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Keywords:

  • ELISA;
  • potato cultivar;
  • powdery scab;
  • root galling;
  • Solanum tuberosum;
  • spraing

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Potato mop-top virus (PMTV) causes disease in both the growing plant and tubers (spraing) of potato and is transmitted by the plasmodiophorid Spongospora subterranea, the cause of powdery scab. The effect of temperature during plant growth on the transmission of PMTV from infected seed tubers and from infested growing media was investigated in a series of glasshouse experiments. Symptoms developed on foliage of plants derived from infected seed tubers but none developed when PMTV was transmitted by S. subterranea in soil. The incidence of foliar symptoms was greatest on plants grown at 12°C, less at 16°C, few at 20°C and absent at 24°C. The transmission of PMTV from infected seed tubers was not significantly affected by temperatures between 12 and 24°C, but when the virus was transmitted by S. subterranea, minimal tuber infection occurred at 24°C and no differences were recorded at temperatures between 12 and 20°C. The incidence of powdery scab on tubers was greatest at 12 and 16°C and very low at 20 and 24°C. However, the incidence and severity of root galling caused by S. subterranea, was greatest at 20 and very low at 24°C. The incidence of powdery scab was greater on tubers of plants derived from infected seed tubers grown in a fluctuating temperature regime of 12 h at 20°C followed by 24 h at 12°C than on those grown at a constant 20°C, whereas the incidence of tuber infection by PMTV and spraing was similar for both regimes. This demonstrates that infection of roots can occur at a higher temperature than that for powdery scab on tubers and that this root infection can enable the transmission of PMTV into the potato plant.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Potato mop-top virus (PMTV) was first reported on potato in Scotland by Todd (1965) and, elsewhere in the United Kingdom, by Calvert & Harrison (1966). PMTV typically produces slightly raised lines and rings on the tuber surface and/or brown arcs and lines, commonly described as spraing, in the flesh of tubers of sensitive cultivars (Calvert & Harrison, 1966; Harrison & Jones, 1971a; Kurppa, 1989). Secondary infected plants, i.e. those from infected tubers, may also produce misshapen or cracked tubers (Calvert, 1968), often with reticulate surface cracking, sometimes known as elephant hide blemishing, on the skin (Tenorio et al., 2006). Symptoms on the growing plant vary in severity with cultivar. Foliar symptoms can range from pale yellow or yellow blotches, rings and chevrons on the leaves to a shortening of the internodes resulting in a dwarfed appearance (mop-top). In many cases, only a proportion of the stems may be affected (Calvert, 1968; Torrance et al., 1992). The development of foliar symptoms on plants produced from seed tubers affected by spraing was reported by Calvert & Harrison (1966) to range between 40 and 71%. The incidence of disease therefore reduces during each cycle of propagation (Calvert, 1968: Cooper et al., 1976), but there is minimal experimental evidence on the extent to which PMTV symptom development and transmission is affected by temperature. Harrison & Jones (1971b) reported that the development of PMTV symptoms in tobacco leaves was increased by a decrease in temperature from 22 to 14°C compared with symptom development when either temperature was kept constant. Cooper & Harrison (1973) reported that, at least in Scotland, temperature had no effect on the occurrence of foliar or tuber symptoms of PMTV infection but that their occurrence increased as rainfall increased above 760 mm.

Jones & Harrison (1969) demonstrated that the powdery scab pathogen, the plasmodiophorid Spongospora subterranea, was a vector in the transmission of PMTV, with infection from spore balls containing PMTV producing symptoms in tubers. Arif et al. (1995) demonstrated conclusively that PMTV could be acquired from the roots of infected plants by S. subterranea and then subsequently transmitted to healthy bait plants. Environmental conditions play a key role in the infection of potato plants by S. subterranea and the development of powdery scab would be expected to affect PMTV infection (Merz, 2008). The most favourable conditions for infection by S. subterranea are considered to be a saturated soil between 12 and 15°C at the time of tuber initiation. Consequently, powdery scab is generally most prevalent in countries with cool, wet climates. However, PMTV has been recorded in warmer countries where S. subterranea is present, e.g. Peru (Salazar & Jones, 1975) and Costa Rica (Montero-Astúa et al., 2008), although mostly at cooler, higher altitudes. A number of seed-importing countries with warmer climates, e.g. Bangladesh, Brazil, China, Iran, Saudi Arabia and Thailand now designate PMTV as a quarantine organism and impose a nil tolerance for the virus in imported seed potatoes. Plant health authorities conduct Pest Risk Analysis to evaluate the risk of the disease to potato production in their environment and the effect of temperature on the transmission of PMTV is likely to be an important factor in such an analysis, but evidence on this aspect is scarce.

The objective of this study was to examine the effect of temperature during plant growth on the transmission of PMTV from infected seed tubers and from infested growing media in a series of experiments conducted in glasshouses. The effect on spraing and powdery scab was also recorded.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The experiments were conducted between December and April or September and December, so that the lowest temperatures could be maintained during the experimental period. Separate, adjacent compartments within a glasshouse unit were used to apply the different temperature treatments and were treated as unreplicated main plots in the experimental design. Treatments within each glasshouse were sub-plots. The layout within each glasshouse was a randomized block for each treatment combination. Details of each experiment are presented in Table 1. The temperature in each glasshouse was controlled and monitored electronically (ecotech (UK) Ltd). This software system controls the temperature to within ± 2°C of the set temperature by managing roof and side blinds, fans drawing in outside air and heaters within each unit. An alarm is activated if the temperature limits are exceeded. There were no such events in the course of these experiments. Artificial lighting, ca. 7000–8000 lux at bench height, was provided for 16 h each day. Tubers were planted at a depth of ca. 7 cm in 1·5 L pots laid on benches lined with capillary matting. Growing media were kept constantly wet after plant emergence. In the first soil transmission experiment, soil moisture sensors (SM200) (Delta-T Devices Ltd) were placed in a few pots to enable daily monitoring using a GP1 Data logger (Delta-T Devices Ltd) to assess the effectiveness of the watering regime. This was judged not to be necessary in subsequent experiments. In each experiment, foliage of plants was removed by cutting stems at soil level. The tubers were harvested into new paper bags, stored for a period, washed, visually assessed for powdery scab, tested for PMTV by ELISA and finally tubers were cut and examined for spraing.

Table 1.   Details of experiments to show effect of temperature during plant growth on transmission of Potato mop-top virus (PMTV) from infected potato seed tubers and from infested growing media
 Experiment 1Experiment 2Experiment 3Experiment 4
  1. aDetermined by ELISA.

Growing mediaPMTV-infestedPMTV-infestedJohn Innes compostJohn Innes compost
Seed tuberaPMTV-freePMTV-freePMTV-infectedPMTV-infected
Temperature (°C)12, 19, 2612, 16, 20, 2412, 16, 20, 2420 and 20/12 for 12/12 h
CultivarsCara, Nicola, Saturna, Slaney, RoosterAtlantic, Cara, Saturna, SlaneyCara, Desiree, Estima, Hermes, Maris Piper, Nicola, Saturna, Slaney, Rooster, WinstonCara, Desiree, Estima, Maris Piper, Nicola, Saturna, Slaney
Replications5487
Date of planting7 Feb, 200714 Jan, 200819 Dec, 200729 Aug, 2008
Date of harvest22 Mar, 200721 Apr -1 May, 20084-14 Apr, 20083 Dec, 2008

Soil transmission experiments

Two experiments were conducted by planting PMTV-free seed tubers in PMTV-infested growing media. Each year, PMTV-free tubers of a range of cultivars were obtained by testing seed tubers produced at SASA’s Gogarbank Farm, Midlothian for PMTV by ELISA. Soil known to be infested by PMTV was collected from a field in Perthshire, Scotland. Diluted soils were prepared in a cement mixer to produce a homogeneous mixture. In both experiments, plants were inspected regularly for foliar symptoms of infection by PMTV.

Experiment 1

The field soil was diluted, 1:1 v/v, with John Innes compost No 2. Pots were filled with either the mixture of field soil and compost or compost alone. Three leaves from each plant were sampled on 23 March and tested for PMTV. After harvest, daughter tubers from each pot were held in a refrigerated store at ca. 5°C for 2 weeks, after which they were held at 16°C for 2 weeks, followed by 1 week at ca. 5°C in order to induce the development of spraing (Harrison & Jones, 1971a).

Experiment 2

Scrapings of scab lesions were taken from tubers of cv. Estima affected by powdery scab which had been produced in a field known to be infested with PMTV. Samples of infested field soil and ground peelings were tested for PMTV using a tomato bioassay and real-time PCR assay (Davey, 2009). Four growing media were tested: John Innes compost No 2 (JI2), JI2 to which 0·3 g of ground scab peelings were added, JI2 mixed with infested soil in proportion of 9:1 v/v (i.e. 10% infested soil) and JI2 mixed with infested soil in proportion of 1:1 v/v (50% infested soil). Tubers were harvested while carefully retaining the root mass, which was washed under running tap water and scored for the incidence and severity of root galls. Tubers were stored at 16°C until 19 May when they were moved to a cold store at ca. 5°C for further storage of at least 2 weeks prior to testing and assessment.

Seed transmission experiments

Experiment 3

Seed tubers of 10 cultivars were obtained from a field experiment in 2007 at a site known to be infested with PMTV. Two PMTV-free tubers of each cultivar were also planted in each glasshouse to provide healthy reference plants. All glasshouses were maintained at 18°C until 3 January when the temperatures of 12, 16, 20 and 24°C were applied. Plants were inspected on 31 January, 12 February and 26 February for symptoms of PMTV infection. At the time of harvest, three leaflets from each plant were sampled and tested for PMTV by ELISA. All tubers were held at 16°C in the glasshouse until 29 April when they were placed in a cold store at ca. 5°C for a further 2 weeks’ incubation before testing.

Experiment 4

The two temperature treatments were a constant 20°C and a fluctuating regime of 20°C for 12 h during the day time and 12°C for 12 h during the night. Plants were inspected weekly for symptoms characteristic of PMTV infection in the period just before flowering to the end of flowering. Daughter tubers were held in a cold store at ca. 5°C for at least 2 weeks, then held at 16°C for a further 2 weeks before being returned to the cold store for another 2 weeks’ storage.

Disease testing and assessment

Tuber testing for PMTV and spraing assessment

Cores, 25–30 mm in length and 5 mm in diameter, were taken from the rose- and heel-end of each tuber and were tested for PMTV by DAS-ELISA (Fox et al., 2005). Tubers were then cut lengthwise to expose six surfaces and the most severely affected surface was scored for severity of spraing using four categories: nil, slight, moderate and severe (Anon, 1976).

Powdery scab assessment

Roots were washed and assessed visually for the severity of root galling in 5 categories: 0 = nil; 1 = one or two galls; 2 = several galls, mostly small, <2 mm; 3 = many galls, some >2 mm and 4 = most major roots with galls, some >4 mm (see http://www.spongospora.ethz.ch/LaFretaz/scoringtablegalls.htm). The percentage tuber surface area covered by powdery scab was recorded using seven categories (Anon, 2002) whose mid-point values were 0, 1·0, 3·6, 7·6, 18, 37·6 and 75. A severity index was then calculated by multiplying each mid point value by the number of tubers in that category, summing and dividing the total by the total number of tubers examined.

PMTV in soil or scab peelings

A tomato bait plant and real time PCR assay was used to detect PMTV in soil and scrapings of scab lesions (Davey, 2009). Three replicates of 20 g of test soil or 0·3 g of scab scrapings added to compost were tested for each sample.

Statistical analysis

The unreplicated temperature treatments were confounded with glasshouse so their effects were examined by chi-squared (χ2) analysis of total frequencies of disease or infection. Analysis of the effects of other treatments, e.g. cultivar, was conducted using a binomial generalized linear mixed model (Jiang, 2007) with logit or angular transformation, as appropriate. Treatments in which the frequency of disease or infection was zero or close to zero were excluded from this further analysis, e.g. compost alone (Experiment 1) and 24°C in Experiment 2. Results of these analyses are presented as LSDs for means of cultivars and growing media. On occasions with some of the powdery scab severity data, a comparison between two temperature treatments was made using Student’s t-test for paired samples of treatments within main plots.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Soil transmission experiments

PMTV was not detected by ELISA in the foliage of any plants in the experiment in 2007 and no foliar symptoms of PMTV infection were observed on any plants in either experiment.

Experiment 1

In 2007, none of the daughter tubers produced by plants grown at 26°C were infected by PMTV, nor were they affected by spraing or powdery scab (Table 2). For plants grown in compost at 12 or 19°C, the incidence of PMTV and powdery scab was very low, with only two out of 25 plants at either temperature having any tubers infected by PMTV. All of the plants grown in the infested soil mixture at 12 and 19°C had some tubers infected by PMTV and the incidence of tuber infection at these two temperatures did not differ significantly. However, none of the tubers produced at 19°C developed spraing while 17% of those produced at 12°C were affected With powdery scab, although all plants grown in infested soil had some affected tubers at 12°C, only 11 out of 25 plants grown at 19°C had affected tubers. The incidence of powdery scab was four times greater on tubers produced at 12°C than at 19°C (Table 2).

Table 2.   Effect of temperature on the transmission of Potato mop-top virus (PMTV) and powdery scab on daughter potato tubers derived from PMTV-free seed planted in infested soil mixture (Experiment 1). Data are means of five cultivars
Growing mediumaTemperature 
12°C19°C26°C
  1. aSoil was a mixture of a naturally PMTV-infested soil diluted 1:1 with John Innes compost.

  2. bNS = Not significant.

  3. ***P < 0·001.

Number of tubers assessed
 Compost146146106 
 PMTV-infested soil26015569 
% tubers affected by powdery scab
 Compost1·42·10 
 PMTV-infested soil48·610·80χ2(1) = 54·0 *** (12 and 19°C only)
% tubers infected by PMTV
 Compost1·77·60 
 PMTV-infested soil73·967·60χ2(1) = 3·3 NSb (12 and 19°C only)
% tubers affected by spraing
 Compost2·100 
 PMTV-infested soil17·300 

With plants grown in the infested soil mixture, the incidence of tuber infection by PMTV did not differ significantly amongst the cultivars at either 12 or 19°C, but the incidence of spraing on tubers grown at 12°C was greatest for cvs Nicola and Cara and least for cvs Rooster and Saturna (Table 3). At 12°C, more tubers of cv. Saturna were affected by powdery scab than those of the other four cultivars but, at 19°C, no differences in the incidence of powdery scab were detected amongst the cultivars, although powdery scab was again most prevalent on tubers of cv. Saturna.

Table 3.   Reaction of five potato cultivars planted in an infested soil mixture to Potato mop-top virus (PMTV), spraing and powdery scab (Experiment 1, 12 or 19°C)
 % tubers
Powdery scabPMTVSprainga
  1. aNo spraing developed at 19°C.

  2. bNS = Not significant.

Cultivar12°C19°C12 °C19°C12°C
Cara37·213·850·975·731·8
Nicola37·9868·954·135·2
Saturna69·028·766·062·34·1
Slaney36·99·360·751·522·5
Rooster43·95·362·261·411·0
Significance level< 0·001NSbNSNS< 0·01
LSDP = 0·5, 16 d..f .12·1121·1318·4817·0815·78
Experiment 2

In 2008, PMTV was detected in all three replicate samples of the field soil and scab scrapings but was not detected in unamended compost. Temperature significantly affected the incidence of tuber infection by PMTV, spraing, root galls and powdery scab (Table 4). The incidence of PMTV in tubers was similar for plants grown at 12, 16 and 20°C (mean 69%) but considerably less (9%) for those grown at 24°C. Spraing was not observed in tubers produced at 24°C. At the other temperatures, the incidence of spraing was greatest in tubers produced at 16°C and similar for those produced at 12 and 20°C. The incidence of plants with root galls was low at 24°C and was considerably less than at the other three temperatures. Root galling, both incidence and severity, was greatest on plants grown at 20°C and was similar at the two lowest temperatures. However, the incidence of powdery scab was considerably greater on tubers produced at 12 and 16°C than on those produced at 20 and 24°C. The severity of powdery scab was also greater on tubers grown at 12°C than on those grown at 16°C. At the two highest temperatures, few tubers were affected by powdery scab and the disease consisted mainly of one or two lesions on a tuber.

Table 4.   Effect of temperature on root galling, powdery scab, infection by Potato mop-top virus (PMTV) and spraing on potato plants and daughter tubers (Experiment 2). Data are means for four cultivars and four growing media
 Temperature (°C) 
  1. aNA indicates that values were zero or close and not appropriate for t-test.

  2. **P < 0·01, ***P < 0·001.

Measure12162024χ2 or t value
Number of plants64636364 
% plants with root galls75·079·490·57·8χ2(3) = 115 ***
Severity of root galling1·31·52·00 
Number of tubers assessed488415278233 
% tubers infected by PMTV72·769·265·19·0χ2(3) = 1405 ***
% tubers affected by spraing5·513·25·80χ2(2) = 207 ***
% tubers affected by powdery scab38·335·99·00·4χ2(2) = 80·2 ***
% surface area affected by powdery scab1·70·9NAaNAt(15) = 3·01 **

Differences amongst the growing media were found for tuber infection by PMTV, spraing, root galls and powdery scab (Table 5). Although PMTV was detected in tubers produced in unamended compost, the incidence of PMTV in these tubers was considerably less than for the two infested soil mixtures and the scab-amended compost which each produced tubers with similar amounts of infection. However, at 12 and 16°C, the incidence of spraing was not related to the amount of tuber infection, being greatest in tubers produced in compost to which scab scrapings had been added and generally similar for the other growing media. The incidence and severity of root galling and powdery scab was greater on plants and tubers produced in unamended and scab-amended compost than for those produced in compost amended with infested soil at either dilution rate.

Table 5.   Effect of growing media on root galling, powdery scab, infection by Potato mop-top virus (PMTV) and spraing on potato plants and daughter tubers (Experiment 2). Data are means of four cultivars and temperatures
MeasureGrowing mediumχ2 or LSDP = 0·05, 88 d.f.
Compost10% infested soil50% infested soilCompost and scab peelings
  1. a12, 16 and 20°C temperatures only.

  2. bPercentages are back transformed means.

  3. cFigures in parenthesis are logit transformed values.

  4. d12 and 16°C temperatures only.

  5. ***P < 0·001

Number of plants62646464 
% plants with root gallinga89·679·270·293·6χ2(3) = 18·2 ***
Severity of root gallinga1·81·41·12·10·30 ***
%b tubers infected by PMTVa12·7 (−1·9)c87·2 (1·9)87·3 (1·9)86·8 (1·9)− (0·69) ***
Number of tubers assessed265242167253 
% tubers affected by spraingd4·26·21·813·8χ2(3) = 29·2 ***
%b tubers affected by powdery scabd49·5 (−0)c15·6 (−1·7)14·7 (−1·8)53·7 (0·2)− (0·72) ***
% (angular transformation) surface area affected by powdery scabd7·82·22·36·80·88 ***

Differences amongst the cultivars were detected for spraing and root galling but not for infection by PMTV or powdery scab (Table 6). The incidence of tuber infection by PMTV was greater than 50% for all cultivars, with the highest incidence occurring with cv. Cara and the lowest with cv. Slaney. The incidence of spraing was ca. 14% in tubers of cvs Slaney and Cara. No spraing was found in tubers of cv. Atlantic and only a trace in those of cv. Saturna. The incidence and severity of root galls was greatest on plants of cv. Slaney and least on those of cv. Saturna. Root galling on plants of cvs Atlantic and Cara was intermediate to that of the other two cultivars.

Table 6.   Reaction of four potato cultivars to root galling, powdery scab, infection by Potato mop-top virus (PMTV) and spraing (Experiment 2). Data are the means for four growing media and temperatures
MeasureCultivarχ2 or LSDP < 0·05,88 d.f.
AtlanticCaraSaturnaSlaney
  1. a12, 16 and 20°C temperatures only.

  2. bPercentages are back transformed means.

  3. cFigures in parenthesis are logit transformed values.

  4. d12 and 16°C temperatures only.

  5. eNS = Not significant.

  6. ***< 0·001.

Number of plants assessed64636364 
% plants with root gallsa83·389·654·297·8χ2(3) = 33·7 ***
Severity of root gallinga1·41·80·82·40·30 ***
%b tubers infected by PMTV72·5 (1·0)c85·0 (1·7)70·4 (0·9)55·8 (0·2)− (0·68) NSe
% tubers affected by spraing014·20·413·7-
%b tubers affected by powdery scabd33·4 (−0·7)c38·6 (−0·5)22·2 (−1·2)28·7 (−0·9)− (0·73) NS
% (angular transformation) surface area affected by powdery scab d4·45·64·34·90·88 NS

Seed transmission experiments

Experiment 3

On plants produced by infected seed tubers, temperature significantly affected the development of symptoms on foliage, incidence of plants in which PMTV was detected by ELISA, and the incidence and severity of powdery scab (Table 7). The incidence and severity of spraing was very low and erratically distributed amongst replications and did not appear to be affected by temperature. The incidence of plants with foliar symptoms declined with each 4°C increase in temperature, with plants showing symptoms being scarce at 20°C and absent at 24°C. However, the incidence of plants in which PMTV was detected was slightly greater at 20°C than at 12 and 16°C, but very low at 24°C. Tuber infection by PMTV was slightly greater at 20°C than at the other three temperatures. No tubers on plants grown at 24°C were affected by powdery scab and only a few (2%) produced at 20°C were affected. The mean incidence and severity of powdery scab was greater on tubers produced at 12°C than on those produced at 16°C.

Table 7.   Effect of temperature on Potato mop-top virus (PMTV) transmission from infected potato seed tuber, symptom development and powdery scab (Experiment 3)
MeasureTemperature (°C) 
12162024
  1. aNA indicates that values were zero or close and not appropriate for t-test.

  2. *P < 0·05, **P < 0·01, ***P < 0·001.

Number of plants assessed80797979 
% plants with foliar symptoms25·013·92·50χ2(2) = 13·6 **
% plants PMTV detected in leaves16·518·822·53·8χ2(3) = 11·6 **
Number of tubers assessed618533388215 
% tubers infected by PMTV26·525·032·022·8χ2(3) = 7·9 *
% tubers affected by spraing0·61·92·10·5 
% tubers affected by powdery scab33·428·02·00χ2(2) = 106·3 ***
% (angular transformation) surface area affected by powdery scab8·24·4NAaNAt(9) = 4·67**

Symptoms on affected plants were generally mild, apart from two plants of cv. Desiree which developed mop-top symptoms. Most affected plants had one stem reduced in height, accompanied by leaflet distortion and mottling, e.g. cv. Cara. Leaflets on a considerable proportion (69%) of plants of cv. Saturna were mottled and slightly distorted; however, as those symptoms also occurred on the reference plants, these plants were not recorded as affected by PMTV. The incidence of plants showing symptoms was greatest for cvs Cara and Desiree (Table 8). Few or no plants of cvs Estima, Hermes, Maris Piper, Nicola, Rooster and Saturna developed symptoms. While the development of plants showing symptoms from infected seed tubers varied considerably amongst cultivars, differences amongst the cultivars in the percentage of plants in which PMTV was detected were much less. However, the mean incidence of tubers infected by PMTV was significantly correlated (r = 0·91, 8 d.f.) with the mean incidence of plants in which PMTV was detected but not with that of plants showing symptoms. The incidence and severity of powdery scab varied significantly amongst the cultivars and the two measures were closely correlated (r = 0·93, 8 d.f.). Estima was the most susceptible cultivar and cv. Winston was the most resistant.

Table 8.   Reaction of potato cultivars to infection by Potato mop-top virus (PMTV) from infected potato seed tuber and powdery scab (Experiment 3). Data are means of four temperatures unless otherwise stated
Cultivar% plants with PMTV foliar symptoms (12 & 16°C)% plants PMTV detected (12, 16 & 20°C)%a tubers infected by PMTV%a tubers affected by powdery scab (12 & 16°C)% (angular transformation) surface area covered by powdery scab(12 & 16°C)
  1. aPercentages are back transformed means.

  2. bFigures in parentheses are logit transformed values.

Cara43·820·831·8 (−0·76)b28·2 (−0·94)b4·6
Desiree26·730·433·5 (−0·69)15·2 (−1·72)3·0
Estima037·535·8 (−0·59)50·1 (0·01)10·6
Hermes0011·5 (−2·04)18·1 (−1·51)4·1
Maris Piper6·312·513·3 (−1·87)44·3 (−0·23)7·9
Nicola6·320·821·6 (−1·29)19·6 (−1·41)4·1
Rooster6·313·017·5 (−1·55)43·3 (−0·27)6·5
Saturna016·724·7 (−1·12)41·2 (−0·35)9·4
Slaney18·833·332·9 (−0·72)44·0 (−0·24)6·9
Winston18·825·024·8 (−1·11)9·5 (−2·26)1·7
χ2 P valueP < 0·001P < 0·061   
LSDP = 0·05, 125 d.f.  (0·83)(0·92)3·62
Experiment 4

In this experiment, five tubers did not produce plants. No symptoms developed on plants grown at a constant 20°C but five plants grown in the fluctuating regime developed foliar symptoms characteristic of PMTV infection. The incidence of detection of PMTV in leaflet tests was 26% for constant 20°C regime and 40% for fluctuating regime. However, the incidence of tubers infected by PMTV or affected by spraing did not differ significantly between the two regimes, but more tubers produced in the fluctuating regime were affected by powdery scab than those produced at a constant 20°C (Table 9). The incidence of spraing was very low; overall only 5% of PMTV-infected tubers developed spraing.

Table 9.   Effect of fluctuating temperature on Potato mop-top virus (PMTV) transmission from infected potato seed tuber, spraing and powdery scab (Experiment 4)
MeasureTemperature (°C)statistic
2020/12a
  1. aRegime of 20°C for 12 h and 12°C for 12 h.

  2. bNS = Not significant.

  3. *< 0·05, **< 0·01, ***< 0·001.

Number of tubers assessed267406 
% tubers infected by PMTV43·450·5χ2(1) = 3·6 NSb
% tubers affected by spraing2·22·5χ2(1) = 0·3 NS
% tubers affected by powdery scab1·510·4χ2(1) = 19·9 ***

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Spongospora subterranea is the only known vector of PMTV, so the infection of PMTV-free plants by the virus is inextricably linked to factors affecting the infection of plants by this organism. In all the experiments, the severity of powdery scab was greatest on tubers produced at 12°C and only slightly less at 16°C. However, between 19 and 26°C, the development of powdery scab on daughter tubers was absent or minimal. This is in agreement with the optimum of 12–15°C for powdery scab (Merz, 2008) although the difference between 12 and 16°C treatments in the present experiment was much less than that recorded by van de Graaf et al. (2005) for 12 and 17°C treatments. Van de Graaf et al. (2007) also demonstrated that temperature affected root galling which had a greater optimum, around 19°C, than that for powdery scab. In Experiment 2 with diluted naturally-infested soil or compost amended with scab scrapings, root galls developed on only a low proportion of plants grown at 24°C (7·8%), but were considerably more prevalent and severe on plants grown at temperatures between 12 and 20°C, with the greatest development occurring at 20°C. The data indicates that S. subterranea can infect either roots, expressed as root galls, or tubers, expressed as powdery scab, when plants are grown at temperatures between 12 and 20°C. Consequently, either pathway of infection can enable PMTV to be transmitted from infested soil to PMTV-free plants and tubers grown at these temperatures, as demonstrated in the experiments with infested growing media. This may partly explain why PMTV has often been found in crops largely unaffected by powdery scab (Jones, 1988; Davey et al., 2008) and not in direct association with powdery scab lesions on tubers (Jones & Harrison, 1969). Extrapolating the effect of constant temperatures to the field, where temperatures will fluctuate, is more problematic. In the field, soil temperature will fluctuate throughout the growing season and, to a lesser extent, during day and night, and with soil depth. Fluctuations within the range 12 to 20°C are unlikely to affect the transmission of PMTV by S. subterranea although they could affect the development of powdery scab. The critical time when soil temperature fluctuations from above 20°C to below 20°C may affect PMTV transmission by S. subterranea will be the stage of growth when plants are susceptible to infection. With powdery scab, this has been demonstrated to be during tuber initiation (Merz, 2008), and Kirk (2008) concluded that this would also be applicable for PMTV. Sandgren (1995) found that inoculating plants at flower bud and flowering stages of growth gave more spraing than inoculation before or after these periods.

In both experiments, infection by PMTV and powdery scab occurred on plants grown in unamended compost although both were less prevalent in Experiment 1 than 2. Although the tubers were confirmed free of PMTV by testing and tubers with obvious scab lesions were not selected, it is possible that powdery scab lesions or sporeballs could have been present which would account for powdery scab. With PMTV, cross contamination in the glasshouse is possible because matting was kept very wet and may have enabled transfer of the virus. In addition, unfortunately the seed tubers in Experiment 2 were exposed to dry dust from the infested soil prior to planting and, although the tubers were lightly rinsed to try to remove it, this seems not to have been successful and probably accounts for the difference between the two experiments.

Jones & Harrison (1969) reported the development of foliar symptoms on two out of nine plantlets of cv. Arran Pilot grown from rooted sprouts which had been inoculated with viruliferous sporeballs. In the present experiments, foliar symptoms developed only when infection was derived from the seed tuber and not from S. subterranea. This difference may be related to the type of plant which was exposed to infection in these studies, as the plantlets produced by Jones & Harrison (1969) may have been physiologically younger, and hence more susceptible, than plants produced by seed tubers and thus not typical of what occurs in the field. The development of foliar symptoms was also most prevalent at cooler temperatures and this probably explains why foliar symptoms are more common in Scotland than Denmark (Kirk, 2008)

The transmission of PMTV from infected seed tubers to daughter tubers was only slightly less at 24°C than at 12 or 16°C, indicating that the transmission of PMTV from infected seed can occur at higher temperatures than the transmission from infested soil. Similarly, allowing the growing temperature to decrease from 20 to 12°C at night had no effect on PMTV transmission from infected seed tubers, confirming that PMTV movement in the plant is not sensitive to temperature within this range. By contrast, the development of powdery scab on daughter tubers was affected by such a temperature fluctuation. The weak transmission of PMTV within the plant was confirmed by the overall mean reduction in tuber infection from seed to daughter tuber of 58% for all temperatures in both experiments. This means that the amount of virus in daughter tubers is generally much less when infection is derived solely from infected seed than from infested soil. In 2008 using the same glasshouses at the same time, the incidence of infection by PMTV of daughter tubers produced at 12, 16 and 20°C was much greater for those produced in infested soil (mean = 69%) compared with those produced from infected seed tubers (mean = 28%). The proportion of infected tubers which developed spraing was also slightly greater for those produced in infested soil (mean = 11·9%) compared with those from infected seed (mean = 7·4%). However, with daughter tubers produced at 24°C the opposite occurred, with more tuber infection by PMTV on plants produced from infected seed than on those grown in infested soil, but the risk of spraing developing in infected daughter tubers produced at this temperature was very low, irrespective of the origin of the infection. This may explain the rarity with which spraing has been found in PMTV-infected tubers produced in countries with higher temperatures than northern Europe. For example, Montero-Astúa et al. (2008) did not observe spraing in tubers produced in Costa Rica. Salazar & Jones (1975) recorded spraing in a tuber of cv. Mariva grown in the Peruvian Andes but did not report on its prevalence. By contrast, Tenorio et al. (2006) did not find spraing in tubers of 26 potato cultivars grown in PMTV-infested land in the Peruvian Andes. The results presented here suggest that planting PMTV-infected seed in countries with climates considerably warmer than Scotland will carry a very small risk of PMTV transmission occurring at a rate sufficient to cause an economic outbreak of the disease. Furthermore, the risk of powdery scab developing at higher temperatures has been shown to be very low; consequently, the risk of PMTV-infested sporeballs being deposited in soils must also be very low. Overall, the results suggest the risk of PMTV posing a threat to potato production in countries where growing temperatures are greater than 20°C could be slight, depending on time of year when cropping, altitude and irrigation.

Cultivar reactions showed some variability amongst the experiments and with published data. Spraing in cv. Saturna was reported by Kirk (2008) to have caused serious problems in potato production in Sweden, but overall in the present experiments, cv. Saturna did not appear to be particularly sensitive. Mølgaard & Nielsen (1996) and Sokmen et al. (1998) also found cv. Saturna to be less sensitive in some comparative trials than suggested by anecdotal evidence. The incidence and severity of root galls on plants was least for cv. Saturna and greatest for cv. Slaney, but the incidence of tuber infection by PMTV on a cultivar did not appear to be associated with the amount of root galling. However, root galling may only be partially indicative of the amount of root infection by S. subterranea and other factors may influence the passage of PMTV from roots to the rest of the plant.

Spraing, particularly internal symptoms, normally develop slowly during storage, although surface rings may be present at harvest on tubers at or near the surface of the drill, probably induced by the daily fluctuations in day and night temperatures at the soil surface (Harrison & Jones, 1971a). Spraing can be induced to develop more quickly by subjecting the tubers to temperature fluctuations during storage. Harrison & Jones (1971a) indicated that these fluctuations should include an increase in temperature from 13°C or less to about 18°C for a period, followed by a decrease to 13°C or below. Mølgaard & Nielsen (1996) applied such temperature fluctuations for one week periods, although others (Cooper et al., 1976; Tenorio et al., 2006) used 2 week periods. In the present experiments, a spraing inducement treatment of 2 weeks at 16–18°C and 2 weeks at 5°C was applied to the tubers before conducting the assessment, but the proportion of infected tubers which developed spraing appeared to differ amongst the experiments. For the cvs Cara, Saturna and Slaney, the mean percentage of infected tubers which developed spraing was 11·9 for the infested soil treatments in 2008, 7·4 for the first infected seed experiment and 5·0 for the second infected seed experiment in 2008 whereas, in the infested soil experiment in 2007, the proportion was 25·7%. This difference may have been due to the timing of the spraing inducement treatment relative to harvest. In the 2008 spring experiments, the treatment was applied immediately after harvest without a drop in temperature below 13°C to give the increase suggested by Harrison & Jones (1971a) at the start of the inducement treatment. In the 2007 infested soil experiment and autumn 2008 seed experiment, the harvested tubers were stored for 2 weeks at 5°C before applying the inducement treatment, but only in the 2007 experiment was the proportion of infected tubers which developed spraing greater than when there was no cold storage. In the spring 2008 experiments, the conditions advocated by Harrison & Jones (1971a) would only have been fulfilled for the tubers produced at 12°C. Nevertheless, more spraing developed in tubers produced at 16°C than in those produced at 12°C, providing further evidence of the variability in the effects of such inducement treatments (Harrison & Jones, 1971a; Mølgaard & Nielsen, 1996). For example, Mølgaard & Nielsen (1996) found more spraing with storage at 4°C than with a fluctuating temperature treatment. Despite these efforts to maximise spraing production, the overall proportion of PMTV infected tubers which developed spraing was never greater than 25%, suggesting that a considerable proportion of a crop has to be infected before the disease is likely to have an economic impact.

Growing plants in compost to which PMTV-infested scab peelings were added resulted in as much infection of tubers by PMTV as growing plants in compost diluted with infested soil. The amount of spraing which developed on the tubers was also greater for the amended soil than for diluted soils. However, the amount of spraing which developed on tubers grown in 50% infested soil was much less than that in 10% infested soil, even though the incidence of PMTV tuber infection was the same and the same spraing inducement treatment was applied for both treatments. Additional work may therefore be needed to establish the growing and storage conditions which maximise spraing development. Potentially, using compost amended with viruliferous scab peeling could provide a means of assessing cultivar susceptibility to PMTV infection and sensitivity to spraing.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank Mr A. Fox and Mr R. Holmes of Virology and Zoology Section, SASA for conducting the ELISA tests, Mr Adrian Roberts, Biomathematics and Statistics for Scotland for conducting some of the analysis and advice and the financial contribution of the Potato Council Ltd for Triona Davey.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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