.e.m.) was recorded after 5 d (for M. persicae,
70 a
a Mock A. pisum and A. glycines) on complete diet, or after 20 h for R. padi fed
Percentage mortality

60 on 25% sucrose in PBS. The bioassay included three biological replicates

50 with 15 aphids per treatment per replicate. Letters indicate statistically
b significant differences for each species (P < 0.0001; Fisher’s exact test with
40
a
v1

Bonferroni correction: Supplementary Table 1). For M. persicae, mortality

H
P-
k

30 b b b in the Hv1a treatment was significantly different from mock at the 5% level
oc

Mr
P-

b b b
M

b b 37
20 b b of significance (Fisher’s exact test: Supplementary Table 1). Bioassays
b 25 conducted at a higher dose of 100 g/ l confirmed that Hv1a is not orally
10
toxic to M. persicae13. Inset: western blot of CP-P-Hv1a in the hemolymph
0 of aphids following membrane feeding for 72 h. Arrow indicates expected
M. persicae A. pisum R. padi A. glycines 28-kDa CP-P-Hv1a detected using Hv1a antiserum. Lanes contain
Aphid species hemolymph proteins from aphids fed diet only (mock) or diet plus CP-P-Hv1a.

NATURE BIOTECHNOLOGY VOLUME 32 NUMBER 1 JANUARY 2014 103

 LETTERS

Figure 3 Aphid populations on transgenic Arabidopsis. (a) Mean a 300 Day 17 b b

b
b
250
number of A. pisum per T2 plant at day 17 (top panel) and survival of
200
M. persicae during the course of a 17-d bioassay (bottom panel) on
150
transgenic plants expressing CP-P-Hv1a, CP-P-Hv1am, gssHv1a alone or 100
CP-P-GFP
CP-P-GFP. Bioassays included three biological replicates with a total of

Mean no. aphids per plant

50 a
27 plants tested for each treatment. Five M. persicae were transferred to 0
each plant and aphid populations monitored. Error bars represent s.e.m.

am

FP
v1

v1

G
v1
H

sH
Different letters indicate statistical difference (P < 0.0001; Tukey’s

P-
P-

gs

P-
P-
P-
HSD test). (b) Aphid infestation on control plants (top left) compared to

C
P-
C
CP-P-Hv1a

C
plants expressing CP-P-Hv1a (bottom left). Aphids on plants expressing 300
CP-P-Hv1a
CP-P-Hv1a died with signs of paralysis (extended legs; bottom right) in 250 CP-P-Hv1am
contrast to the folded legs typical of insects that die from natural causes 200 gssHv1a
CP-P-GFP
(top right). 150
100
50
0
Lines with high concentrations of proteins encoded by transgenes 0 3 6 11 14 17
were tested for toxicity to aphids. Day

Bioassays were conducted with M. persicae on T2 Arabidopsis

plants expressing CP-P-Hv1a, CP-P-Hv1am, CP-P-GFP or gssHv1a
(Hv1a with the snowdrop lectin Galanthus nivalis agglutinin (GNA)
secretory signal), with 27 plants tested per treatment. Aphid num-
bers were recorded for a period of 17 d. All negative controls, that
is, lines expressing CP-P-Hv1am, CP-P-GFP and gssHv1a, showed
© 2014 Nature America, Inc. All rights reserved.
few cases these proteins suppress insect development21,22. GNA binds
to mannose residues in the insect gut and crosses the gut epithelium
into the insect hemocoel23. In addition to the toxic effect resulting
from GNA binding to the gut epithelium, bioassays with recombinant
fusion proteins have shown that GNA can also be used to deliver

significantly higher aphid numbers per plant by day 17 compared
to lines expressing CP-P-Hv1a (P < 0.0001: Tukey’s honestly signifi-
cant difference (HSD) test; Fig. 3a and Supplementary Table 1).
No significant differences in mean number of aphids per plant were
observed among the control lines (P = 0.56 for CP-P-Hv1am and
gssHv1a; P = 1.0 for CP-P-Hv1am and CP-P-GFP; P = 0.6 for
CP-P-GFP and gssHv1a; Tukey’s HSD test: Supplementary Table 1).
All three sets of control plants had mean aphid counts per plant similar
to those seen on wild-type Arabidopsis (258 39) at day 17. Aphid
numbers continued to increase on control lines over the 17-d bioassay
period, whereas populations were suppressed on plants expressing
CP-P-Hv1a (Fig. 3a). The stems and leaves of control plants express-
ing CP-P-Hv1am, CP-P-GFP or gssHv1a alone were heavily infested
with aphids, in contrast to plants expressing CP-P-Hv1a (Fig. 3b).
Heavy aphid infestation resulted in necrosis and damage of all con-
trol plants by day 17, whereas CP-P-Hv1a plants appeared healthy
(Supplementary Fig. 4). Aphids that died after feeding on CP-P-Hv1a
plants showed signs of paralysis with legs extended rather than folded
npg
peptide toxins into the hemocoel of pest insects24–26. However, GNA-
mediated toxin delivery lacks the specificity of coat protein–mediated
toxin delivery, potentially to the detriment of nontarget and beneficial
insects. We also expect that luteovirids have evolved for efficient
transcytosis across the gut epithelium of the hemipteran vector, that is, to
avoid being targeted to the lysosome on entry into the gut epithelial
cell, in contrast to other proteins27.
Insect-specific toxins that act only within the hemocoel of the
insect constitute an untapped resource for the development of insect-
resistant transgenic plants. Because these toxins are not orally active,
they require a means of delivery from the insect gut into the hemo-
coel. We have shown that the PEMV coat protein can deliver one
such toxin to aphids. The range of aphid species that can be targeted
using this approach may be large because luteovirid virions enter
the hemocoel of nonvector aphids23. This supposition is supported
by the toxicity of CP-P-Hv1a to R. padi and A. glycines, which are
not vectors of PEMV. Hence, a transgene consisting of a PEMV coat
protein–toxin fusion is expected to be effective against multiple aphid

(Fig. 3b). Hence, CP-P-Hv1a fusions delivered by transgenic plants
were aphicidal.
This work demonstrates the use of a coat protein derived from a
plant virus that is transmitted by hemipteran vectors to make an insect
neurotoxin orally toxic. Such toxins typically lack toxicity on ingestion
because they act within the insect hemocoel rather than the gut. The
toxin Hv1a is aphicidal by injection, but has no significant oral toxic-
ity13. Key aspects of this strategy are that inclusion of the proline-rich
domain at the N terminus of RTD is required to retain solubility of
the fusion protein (Supplementary Fig. 1) and that virion forma-
tion is unnecessary for movement of coat protein across the aphid
gut epithelium. To our knowledge, no previous study has shown that
virion assembly is not necessary for entry of viral coat protein into the
hemolymph. PEMV coat protein–mediated delivery of cargo into the
aphid hemolymph was demonstrated directly by fluorescence of peri-
cardial cells after ingestion of CP-P-GFP (Fig. 1b), and western blot
detection of CP-P-Hv1a in the hemolymph after feeding (Fig. 2), and
indirectly by mortality of aphids fed on CP-P-Hv1a in experimental
membrane sachets (Fig. 2) and from transgenic plants (Fig. 3a), and
observation of toxin-induced paralysis (Fig. 3b).
In addition to luteovirid coat protein, a variety of proteins transcy-
tose across the insect gut epithelium into the hemocoel20, and in a
species. Given that only aphids transmit luteovirids, the luteovirid
CP-P fusion strategy for toxin uptake is expected to be specific to aphids,
without harming nontarget organisms. Indeed, we saw no toxicity
of the CP-P-Hv1a fusion protein to the lepidopteran, H. virescens.
Identification of the PEMV receptor in the aphid gut and increased
understanding of the mechanisms of transcytosis across the insect gut
epithelium may facilitate adaptation of this strategy for management
of other insect pests of economic importance.
METHODS
Methods and any associated references are available in the online
version of the paper.
Note: Any Supplementary Information and Source Data files are available in the
online version of the paper.
ACKNOWLEDGMENTS
We thank R. Harrison, US Department of Agriculture (USDA), Beltsville,
Maryland, for construction of the baculovirus expressing CP-GFP and for
production of the PEMV coat protein antiserum. This work was supported by the
USDA North Central Biotechnology Initiative grant number 97-34340-3987,
USDA National Research Initiative grant number 02-01280, Australian
Research Council Discovery Grant DP0774245, Bayer Crop Science, Syngenta,

104 VOLUME 32 NUMBER 1 JANUARY 2014 NATURE BIOTECHNOLOGY


DuPont Pioneer, Grow Iowa Values Funds, Iowa State University Plant Sciences
Institute, and by Hatch Act and State of Iowa funds. Mention of trade names or
commercial products in this publication is solely for the purpose of providing
specific information and does not imply recommendation or endorsement by the
US Department of Agriculture.
AUTHOR CONTRIBUTIONS
W.A.M. devised the coat protein–toxin fusion strategy; B.C.B. and W.A.M. planned
the experiments, interpreted results and wrote the manuscript; N.P. conducted
E. coli expression of fusion proteins, generation and molecular testing of transgenic
plants, membrane feeding assays and aphid feeding bioassays with transgenic
plants; S.L. conducted aphid microinjections and preliminary experiments;
Z.W. constructed plasmids and performed preliminary experiments; S.S.
conducted research with baculovirus expressed fusions; G.F.K. provided oversight
for use of the Hv1a toxin. P.M.D. conducted the statistical analyses.
COMPETING FINANCIAL INTERESTS
The authors declare competing financial interests: details are available in the online
version of the paper.
Reprints and permissions information is available online at http://www.nature.com/
reprints/index.html.
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105
 ONLINE METHODS
Construction of recombinant baculoviruses expressing EGFP. The CP-GFP
construct (Fig. 1a), which lacks a stop codon between coat protein and GFP,
was obtained in two steps, by fusing a cDNA clone of PEMV RNA-1 (ref. 28)
with the GFP coding sequence (Invitrogen). First, the cp and gfp sequences
were each amplified by PCR. Second, the two fragments were combined to gen-
erate CP-GFP. The first fragment was obtained by using primers PEMV19F and
PEMV10R (Supplementary Table 3). The second fragment was obtained with
PEMV9F and PEMV5R. The coat protein and GFP PCR products were then
combined by PCR using the PEMV19F and PEMV5R primers. The CP-P-GFP
construct, containing the proline-rich region of the RTD sequence (P) between
the coat protein and GFP sequences, was obtained in a similar manner. The first
fragment (CP-P) was amplified with primers PEMV19F and PEMV18R using
a CP-RTD construct without the stop codon as template14. GFP was amplified
using PEMV17F and PEMV5R primers. The CP-P and GFP PCR products
were then combined by PCR using the PEMV19F and PEMV5R primers. The
EGFP construct alone was amplified using GFP1F and the PEMV5R primers.
Constructs were made with N-terminal His tags and Kozak sequences, as
described previously14. The PCR-amplified coat protein, CP-GFP, CP-P-GFP
and GFP fragments were cloned into pFastBac1 (Invitrogen), and the baculo-
viruses vPEMV-CP-GFP, vPEMV-HisCP-GFP, vPEMV-KHisCP-P-GFP and
vKHisGFP produced. Construction of the recombinant baculovirus carrying
sequences for the PEMV coat protein alone (vPEMV-CP) is described else-
© 2014 Nature America, Inc. All rights reserved.
where14. Viruses were amplified and recombinant proteins expressed in Sf21
cells (Life Technologies 11497-013) using standard procedures.
Analysis and purification of baculovirus-expressed recombinant proteins.
To assess the solubility of CP-GFP and CP-P-GFP, we resuspended cells har-
vested 72 h post infection (p.i.) in lysis buffer (50 mM NaH2PO4; 300 mM
NaCl; 1% Igepal CA-630) and sonicated them. The lysate was centrifuged at
10,000g for 20 min and the supernatant and pellet subjected to western blot
analysis with polyclonal GFP antibody (Invitrogen). To confirm baculovirus
expression of recombinant proteins, we infected Sf21 cells at a multiplicity of
infection (m.o.i.) of 5 plaque-forming units (pfu/cell and harvested cells 72 h
p.i. Proteins from 50,000 cell equivalents were run on 12% SDS-PAGE gels and
stained or transferred to Hybond-P PVDF membrane (Amersham Biosciences)
for western blot analysis. Blots were probed with polyclonal PEMV-CP antise-
rum11 or GFP antiserum (Sigma G6539). Bound antibodies were visualized
using the ECL Plus system (Amersham Biosciences).
For fluorescence analysis, virus-infected Sf21 cells were harvested, pelleted,
washed with PBS, placed in a glass slide and examined for fluorescence using
a Zeiss Axioplan 2 fluorescence microscope (FITC; excite: 480/40 nm; emit
npg
535/50 nm). For immunoelectron microscopy, Sf21 cells were infected at an
m.o.i. of 10 and harvested 72 h p.i. The cells were pelleted and processed
for examination using a JEOL 1200EX STEM at 80 kV. Recombinant pro-
teins in embedded cells were detected using GFP antiserum. Cells harvested
at 72 h p.i. were analyzed for the presence of virions by transmission
electron microscopy.
Recombinant His-tagged proteins were purified by employing Ni-NTA resin
according to the manufacturer’s protocol (Qiagen). Purified proteins were
analyzed using SDS-PAGE, dialyzed overnight in PBS, then concentrated using
Centricon/Microcon concentrators (3 kDa MWCO; Millipore).
Aphid injection assays. Injection assays were done on a microinjector as
described29. Individual pea aphids were injected with 100 nl of the purified,
baculovirus-expressed GFP and CP-P-GFP by using ultra-thin glass capillary
tubes. Control aphids were injected with PBS. To visualize the pericardial
cells, we injected aphids with 50 nl Trypan blue and dissected them 1 h
after injection.
E. coli expression of CP-P-Hv1a and CP-P-Hv1am. Overlapping PCR was
used to generate the CP-P-Hv1a and CP-P-Hv1am fusion expression con-
structs. Primers BamHI-CP and CPP-Hv1a-r (Supplementary Table 2) were
used to amplify coat protein and the proline-rich coding region (P) from
the fused CP-RTD template lacking the coat protein stop codon. Primers
CPP-Hv1a-f and Hv1a-r, CPP-Hv1a-f and Hv1a-mr were used to amplify Hv1a and
Hv1am from pHWT1 (ref. 19) and pHWT1-N27AR35A (ref. 30), respectively.
NATURE BIOTECHNOLOGY
Primers BamHI CP/Hv1a-r and BamHI-CP/Hv1a-mr were then applied to
fuse CP-P-Hv1a and CP-P-Hv1am by overlap PCR from CP-P/Hv1a and
CP-P/Hv1am PCR products. The final products were digested with BamH1
and EcoRI and inserted into pGEX-2T (GE LifeSciences). E. coli BL21 (DE3)
pLysS cells were transformed with pGEX CP-P-Hv1a and pGEX CP-P-Hv1am.
Protein induction and purification using glutathione sepharose 4B affinity
resin (Amersham Bioscience) were conducted according to the manufacturer’s
instructions. After thrombin cleavage, fusion proteins were eluted from the
column with PBS.
Aphid membrane feeding assays. Purified, baculovirus-expressed recom-
binant proteins (KHisGFP, KHisCP-P-GFP) were fed to starved pea aphids
(15 per treatment) using a membrane feeding assay. Aphids were allowed to
feed on parafilm sachets containing purified preparations of the recombinant
proteins in 25% sucrose. Control aphids were fed on 25% sucrose alone. Aphids
were examined for fluorescence after 16 h using a Zeiss Axioplan 2 fluores-
cence microscope.
For aphid feeding bioassays with E. coli–produced recombinant fusion pro-
teins, 15 fourth instar A. pisum, M. persicae, A. glycines or R. padi were used per
treatment per replicate, with a total of three biological replicates. Fifteen aphids
in each replicate were allowed to feed on 100 l of the complete diet31 alone
(control) or complete diet containing 15 g of CP-P-Hv1a or CP-P-Hv1am or
20 g of Hv1a alone (purified as described previously19) in a parafilm sachet
for 5 d with diet change every third day. R. padi, which does not feed on com-
plete diet, was fed on 25% sucrose in PBS for 20 h.
To determine the LC50 for CP-P-Hv1a by oral feeding, we fed M. persicae
on different doses (3, 6, 9, 12 or 15 g in 100 l diet) of pGEX-purified
CP-P-Hv1a expressed in E. coli. Three biological replicates were set up for
each dose, with 15 aphids per dish fed continuously for 7 d with diet changed
every third day.
Detection of CP-P-Hv1a in the aphid hemocoel. To detect CP-P-Hv1a in the
aphid hemocoel, we membrane fed 60 pea aphids for 72 h on artificial diet
containing 1% blue food coloring and either no recombinant protein (controls)
or 950 ng/ l CP-P-Hv1a. Hemolymph was extracted only from aphids that
had fed, indicated by uptake of food coloring32. Hemolymph proteins were
concentrated using Amicon 0.5 ml ultracentrifugation columns, and detected
by western blot analysis with the Hv1a antiserum24 with 57 g total protein
per lane on 12% SDS-PAGE gels.
Stable expression of CP-P-Hv1a in Arabidopsis thaliana. The plant expres-
sion vectors were constructed by insertion of the CP-P-GFP, CP-P-Hv1a,
CP-P-Hv1am or gssHv1a coding sequences between the Cauliflower mosaic virus
(CaMV) 35S promoter and Nos terminator of pBITG containing a viral trans-
lation enhancer (TMV ). The plasmids were transformed into strain C58C1
of Agrobacterium tumefaciens and used for Agrobacterium-mediated transfor-
mation of A. thaliana Col-0 plants by floral dip33. Plants were grown at 24 °C,
light/dark, 12 h:12 h. Recombinant protein expression in Arabidopsis was
confirmed by western blot analysis. Two to three leaves from each plant were
ground in liquid nitrogen, homogenized in 100 l of protein extraction buffer
(50 mM Tris, pH 7.5, 50 mM KCl, 4 mM EDTA, 1 g/ml PMSF) and incubated
on ice for 15 min with occasional mixing followed by two centrifugations at
16,000g. The supernatant was transferred to a fresh tube and protein concen-
tration measured by Bradford assay. Protein (75 g) was loaded on a 12% or
15% (gssHv1a) SDS PAGE gel for blotting. Bound antibodies were detected
with HyGlo chemiluminescent HRP antibody detection reagent (Denville
Scientific, NJ). The signals were quantified using ImageJ software34.
To detect fusion proteins in phloem, we collected sap from leaves with cut
petioles into PBS containing 5 mM EDTA for 24 h. Proteins were concen-
trated (Amicon 0.5 ml ultracentrifugation columns) and detected by western
blot analysis.
Feeding bioassay using transgenic Arabidopsis thaliana. Bioassays were
conducted on T2 plants expressing CP-P-Hv1a, CP-P-Hv1am, CP-P-GFP and
gssHv1a. The bioassay conducted in a randomized complete block design
included three biological replicates, each replicate consisting of three plants
of three independently derived transgenic lines (i.e., nine plants per replicate
doi:10.1038/nbt.2753
 per construct for each of three transgenic lines) of CP-P-Hv1a, CP-P-Hv1am,
CP-P-GFP and gssHv1a. A total of 27 plants was tested for each transgene.
Wild-type Arabidopsis Col-0 plants were also used as a control. Five fourth
instar M. persicae were transferred to each plant and aphids counted for a
period of 17 d.
H. virescens bioassay. Bioassays with 1.1 mg/ml CP-P-Hv1a, CP-P-Hv1am
and 30 g/ml Hv1a were conducted with neonate larvae of H. virescens (15 per
treatment with three replicates) using a droplet feeding assay35. Larvae that had
fed after 15 min (indicated by green coloration of the gut from dye included in
treatment) were transferred to cups with artificial diet at 28 °C and monitored
for mortality.
Statistical analyses. For membrane feeding assays, statistical analysis was
conducted using Fisher’s exact test with Bonferroni correction. As there was
no evidence of extra-binomial variation among replicates of membrane feeding
bioassays, the numbers of live and dead aphids were summed across the three
replicates before comparison of percent mortality. Preliminary inspection of
the transgenic plant bioassay data indicated no evidence of non-normality
but that one insert had a markedly smaller variance. Hence these data were
analyzed with a one-way ANOVA that allowed each insert to have a unique
variance. Degrees of freedom were estimated by the Satterthwaite approxima-
tion. P values for comparisons between pairs of inserts were adjusted using
© 2014 Nature America, Inc. All rights reserved.
Tukey’s HSD correction for multiple comparisons. SAS/STAT36 software, ver-
sion 9.3, was used for these analyses. All tests were two-sided tests. The LC50
npg
doi:10.1038/nbt.2753
for CP-P-Hv1a in aphid membrane feeding assays was calculated by probit
analysis using PoloPlus version 2.0 (ref. 37). No statistical method was used
to predetermine sample size. The investigators were not blinded to allocation
during experiments and outcome assessment.
28. Demler, S.A., Rucker-Feeney, D.G., Skaf, J.S. & deZoeten, G.A. Expression and
suppression of circulative aphid transmission in pea enation mosaic virus. J. Gen.
Virol. 78, 511–523 (1997).
29. Fukatsu, T., Tsuchida, T., Nikoh, N. & Koga, R. Spiroplasma symbiont of the pea
aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 67,
1284–1291 (2001).
30. Tedford, H.W. et al. Scanning mutagenesis of -atracotoxin-Hv1a reveals a spatially
restricted epitope that confers selective activity against insect calcium channels.
J. Biol. Chem. 279, 44133–44140 (2004).
31. Febvay, G., Delobel, B. & Rahbe, Y. Influence of the amino-acid balance on the
improvement of an artificial diet for a biotype of Acyrthosiphon pisum (Homoptera,
Aphididae). Can. J. Zool. 66, 2449–2453 (1988).
32. Liu, S., Bonning, B.C. & Miller, W.A. A simple wax-embedding method for isolation
of aphid hemolymph for detection of luteoviruses in the hemocoel. J. Virol. Methods
132, 174–180 (2006).
33. Clough, S.J. & Bent, A.F. Floral dip: a simplified method for Agrobacterium-mediated
transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).
34. Collins, T.J. ImageJ for microscopy. Biotechniques 43, S25–S30 (2007).
35. Hughes, P.R., Van Beek, N.A.M. & Wood, H.A. A modified droplet feeding method
for rapid assay of Bacillus thuringiensis and baculoviruses in noctuid larvae.
J. Invertebr. Pathol. 48, 187–192 (1986).
36. SAS Institute. SAS/STAT(R) 9.3 User’s Guide (SAS Institute Inc., Cary NC, 2013).
37. LeOra-Software POLO-PC. A User’s Guide to Probit and Logit Analysis (LeOra
Software, Berkeley, California, 1987).
NATURE BIOTECHNOLOGY
5/28/22, 11:38 AM Plant virus - Wikipedia

Plant virus
Plant viruses are viruses that affect plants. Like all other viruses,
plant viruses are obligate intracellular parasites that do not have
the molecular machinery to replicate without a host. Plant viruses
can be pathogenic to higher plants.

Most plant viruses are rod-shaped, with protein discs forming a

tube surrounding the viral genome; isometric particles are another
common structure. They rarely have an envelope. The great
majority have an RNA genome, which is usually small and single
stranded (ss), but some viruses have double-stranded (ds) RNA,
ssDNA or dsDNA genomes. Although plant viruses are not as well
understood as their animal counterparts, one plant virus has Pepper mild mottle virus
become very recognizable: tobacco mosaic virus (TMV), the first
virus to be discovered. This and other viruses cause an estimated
US$60 billion loss in crop yields worldwide each year. Plant
viruses are grouped into 73 genera and 49 families. However,
these figures relate only to cultivated plants, which represent only
a tiny fraction of the total number of plant species. Viruses in wild
plants have not been well-studied, but the interactions between
wild plants and their viruses often do not appear to cause disease
in the host plants.[1]

To transmit from one plant to another and from one plant cell to
Leaf curl virus
another, plant viruses must use strategies that are usually different
from animal viruses. Most plants do not move, and so plant-to-
plant transmission usually involves vectors (such as insects). Plant
cells are surrounded by solid cell walls, therefore transport through plasmodesmata is the preferred
path for virions to move between plant cells. Plants have specialized mechanisms for transporting
mRNAs through plasmodesmata, and these mechanisms are thought to be used by RNA viruses to
spread from one cell to another.[2] Plant defenses against viral infection include, among other
measures, the use of siRNA in response to dsRNA.[3] Most plant viruses encode a protein to suppress
this response.[4] Plants also reduce transport through plasmodesmata in response to injury.[2]

Contents
History
Structure
Transmission of plant viruses
Through sap
Insects
Nematodes
Plasmodiophorids
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Seed and pollen borne viruses

Direct plant-to-human transmission
Effects on hosts
Translation of plant viral proteins
5' Cap
Readthrough
Production of sub-genomic RNAs
Segmented genomes
Polyprotein processing
Genome packaging
Applications of plant viruses
References
Further reading
External links

History
The discovery of plant viruses causing disease is often accredited to A.
Mayer (1886) working in the Netherlands demonstrated that the sap of
mosaic obtained from tobacco leaves developed mosaic symptom when
injected in healthy plants. However the infection of the sap was destroyed
when it was boiled. He thought that the causal agent was bacteria.
However, after larger inoculation with a large number of bacteria, he
failed to develop a mosaic symptom.

In 1898, Martinus Beijerinck, who was a Professor of Microbiology at the

Technical University the Netherlands, put forth his concepts that viruses
were small and determined that the "mosaic disease" remained infectious
when passed through a Chamberland filter-candle. This was in contrast to
bacteria microorganisms, which were retained by the filter. Beijerinck Electron micrograph of the
referred to the infectious filtrate as a "contagium vivum fluidum", thus rod-shaped particles of
tobacco mosaic virus
the coinage of the modern term "virus".

After the initial discovery of the 'viral concept' there was need to classify
any other known viral diseases based on the mode of transmission even though microscopic
observation proved fruitless. In 1939 Holmes published a classification list of 129 plant viruses. This
was expanded and in 1999 there were 977 officially recognized, and some provisional, plant virus
species.

The purification (crystallization) of TMV was first performed by Wendell Stanley, who published his
findings in 1935, although he did not determine that the RNA was the infectious material. However,
he received the Nobel Prize in Chemistry in 1946. In the 1950s a discovery by two labs simultaneously
proved that the purified RNA of the TMV was infectious which reinforced the argument. The RNA
carries genetic information to code for the production of new infectious particles.

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More recently virus research has been focused on understanding the genetics and molecular biology of
plant virus genomes, with a particular interest in determining how the virus can replicate, move and
infect plants. Understanding the virus genetics and protein functions has been used to explore the
potential for commercial use by biotechnology companies. In particular, viral-derived sequences have
been used to provide an understanding of novel forms of resistance. The recent boom in technology
allowing humans to manipulate plant viruses may provide new strategies for production of value-
added proteins in plants.

Structure
Viruses are extremely small and can only be observed under an
electron microscope. The structure of a virus is given by its coat of
proteins, which surround the viral genome. Assembly of viral
particles takes place spontaneously.

Over 50% of known plant viruses are rod-shaped (flexuous or

rigid). The length of the particle is normally dependent on the
genome but it is usually between 300 and 500 nm with a diameter
of 15–20 nm. Protein subunits can be placed around the Structural comparison of some plant
circumference of a circle to form a disc. In the presence of the viral viruses
genome, the discs are stacked, then a tube is created with room for
the nucleic acid genome in the middle.[5]

The second most common structure amongst plant viruses are isometric particles. They are 25–50 nm
in diameter. In cases when there is only a single coat protein, the basic structure consists of 60 T
subunits, where T is an integer. Some viruses may have 2 coat proteins that associate to form an
icosahedral shaped particle.

There are three genera of Geminiviridae that consist of particles that are like two isometric particles
stuck together.

A very small number of plant viruses have, in addition to their coat proteins, a lipid envelope. This is
derived from the plant cell membrane as the virus particle buds off from the cell.

Transmission of plant viruses

Through sap

Viruses can be spread by direct transfer of sap by contact of a wounded plant with a healthy one. Such
contact may occur during agricultural practices, as by damage caused by tools or hands, or naturally,
as by an animal feeding on the plant. Generally TMV, potato viruses and cucumber mosaic viruses are
transmitted via sap.

Insects

Plant viruses need to be transmitted by a vector, most often insects such as leafhoppers. One class of
viruses, the Rhabdoviridae, has been proposed to actually be insect viruses that have evolved to
replicate in plants. The chosen insect vector of a plant virus will often be the determining factor in that

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virus's host range: it can only infect plants that the insect vector
feeds upon. This was shown in part when the old world white fly
made it to the United States, where it transferred many plant
viruses into new hosts. Depending on the way they are
transmitted, plant viruses are classified as non-persistent, semi-
persistent and persistent. In non-persistent transmission, viruses
become attached to the distal tip of the stylet of the insect and on
the next plant it feeds on, it inoculates it with the virus.[6] Semi-
persistent viral transmission involves the virus entering the
foregut of the insect. Those viruses that manage to pass through
the gut into the haemolymph and then to the salivary glands are
known as persistent. There are two sub-classes of persistent
Plant virus transmission strategies
viruses: propagative and circulative. Propagative viruses are able in insect vectors.
to replicate in both the plant and the insect (and may have
originally been insect viruses), whereas circulative can not.
Circulative viruses are protected inside aphids by the chaperone protein symbionin, produced by
bacterial symbionts. Many plant viruses encode within their genome polypeptides with domains
essential for transmission by insects. In non-persistent and semi-persistent viruses, these domains are
in the coat protein and another protein known as the helper component. A bridging hypothesis has
been proposed to explain how these proteins aid in insect-mediated viral transmission. The helper
component will bind to the specific domain of the coat protein, and then the insect mouthparts –
creating a bridge. In persistent propagative viruses, such as tomato spotted wilt virus (TSWV), there is
often a lipid coat surrounding the proteins that is not seen in other classes of plant viruses. In the case
of TSWV, 2 viral proteins are expressed in this lipid envelope. It has been proposed that the viruses
bind via these proteins and are then taken into the insect cell by receptor-mediated endocytosis.

Nematodes

Soil-borne nematodes also have been shown to transmit viruses.[7] They acquire and transmit them by
feeding on infected roots. Viruses can be transmitted both non-persistently and persistently, but there
is no evidence of viruses being able to replicate in nematodes. The virions attach to the stylet (feeding
organ) or to the gut when they feed on an infected plant and can then detach during later feeding to
infect other plants. Examples of viruses that can be transmitted by nematodes include tobacco
ringspot virus and tobacco rattle virus.

Plasmodiophorids

A number of virus genera are transmitted, both persistently and non-persistently, by soil borne
zoosporic protozoa. These protozoa are not phytopathogenic themselves, but parasitic. Transmission
of the virus takes place when they become associated with the plant roots. Examples include
Polymyxa graminis, which has been shown to transmit plant viral diseases in cereal crops[8] and
Polymyxa betae which transmits Beet necrotic yellow vein virus. Plasmodiophorids also create
wounds in the plant's root through which other viruses can enter.

Seed and pollen borne viruses

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Plant virus transmission from generation to generation occurs in about 20% of plant viruses. When
viruses are transmitted by seeds, the seed is infected in the generative cells and the virus is maintained
in the germ cells and sometimes, but less often, in the seed coat. When the growth and development of
plants is delayed because of situations like unfavorable weather, there is an increase in the amount of
virus infections in seeds. There does not seem to be a correlation between the location of the seed on
the plant and its chances of being infected. [5] Little is known about the mechanisms involved in the
transmission of plant viruses via seeds, although it is known that it is environmentally influenced and
that seed transmission occurs because of a direct invasion of the embryo via the ovule or by an indirect
route with an attack on the embryo mediated by infected gametes. [5] [6] These processes can occur
concurrently or separately depending on the host plant. It is unknown how the virus is able to directly
invade and cross the embryo and boundary between the parental and progeny generations in the
ovule. [6] Many plants species can be infected through seeds including but not limited to the families
Leguminosae, Solanaceae, Compositae, Rosaceae, Cucurbitaceae, Gramineae. [5] Bean common
mosaic virus is transmitted through seeds.

Direct plant-to-human transmission

Researchers from the University of the Mediterranean in Marseille, France have found tenuous
evidence that suggest a virus common to peppers, the Pepper Mild Mottle Virus (PMMoV) may have
moved on to infect humans.[9] This is a very rare and highly unlikely event as, to enter a cell and
replicate, a virus must "bind to a receptor on its surface, and a plant virus would be highly unlikely to
recognize a receptor on a human cell. One possibility is that the virus does not infect human cells
directly. Instead, the naked viral RNA may alter the function of the cells through a mechanism similar
to RNA interference, in which the presence of certain RNA sequences can turn genes on and off,"
according to Virologist Robert Garry from the Tulane University in New Orleans, Louisiana.[10]

Effects on hosts
The intracellular life of plant viruses in hosts is still understudied especially the earliest stages of
infection.[11] Many membranous structures which viruses induce plant cells to produce are motile,
often being used to traffic new virions within the producing cell and into their neighbors.[11] Viruses
also induce various changes to plants' own intracellular membranes.[11] The work of Perera et al. 2012
in mosquito virus infection and various others studying yeast models of plant viruses find this to be
due to changes in homeostasis of the lipids that compose their intracellular membranes, including
increasing synthesis.[11] These comparable lipid alterations inform our expectations and research
directions for the lesser understood area of plant viruses.[11]

Translation of plant viral proteins

75% of plant viruses have genomes that consist of single stranded RNA (ssRNA). 65% of plant viruses
have +ssRNA, meaning that they are in the same sense orientation as messenger RNA but 10% have -
ssRNA, meaning they must be converted to +ssRNA before they can be translated. 5% are double
stranded RNA and so can be immediately translated as +ssRNA viruses. 3% require a reverse
transcriptase enzyme to convert between RNA and DNA. 17% of plant viruses are ssDNA and very few
are dsDNA, in contrast a quarter of animal viruses are dsDNA and three-quarters of bacteriophage are
dsDNA.[13] Viruses use the plant ribosomes to produce the 4-10 proteins encoded by their genome.
However, since many of the proteins are encoded on a single strand (that is, they are polycistronic)
this will mean that the ribosome will either only produce one protein, as it will terminate translation
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at the first stop codon, or that a polyprotein will be produced.

Plant viruses have had to evolve special techniques to allow the
production of viral proteins by plant cells.

5' Cap

For translation to occur, eukaryotic mRNAs require a 5' Cap

structure. This means that viruses must also have one. This
normally consists of 7MeGpppN where N is normally adenine or
guanine. The viruses encode a protein, normally a replicase, with a
methyltransferase activity to allow this.

Some viruses are cap-snatchers. During this process, a 7mG-

capped host mRNA is recruited by the viral transcriptase complex
and subsequently cleaved by a virally encoded endonuclease. The
resulting capped leader RNA is used to prime transcription on the
viral genome.[14] Polyprotein processing is used by
45% of plant viruses. Plant virus
However some plant viruses do not use cap, yet translate families that produce polyproteins,
efficiently due to cap-independent translation enhancers present their genomes, and colored triangles
in 5' and 3' untranslated regions of viral mRNA.[15] indicating self-cleavage sites.[12]

Readthrough

Some viruses (e.g. tobacco mosaic virus (TMV)) have RNA sequences that contain a "leaky" stop
codon. In TMV 95% of the time the host ribosome will terminate the synthesis of the polypeptide at
this codon but the rest of the time it continues past it. This means that 5% of the proteins produced
are larger than and different from the others normally produced, which is a form of translational
regulation. In TMV, this extra sequence of polypeptide is an RNA polymerase that replicates its
genome.

Production of sub-genomic RNAs

Some viruses use the production of subgenomic RNAs to ensure the translation of all proteins within
their genomes. In this process the first protein encoded on the genome, and is the first to be
translated, is a replicase. This protein will act on the rest of the genome producing negative strand
sub-genomic RNAs then act upon these to form positive strand sub-genomic RNAs that are essentially
mRNAs ready for translation.

Segmented genomes

Some viral families, such as the Bromoviridae instead opt to have multipartite genomes, genomes
split between multiple viral particles. For infection to occur, the plant must be infected with all
particles across the genome. For instance Brome mosaic virus has a genome split between 3 viral
particles, and all 3 particles with the different RNAs are required for infection to take place.

Polyprotein processing
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Polyprotein processing is adopted by 45% of plant viruses, such as the Potyviridae and
Tymoviridae.[12] The ribosome translates a single protein from the viral genome. Within the
polyprotein is an enzyme (or enzymes) with proteinase function that is able to cleave the polyprotein
into the various single proteins or just cleave away the protease, which can then cleave other
polypeptides producing the mature proteins.

Genome packaging

Besides involvement in the infection process, viral replicase is a directly necessary part of the
packaging of RNA viruses' genetic material. This was expected due to replicase involvement already
being confirmed in various other viruses.[16]

Applications of plant viruses

Plant viruses can be used to engineer viral vectors, tools commonly used by molecular biologists to
deliver genetic material into plant cells; they are also sources of biomaterials and nanotechnology
devices.[17][18] Knowledge of plant viruses and their components has been instrumental for the
development of modern plant biotechnology. The use of plant viruses to enhance the beauty of
ornamental plants can be considered the first recorded application of plant viruses. Tulip breaking
virus is famous for its dramatic effects on the color of the tulip perianth, an effect highly sought after
during the 17th-century Dutch "tulip mania." Tobacco mosaic virus (TMV) and cauliflower mosaic
virus (CaMV) are frequently used in plant molecular biology. Of special interest is the CaMV 35S
promoter, which is a very strong promoter most frequently used in plant transformations. Viral
vectors based on tobacco mosaic virus include those of the magnICON® (https://www.icongenetics.c
om/technology/) and TRBO plant expression technologies.[18]

Representative applications of plant viruses are listed below.

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Applications of plant viruses[17]

Use Description References
Enhanced plant Increase beauty and commercial value of [19]
aesthetics ornamental plants
Delivery of mild virus strains to prevent [20]
Cross‐protection
infections by their severe relatives
Viruses triggering lethal systemic [21]
Weed biocontrol
necrosis as bioherbicides
Enhanced toxin and pesticide delivery for [22]
Pest biocontrol
insect and nematode control
Nanoparticle Virion surfaces are functionalized and [23]
scaffolds used to assemble nanoparticles
Virions are used to transport cargo [24]
Nanocarriers
compounds
Enzymes are encapsulated into virions to [25]
Nanoreactors
engineer cascade reactions
Recombinant Fast, transient overproduction of
protein/peptide recombinant peptide, polypeptide [26] Application of plant viruses to
expression libraries and protein complexes enhance the plant beauty. The
Semper Augustus, famous for being
Functional Targeted gene silencing using VIGS and [27]
genomic studies miRNA viral vectors the most expensive tulip sold during
tulip mania. The effects of tulip
Targeted genome editing via transient [28][29] breaking virus are seen in the
Genome editing
delivery of sequence‐specific nucleases
striking streaks of white in its red
Metabolic Biosynthetic pathway rewiring to improve petals.
pathway production of native and foreign [30][31]
engineering metabolites
Viral expression of FLOWERING LOCUS
Flowering [32]
T to accelerate flowering induction and
induction
crop breeding
Open‐field use of viral vectors for
Crop gene [17]
transient reprogramming of crop traits
therapy
within a single growing season

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Further reading
Zaitlin, Milton; Palukaitis, Peter (2000). "Advances in Understanding Plant Viruses and Virus
Diseases". Annual Review of Phytopathology. 38: 117–143. doi:10.1146/annurev.phyto.38.1.117
(https://doi.org/10.1146%2Fannurev.phyto.38.1.117). PMID 11701839 (https://pubmed.ncbi.nlm.ni
h.gov/11701839).
Zaitlin, Milton (1998), Discoveries in Plant Biology, New York 14853, USA. pp. 105–110. S. D.
Kung and S. F. Yang (eds).
Dickinson, M. (2003), Molecular Plant Pathology. BIOS Scientific Publishers.
https://web.archive.org/web/20080529082637/http://stinet.dtic.mil/oai/oai?
&verb=getRecord&metadataPrefix=html&identifier=Plant
Wang Daowen; Maule Andrew J (1994). "A Model for Seed Transmission of a Plant Virus: Genetic
and Structural Analyses of Pea Embryo Invasion by Pea Seed-Borne Mosaic Virus" (https://www.n
cbi.nlm.nih.gov/pmc/articles/PMC160477). The Plant Cell. 6 (6): 777–787. doi:10.2307/3869957 (h
ttps://doi.org/10.2307%2F3869957). JSTOR 3869957 (https://www.jstor.org/stable/3869957).
PMC 160477 (https://www.ncbi.nlm.nih.gov/pmc/articles/PMC160477). PMID 12244258 (https://pu
bmed.ncbi.nlm.nih.gov/12244258).
http://www.plantcell.org/cgi/reprint/6/6/777

External links
Plant Viruses Online (https://web.archive.org/web/20061018063001/http://image.fs.uidaho.edu/vid
e/refs.htm), a full list of plant viruses
DPVweb (http://www.dpvweb.net/), on-line plant virus database
Plant virus symptoms (https://web.archive.org/web/20030905193132/http://www.dias.kvl.dk/Plantvi
rology/esymptoms/symp.html) Danish Institute of Agricultural Sciences

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