Viruses of Potato

–
Virus Incidence
in Scottish Seed Crops
Epidemiology & Management

Christophe Lacomme

Science & Advice for Scottish Agriculture,

Edinburgh, UK

SASA © Crown Copyright

 Viruses of Potato:
Epidemiology & Management

Outline
 Virus epidemiology
– Population dynamics of viruses in Scottish seed crops – Survey of growing crops
– Risk posed to crops
– What drives PVY prevalence?
– Transmission & spread of Potato virus Y (PVY) in field conditions

 Control & Management of Viruses and their Aphid vectors

– Aphid monitoring in the UK / Scotland
– Association between aphid species & PVY transmission

 Summary: Implications for the Management of Viruses & their Vectors

SASA © Crown Copyright

 Acknowledgements

 AHDB-Potato Council Project R428 - Aphids & virus transmission in seed potato
The James Hutton Institute, Fera, SASA, SRUC, Scottish Agronomy, Rothamsted Research
http://potatoes.ahdb.org.uk/publications/r428-aphids-virus-transmission-seed-crops

 AHDB-Potato Council Project R449 –

Effectiveness of Mineral oils
Scottish Agronomy, NIAB, SASA, SRUC
http://potatoes.ahdb.org.uk/publications/r449-effectiveness-mineral-oils

 Scottish Government
AFRC-RPID Potato Inspectors
SASA Virology & Entomology staff

SASA © Crown Copyright

 Virus Incidence – Epidemiology – Management
Seed Potatoes

 All Scottish seed crops are inspected for visual symptoms of virus infection
 Growing Crop Inspection: Symptomatic leaf samples are tested at SASA Virology
Laboratory ELISA / Real-Time RT-PCR for 11 most common virus species:
 PLRV, PMTV, PVA, PVM, PVS, PVV, PVX, PVYN, PVYO/C, TRV, TBRV

 Post-harvest testing for viruses for selected seed crops (export, certification)
 Sources of data for epidemiology studies - virus incidence in Scottish seed potatoes
 Use of Suction Trap Data Aphid Monitoring for supporting decisions on aphid management
during the growing season
SASA © Crown Copyright
 Virus Symptoms in Seed Crops

80%
Area of seed crops containing at least one

70%
plant exhibiting virus symptoms

60%
Mosaics Leafroll
50%

40%

30%

20%

10%

0%
1969 1974 1979 1984 1989 1994 1999 2004 2009 2014

• Prevalence of mosaic causing viruses over leaf roll over the past two decades
SASA © Crown Copyright
 Potato Viruses & Tuber Symptoms

Net necrosis (PLRV) Spraing (TRV, PMTV)

Tuber cracking (PVA, PVV, PVY)

PTNRD (PVYNTN)

SASA © Crown Copyright

 Economic Impact of Viruses
Symptoms Virus Species Consequences

Leaf roll PLRV Yield, marketability, downgrade,

fail export tolerances.
(conversion starch to sucrose resulting in
bad chipping quality)

Mild & Severe Mosaic Potyviruses, Yield

(PVA, PVV,PVYC, PVYO, PVYN) USA (2008): 1% virus = loss 170 Kg/Ha
Potexviruses (PVX) Synergism: Severe Mosaic observed in
mixed infection Potyviruses + PVX

Potato Tuber Necrotic PVYN, PVYN-Wilga, PVYNTN

Ringspot Disease
(PTNRD)
Yield, marketability, downgrade,
Tuber Cracking PVA, PVV, PVY Fail export tolerance

Spraing soil-borne viruses

TRV, PMTV

Mild Mosaic Carlaviruses Yield, marketability, fail export tolerance

(PVS, PVM) Synergism: Severe Mosaic
in mixed infections with PVY or PVX
SASA © Crown Copyright
 Seed Area Downgraded per Fault

(figures expressed as a % of seed area entered for inspection)

SASA © Crown Copyright
 Virus Incidence in Symptomatic
Seed Crops

• While virus levels remains low, Potato virus Y (PVYN) relative incidence is increasing
o Trend observed since early 2000’s
• PVYN account for 67% of all virus cases in 2015
• ~ 80% of virus cases are aphid-transmitted viruses ! SASA © Crown Copyright
Potato leaf roll virus (PLRV)

• Infected plants are stunted, leaf roll upwards

• Phloem–restricted virus
• Relative importance of PLRV has decreased
 Healthy seeds
 Breeding PLRV-resistant variety

• Transmitted persistently by the peach potato aphid

 Myzus persicae

• Acquisition of PLRV by feeding (uptake phloem sap)

• Relatively well-controlled:
 Control of aphid vector by aphicides
 M. persicae clones resistant to carbamates, organophosphates,
pyrethroid have been reported

SASA © Crown Copyright

Potyviruses: PVY (PVA, PVV)

• Mild & Severe Mosaic on leaves

• PVY is the most important virus of potato (used to be PLRV)
 Important cause of cultivar degeneration worldwide

• Occasionally associated with tuber growth cracks

 PVA + PVV (Scotland), PVY (Norway)

• PVY is the cause of Potato Ringspot Necrosis Disease (PTRND)

 Outbreak central Europe (1980’s – 1990’s)
 Not observed in the SPCS

• Transmitted non-persistently by aphids

 More than 40 aphid species are known vectors of PVY
 Level of transmission vary between aphid species
 While M. persicae is the most efficient vector, in Scotland cereal aphids
(M. dirhodum, S. avenae) are strongly associated with PVY transmission
 Very short period (second-mins) of acquisition & transmission (leaf probing)
 Aphicides are not efficient in controlling aphids vectors & virus transmission
SASA © Crown Copyright
 Diagnostic & Characterisation of Viruses

 ELISA:
– Monoclonal & Polyclonal antibodies

 Molecular diagnoses & characterisation of

PVY variants:
– Real-Time RT-PCR
– Sequencing Virus Genome

 Biological characterisation:
– Symptoms development on indicator plants
• Tobacco (Vein Necrosis / Mosaic)
• Hypersensitive Response on Potato
cultivars of genotype Nc, Ny, Nz
• PTNRD on Potato

SASA © Crown Copyright

 Characterisation of PVY Species

ELISA Biotype Molecular Type

N N N
O/C O O
O/C C C

N N N, EU-N
O/C O O
Wilga

N, NTN N-Wilga
O/C
N:O

EU-NTN
N NTN, E, Z
NA-NTN
NA

SASA © Crown Copyright

Adapted from Schubert et al, 2007
Relative Percentage of PVY cases (%) Population Dynamics of PVY Variants

Serotype

PVYN

PVYO/C

• Yearly survey PVY species

 Increased relative incidence of PVYN species vs PVYO
SASA © Crown Copyright
Relative Percentage of PVY cases (%) Population Dynamics of PVYO Variants

• Yearly survey PVYO species:

 Diversity of PVYO recombinant species (NA:O, N:O, N-Wilga)
 None of these species is prevalent in Scotland (prevalent in mainland Europe
SASA © Crown & USA)
Copyright
 R1 10038
R1 10001
R1R RC9832
R1 9773
R1 10059
R1 9725

Survey of PVYN Species R1 9736

R1 9583
R1 9676
R1 9787

- Hun-NTN
R1 10039
R1 9586
R1 9748

2010-2011 R1 10057
L26
SASA390-R1
DV76-1
R1 9640
R1 9919
R1 10040
R1 9681
R1 9550
R1 9747
R1 9631
R1 9863
R1 10539
EU-NTN
80 R1 9799
R1 9845
R1 10538
R1 9838
R1 9743
R1 9562
R1 9597
R1 9542
R1 9529
R1 9816
R1 9654
R1 10076
R1 9523
R1 9758
R1 10088
R1 9651
R1F 9579
PVYN Population R1 9730
R1 10042
R1 9827
Structure R1 10537
R1 11301
SASA207
L56
SCRI-O
N-Wilga
EU-NTN = 85% DV71-4 O
86
95
R1R RC9792
SASA110
O
R1 9592
EU-N = 3% R1 9580

82
R1 9552
N605
New-Zealand
EU-N
SCRI-N
NA-NTN = 12% RRA-1
R1 9737
Nicola Germany
R1 9575
100
R1 9941
SASA61
NA-NTN/N
DV69-1 SASA © Crown Copyright
R1 9561
SASA154-R1
Relative Percentage of PVY cases (%) Population Dynamics of PVYN Variants

Serotype Molecular type

PVYEU-NTN

PVYN PVYNA-NTN
PVYEU-N
PVYO/C

•Yearly survey PVYN group:

 PVYEU-NTN is the most prevalent PVY subspecies SASA © Crown Copyright
 PTNRD Index PTNRD Disease Index (DI)
Ranking Isolate Molecular type Average score

1 9561 NA-N/NTN 4

2 9529 EU-NTN 3.5

3 9737 NA-N/NTN 3.5

4 9552 EU-N 3

5 10057 EU-NTN 3

10088
6 (PVYE) EU-NTN 2

7 9792 O 1.5
PTNRD Indexing on cv. Nadine
8 10766 N-Wilga 0.2 SASA © Crown Copyright
 Potato Tuber Necrotic Ringspot Disease
(PTNRD) Development – A Risk Assessment
PTNRD Risk PVY Isolate Varieties Environment
Dis.Index High
EU-NTN Nadine Tuber storage Plant Growth
9529 Igor
NA-NTN Yukon Gold 20°C Glasshouse
Nicola (18°C - 20°C) PVY Environmental
9561
Hermes isolates conditions
9737
EU-N Marfona .
Markies .
9552 .
. .
EU-NTN
. . PTNRD
10057 Desiree . .
10088 .
Saxon
. .
N-Wilga .
.
.
.
O Bintje Potato
.
9792 Spunta Field Grown varieties
.
N-Wilga (variable –
Maris Peer
10766 10°C – 15°C)
Lady Rosetta 10°C - 15°C
King Edward .
O . .
Maris Piper
Low

• All PVY isolates have the ability to cause PTNRD given the right conditions
• PTNRD development is highly dependant on cultivar & environmental conditions
• No obvious association between PVY resistance/susceptibility & PTNRD sensitivity
• So far no obvious association between PVY genetic determinants and PTNRD …
SASA © Crown Copyright
 What drives PVY prevalence ?

 Aphid / Virus Interactions?

– Timing transmission
– Aphid species
– Frequency & Efficiency of transmission

 Plant / Virus Interactions?

– Replication & Movement
– Ability to overcome Host Resistance Mechanisms

 Interactions between virus species?

– Competition between PVY variants

 Environmental conditions ?
- Climate, Symptoms development, …

SASA © Crown Copyright

 Distribution of Viruses per Variety
MARIS PIPER
KING EDWARD
MARIS PEER
ATLANTIC
DESIREE
HARMONY
M. Piper M. Piper SLANEY
MARFONA
CHARLOTTE
CABARET
Valor WILJA
PVYO PVYN DUKE OF YORK
PENTLAND DELL
K. Edward VALOR
M. Peer WINSTON
CARA
ESTIMA
GOLDEN WONDER
M. Peer KERR'S PINK
VALES SOVEREIGN
HERMES

• PVYN is found in twice more varieties

than PVYO & PVA
Hermes

• Susceptibility to PVYN is frequent

Desiree
PVA • Resistance to PVYO and PVA is frequent
Estima
• Information on varietal virus resistance
available mainly for PVYO
http://varieties.ahdb.org.uk/ SASA © Crown Copyright

https://www.europotato.org/menu.php?
 PVY Incidence in Tubers in Relation to Plant Development
100
PVYEU-NTN
of plants infected (%) 80 PVYO
Relative proportion

60

40

20

0
1 WPE 2 WPE 3 WPE 5 WPE 6 WPE 7 WPE 8 WPE 10 WPE

 Suggest higher incidence of plants infected by PVYEU-NTN in older plants as opposed to PVYO
 PVYEU-NTN overcome MPR more efficiently than PVYO ?

 Conundrum!: Whilst potato plants become less susceptible to virus acquisition as they mature,
relationships with suction trap data only ‘become’ significant if catches to day 210 or 220 are included
(i.e. 29 July, 8 August)
 Management of viruses:
• advise early planting to maximise development of Mature Plant Resistance. SASA © Crown Copyright
• virus management is required through to burn down of the crop
 What drives PVY prevalence ?

 Aphid / Virus Interactions?

– Timing of transmission
– Frequency & Efficiency of transmission by aphid
species

 Plant / Virus Interactions?

– Replication & Movement
– Ability to overcome Host Resistance Mechanisms

 Interactions between virus species?

– Competition between PVY variants

 Environmental conditions ?
- Climate, Symptoms development (latent infection), …

SASA © Crown Copyright

 Field Transmission Studies of PVY Variants

PVY EU-NTN PVYNA-NTN PVYO

8m

10 m
- Design of the trial :
- 7 “Infectors” for each PVYO, PVYNA-NTN and PVYEU-NTN isolate
- Tobacco (60 plants per week) and Potato (450 plants Maris Piper) bait plants (~4.5% inoculum)
- Trials run over a 3-year period
- Purpose of the trial:
- Timing of transmission, frequency of transmission, & nature of aphid species
SASA © Crown Copyright
- Spatial distribution & frequency transmission at post harvest (virus PH test individual potato plant)
 Aphid monitoring – Transmission of PVY
Transmission Field trials

Suction trap Yellow water pan traps

- Monitor weekly virus transmission & aphid catches using ST & YWT
• Timing of transmission, frequency of transmission & nature of aphid species

SASA © Crown Copyright

 Epidemiology of PVY
-
Timing and Frequency of Transmission of PVY isolates

90% 400
Weekly Frequency of transmission

PVY Field Transmission – Year 2

PVYEU-NTN

Aphid vector pressure

80% 350
PVYNA-NTN
70% 300
PVYO
60%
Aphid Vector 250
50% Pressure
200
40%
150
30%
20% 100

10% 50
0
01/06/11 08/06 15/06 22/06 29/06 06/07 13/07 20/07 27/07/11

• Higher frequency of transmission for PVYEU-NTN vs PVYNA-NTN and PVYO

• Comparable transmission pattern:
o PVY isolates likely to be transmitted by similar aphid species

SASA © Crown Copyright

 Field Transmission Studies of PVY Variants

PVY EU-NTN PVYNA-NTN PVYO

- Spatial & Frequency of distribution: assess virus incidence in tubers for each potato plant

SASA © Crown Copyright

 Distribution and Incidence of PVY Species
at Post Harvest

PVY- EU-NTN PVY-NA-NTN PVY-O

 Higher incidence of PVYEU-NTN in comparison to PVYNA-NTN and PVYO

SASA © Crown Copyright

 Transmission Efficiency of PVY variants
-
Incidence of PVYO, PVYEU-NTN and PVYNA-NTN in field conditions

Cumulative Relative Incidence of Aphid Transmitted

PVY strains at Post-Harvest
100

Year 1
80
Year 2
Year 3
% PVY incidence

60 Overall

40

20

0
PVYEU-NTN PVYNA-NTN PVYO

• Higher incidence of PVYEU-NTN in progeny tubers (3-fold > PVYNA-NTN & 5-fold > PVYO)
• PVYEU-NTN might outcompete others PVY isolates in field conditions

SASA © Crown Copyright

 Summary - Part 1
• While virus incidence is low, aphid transmitted viruses represent ~ 80% of
virus cases

 Cereal aphids are the main vectors of PVY in Scotland

• PVYN species are found worldwide however PTNRD is not observed in the
SPCS
 PTNRD can be observed upon infection by different types of PVY strains
 dependant on environmental conditions & on PVY species / variety
combination

• Control and management of viruses:

 Viruses (PVY) are efficiently transmitted to tubers:
o Plant high quality seed
o Ensure seed crops are free of viruses
 A wide range of colonizing & non-colonizing aphid species can transmit PVY:
o Control potential sources of inoculum (roguing, proximity of ware crops)
o Prevent aphid build up in crops & when possible neighbouring crops
 Advise early planting to maximise development of Mature Plant Resistance.
 Virus management is required through to burn down of the crop SASA © Crown Copyright
 Control & Management of Viruses & their Aphid Vectors
Aphid Monitoring in the UK

http://www.rothamsted.ac.uk/insect-survey-bulletins/count-maps

http://aphmon.fera.defra.gov.uk/ https://www.sasa.gov.uk/wildlife-environment/aphid-monitoring/

SASA © Crown Copyright

 Aphid Monitoring: Dissemination
https://www.sasa.gov.uk/wildlife-environment/aphid-monitoring/

 SASA website:
 Weekly Suction Trap Data
 Weekly aphid bulletins
 Aphid Prediction
 Email on request (let us know…) / SMS alert from AHDB (Claire Hodge)

 Suction Trap Data can be used to support decisions on aphid management during the growing season
- Assist decision making: Haulm destruction, spraying (insecticide, mineral oil,…)
SASA © Crown Copyright
Population development of cereal aphids
monitored by suction traps

SASA © Crown Copyright

SASA © Crown Copyright
 Summary - Part 2
Aphid Monitoring & Virus Transmission - Scotland
 Virus symptoms in crops are the result of transmission in the previous season
in Scotland
 There is a strong relationship between transmission of Potato Leafroll (PLRV)
and Suction Trap catches of Peach-Potato aphids Myzus persicae
 Significant relationships exist between transmission of Potato Virus Y (PVY)
and Suction Trap catches of three species of cereal aphids: Metopolophium
dirhodum, Sitobion avenae and Rhopalosiphum padi (see Model next slide)
 Field trial and laboratory data support the role of Metopolophium dirhodum
and Sitobion avenae in PVY transmission
 Suction Trap Data can be used to support decisions on aphid management
during the growing season
 Peach-Potato aphids Myzus persicae have not played a major role in virus
transmission in recent years – this may not be the case in England!

SASA © Crown Copyright

The strongest relationship with PVY transmission is
produced using the mean catch of cereal aphids prior
to 29 July
and the incidence of PVY in the previous year

• The incidence of PVY in 2015 was 6.0%

• The incidence of PVY in 2016 is predicted to be 2.4%
SASA © Crown Copyright
 Summary - Part 2
Aphid Monitoring & Virus Transmission - Scotland
 Virus symptoms in crops are the result of transmission in the previous season
in Scotland
 There is a strong relationship between transmission of Potato Leafroll (PLRV)
and Suction Trap catches of Peach-Potato aphids Myzus persicae
 Significant relationships exist between transmission of Potato Virus Y (PVY)
and Suction Trap catches of three species of cereal aphids: Metopolophium
dirhodum, Sitobion avenae and Rhopalosiphum padi
 Field trial and laboratory data support the role of Metopolophium dirhodum
and Sitobion avenae in PVY transmission
 Suction Trap Data can be used to support decisions on aphid management
during the growing season
 Peach-Potato aphids Myzus persicae have not played a major role in virus
transmission in recent years – this may not be the case in England!

SASA © Crown Copyright

 Conclusions:
Implications for the Management of Viruses
 Viruses (PVY) are efficiently transmitted “horizontally” (plant-to-plant) and
“vertically” (tuber progeny)
 Reduce the level of initial inoculum in the crop
o Eliminate overwintering sources of viruses
o Rogue volunteers early in the season
o Planting high quality seed
 Ensure seed crops are free of viruses
 Virus testing of input crop
 Maximise the use of host resistance mechanism:
o Use resistant cultivars (low propensity*)
http://varieties.ahdb.org.uk/ ;
https://www.europotato.org/menu.php?
https://www.sasa.gov.uk/seed-ware-potatoes/virology/varietal-propensity-virus-infection
o Advise early planting to maximise development of Mature Plant Resistance before aphid build up

 A wide range of colonizing & non-colonizing aphid species can transmit PVY
 Reduce virus spread:
o Avoid proximity of ware crops / lower grade seed crops to high grade seed crops
o Eliminate weed reservoirs of aphids & potential PVY hosts
o Control aphid vectors
 Prevent aphid build up in crops & aphid feeding
 Prevent aphid build up when possible in neighbouring crops (ware, cereals, …)
 Liaise with agronomists for best practice (Insecticide / Mineral oil treatments)

 Virus management is required through to burn down of the crop!

SASA © Crown Copyright
 Acknowledgements
 AHDB-Potato Council Project R428
Aphids & virus transmission in seed potato
The James Hutton Institute, Fera, SASA, SRUC
Scottish Agronomy, Rothamsted Research
http://potatoes.ahdb.org.uk/publications/r428-aphids-virus-transmission-seed-crops

 AHDB-Potato Council Project R449 –

Effectiveness of Mineral oils
Scottish Agronomy, NIAB, SASA, SRUC
http://potatoes.ahdb.org.uk/publications/r449-effectiveness-mineral-oils

 Scottish Government, AFRC-RPID Potato Inspectors

SASA Virology & Entomology staff

 Weblinks / contacts:
virology@sasa.gsi.gov.uk
https://www.sasa.gov.uk/
https://www.sasa.gov.uk/diagnostics/virus-testing
https://www.sasa.gov.uk/wildlife-environment/aphid-monitoring/
SASA © Crown Copyright
 Effect of Variety - Propensity
 We are proposing the term ‘varietal propensity’ as a measure of the
extent to which a disease is present in that variety compared with the
norm:
– Propensity = %age of diseased crops of a variety / %age of diseased crops of all
varieties
– e.g. Maris Piper constitutes 8% of Scottish seed crops but is responsible for 36% of
the leafroll seen.
• Propensity of Maris Piper to leafroll is 36/8 = 4.5

 A propensity of 1 is what would be expected if viruses/symptoms were

evenly distributed across all varieties
 Values > 1virus/symptom more likely found in a given variety
 Values < 1virus/symptom less likely found in a given variety

https://www.sasa.gov.uk/seed-ware-potatoes/virology/varietal-propensity-virus-infection
SASA © Crown Copyright
 Summary of Varietal Propensity
(Data for Mosaics from symptom expression at crop inspection)
(Data for viruses are from leaf test diagnosis)

Variety Crops Mosaics PVYN PVYO/C PVA PVV Leafroll

HERMES 1771 0.5 0.1 0.6 1.8 0.0 0.3
MARIS PIPER 1746 1.7 1.7 1.0 0.1 0.0 4.4
DESIREE 1031 2.0 1.1 1.2 5.9 0.0 1.4
MARIS PEER 714 2.2 2.4 2.9 0.3 0.0 0.5
ESTIMA 592 1.1 0.2 0.8 5.4 26.4 1.5
MARKIES 426 0.3 0.1 0.0 1.5 0.0 0.4
KING EDWARD 395 2.3 4.7 3.2 0.2 0.0 1.5
MARFONA 363 0.9 1.2 2.2 0.2 0.0 1.0
PENTLAND DELL 357 0.5 0.9 0.0 0.3 0.0 1.1
CABARET 331 1.1 1.3 1.4 4.9 0.0 0.5
LADY ROSETTA 330 0.2 0.0 0.0 0.0 0.0 0.4
SAXON 323 0.1 0.1 0.0 0.3 0.0 0.2
VALOR 314 3.8 2.7 4.0 0.0 0.0 0.9
ATLANTIC 296 1.9 4.4 4.2 0.3 0.0 0.2
CHARLOTTE 288 1.1 1.7 2.2 0.0 0.0 0.2
CARA 280 0.5 0.5 0.6 0.0 0.0 1.4
WINSTON 274 2.3 0.8 5.7 0.0 0.0 0.8
HARMONY 269 2.3 2.0 0.6 0.0 0.0 1.1

https://www.sasa.gov.uk/seed-ware-potatoes/virology/varietal-propensity-virus-infection

SASA © Crown Copyright

 Infection by test species divided by
infection by the internal control
Vector efficiency

PCL Project – R428

SASA © Crown Copyright
 Aphids - Vector Efficiency Results

Aphid species PVY PVA PVY PVA

Acyrthosiphon pisum 0.7 ? 0.55 0.19
Aphis fabae group 0.1 ? 0.06 0.47
Aulacorthum solani 0.2 No (1933)
Brachycaudus helichrysi 0.21 Yes (1963)
Hyperomyzus lactucae 0.16 ? 0 0
Macrosiphum euphorbiae 0.2 Yes (2002) 0.49 0.94
Metopolophium dirhodum 0.3 ? 0.37 0.02
Myzus ascolonicus 0.2 ?
Myzus persicae 1 Yes (1933, 1996, 2002) 1 1
Rhoplalosiphum padi 0.4 Yes (2002) 0.81 0.02
Sitobion avenae 0.01 ? 0.68 0.63
Brevicoryne brassicae 0.01 ? 0 0
Aphis frangulae Yes (1996)
Aphis nasturtii 0.4 Yes (1996, 2002)
Neomyzus circumflexum Yes (1933)
Cavariella aegopodii 0 ? 0.78 0.55
Drepanosiphum platanoides 0 ? 0 0
Microlophium carnosum 0 ? 0 0
SASA © Crown Copyright
PCL – R428