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Keywords:

  • Fusarium sambucinum;
  • Fusarium sulphureum;
  • postharvest disease;
  • Solanum tuberosum;
  • storage disease;
  • wheat scab

Abstract

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

A 2004–2005 survey of potatoes from stores in the north-central potato-producing region of the USA showed that the predominant causes of dry rot were Fusarium graminearum and Fusarium sambucinum. Isolates of F. graminearum originally isolated from potato tubers with dry rot (n = 15), wheat kernels with scab (n = 15), and sugarbeet tap roots with decay (n = 5) were tested for aggressiveness to potato tubers. There were no significant differences in aggressiveness among isolates of F. graminearum, regardless of original host, as measured by their ability to cause dry rot. These findings may have implications for survival of F. graminearum inoculum since potatoes, wheat and sugarbeets are frequently used in crop rotation in the region. Fusarium graminearum required larger wounds for infection of potato tubers than F. sambucinum. Plug-removal injury, simulating a stolon-removal injury, resulted in equal incidence of dry rot caused by the two Fusarium species, whereas abrasion and bruising injury were sufficient for infection and dry rot development by F. sambucinum, but not F. graminearum. A change in harvest practices from vine-killing prior to harvest to mechanical vine-killing on the day of harvest may be a factor affecting the onset of dry rot caused by F. graminearum, since this process often causes large wounds at the stem end of the tubers when the stolon is forcibly removed.


Introduction

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

Fusarium species are among the most globally important plant pathogens because a plethora of hosts are affected by one or more species of this fungal genus. Diseases caused by Fusarium are important in virtually every crop grown (Nelson et al., 1983). Fusarium species cause many diseases of potatoes in the field and after harvest, including wilt, vascular discoloration, seed decay, and dry rot of stored potatoes (Secor & Gudmestad, 1999; Secor & Salas, 2001). Several species of Fusarium can cause postharvest dry rot of potatoes. The most frequent causes of potato dry rot in both the USA (Secor & Salas, 2001) and Great Britain (Peters et al., 2008a) are Fusarium coeruleum and Fusarium sambucinum. Other species of Fusarium reported to cause dry rot of potatoes include F. avenaceum and F. culmorum (Secor & Salas, 2001; Peters et al., 2008a; b). A recent study showed that these four species are responsible for almost 95% of the dry rot found in Great Britain (Peters et al., 2008a).

Fusarium is both seed- and soilborne. Infection of tubers occurs through wounds produced during harvest operations, and dry rot develops slowly in storage. Temperatures >10°C favour Fusarium growth, whilst temperatures <5°C inhibit fungal growth (Secor & Salas, 2001). The primary sources of inoculum are contaminated or infected seed tubers and infested soil (Secor & Gudmestad, 1999). Dry rot causes a dry and crumbly decay with abundant white, yellow or carmine-coloured mycelium depending on the species of Fusarium (Secor & Salas, 2001).

Management of dry rot begins by avoiding harvest wounds and bruises that act as infection sites for Fusarium. Storage conditions that promote suberization and wound healing of harvested tubers limit the size of dry rot lesions by preventing fungal growth into healthy tuber tissues. Seed treatment compounds applied as liquids or dusts are useful in reducing seedborne inoculum spread during the cutting and planting operations (Secor & Johnson, 2008). Postharvest application of thiabendazole (TBZ) was an effective treatment for control of potato dry rot until widespread resistance to this fungicide developed in F. sambucinum (Hide et al., 1992; Desjardins et al., 1993; Kawchuck et al., 1994; Hanson et al., 1996). Resistance to TBZ not only results in reduced control, but may also result in increased incidence and severity of dry rot (Secor et al., 1995). In Europe, dry rot is controlled by postharvest applications of TBZ and imazalil (Hide & Cayley, 1985; Carnegie et al., 1990). Commercially acceptable cultivars with resistance to fusarium dry rot are not widely grown.

Fusarium graminearum is best known as a pathogen causing head blight (scab) on wheat and barley, and ear rot in corn, but in recent years, has been implicated as the cause of other plant diseases in North America, including a dry decay of sugarbeet tap roots (Estrada et al., 2007), sugarbeet yellows (Hanson, 2006), soyabean root and seedling rot (Martinelli et al., 2004; Broders et al., 2007) in the USA, and pea root rot in Canada (Feng et al., 2010). Fusarium graminearum has also been isolated along with other Fusarium spp. from tuber dry rot lesions in Europe (Seppanen, 1980; Tivoli & Jouan, 1980; Bang, 1989), and isolates of F. graminearum were reported to cause dry rot when inoculated on potato tubers in Chile (Acuña et al., 2004), Tunisia (Daami-Remadi et al., 2006) and Canada (Peters et al., 2008b). These observations of additional hosts of F. graminearum have epidemiological implications since cereals, potatoes, sugarbeet and soyabeans, for example, are frequently grown in close rotation. Inoculum buildup in successive susceptible crops could lead to more disease since Fusarium propagules can survive long periods in the soil (Khonga & Sutton, 1988; Gilbert & Fernando, 2004). Fusarium graminearum is a notorious producer of mycotoxins, which are commonly found associated with infected grain (McMullen et al., 1997; Bai & Shaner, 2004; Burlakoti et al., 2007) and sugarbeets (Bosch & Mirocha, 1992). Production of mycotoxins in potatoes as a result of infection by F. graminearum is not known, but isolates of this fungus recovered from both potato and sugar beet were shown to produce mycotoxins in inoculated wheat heads (Burlakoti et al., 2007).

An outbreak of dry rot in stored potato tubers destined for French-fry processing has been observed in the north-central potato-producing region of the USA in recent years. This epidemic has been widespread in commercial stores throughout the growing area and has caused substantial economic losses of potatoes (unpublished). The outbreak was present in areas known for fusarium head blight of wheat and seemed to follow several years in which there had been an unusually high incidence of fusarium head blight (McMullen et al., 1997; Nganje et al., 2002). All potatoes affected were produced under irrigation and the dry rot was concomitant with the elimination of vine (haulm) desiccation in advance of harvest in order to maximize yields. The cause of this dry rot outbreak was identified as F. graminearum (Ali et al., 2005). Because this was the first reported case of dry rot in the USA caused by F. graminearum, it is of interest to study some of the factors that may be involved in the development of this disease. The objectives of the present study were (i) to determine the importance of F. graminearum as the cause of dry rot in commercial stores reporting a high incidence of the disease, (ii) to examine the aggressiveness of F. graminearum isolated from naturally infected potatoes, sugarbeet and wheat for the ability to cause dry of stored potato tubers, and (iii) investigate potential factors that may explain the increased incidence of F. graminearum as a potato dry rot pathogen.

Materials and methods

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

Sources and sampling of F. graminearum isolates

Isolates from stored potatoes

Potato tubers with putative dry rot were collected from six potato stores reporting significant problems with dry rot in 2004–2005 and returned to the laboratory for processing. The stores represented the three major irrigated potato-production areas of the region: central North Dakota, northeast North Dakota and central Minnesota. The sample represented potatoes harvested from 51 different production fields from this area. All lots sampled were cv. Russet Burbank, except for one cv. Shepody lot. Table 1 summarizes the collection data of F. graminearum and F. sambucinum from potato stores. All stores sampled came from fields that were harvested without desiccation and stored at 10°C. Tubers were sampled by company agriculturists or university staff, and were selected based on visual external tuber symptoms resembling dry rot. Potato tubers were washed with tap water to remove soil and reduce contaminants prior to isolations being performed. Two small pieces (approximately 5 mm) were removed from the margin of the infected tissue of the tuber and placed on half-strength potato dextrose agar acidified with 0·05% lactic acid (APDA) and maintained under continuous light at room temperature to promote growth of Fusarium. Subsequent growth was visually screened for the presence of Fusarium macroconidia and cultures were saved for further manipulation. Only cultures identified as F. graminearum or F. sambucinum were saved and reported; other Fusarium spp. were neither identified nor saved for this study, since the purpose was to identify the primary cause(s) of the dry rot, not to conduct a comprehensive survey of all causes of dry rot.

Table 1.   Summary of collection and isolate recovery data of Fusarium graminearum and Fusarium sambucinum collected from potato stores in North Dakota (ND) and Minnesota (MN) in 2004–2005 used in this study
LocationNo. of storesNo. of fieldsNo. of tubers collectedNo. of tubers with dry rotNo. of tubers with Fusarium graminearumNo. of tubers with Fusarium sambucinum
Central ND1133251663627
Northeast ND1102001381620
Central MN42861056367118
Total6511135867119165
Isolates from sugarbeet

One isolate of F. graminearum used in this study was isolated from sugarbeet collected in a commercial field near Sabin, Minnesota showing symptoms of dry decay of the tap root. Four additional isolates used in this study were previously isolated from diseased sugarbeets in a field near Fisher, Minnesota (courtesy of C. Windels, University of Minnesota, Crookston).

Isolates from wheat

Ten isolates of F. graminearum used in this study were originally isolated from infected wheat heads in North Dakota (courtesy of S. Ali, North Dakota State University) and five isolates from infected wheat heads in Idaho (courtesy of J. Windes, University of Idaho). Preliminary morphological identification of F. graminearum was based on formation of perithecia and macroconidia on carnation leaf agar, carmine colouration of the underside of the culture, and white fluffy mycelium of cultures on PDA. To further confirm the identity as F. graminearum, PCR was conducted using Fg16NF/R primer pairs of representative isolates from potato (n = 6) and sugarbeet (n = 5) previously identified by morphological characteristics (Burlakoti et al., 2007). Single-spore cultures were prepared for each isolate used in this study, and each isolate retained was recovered from a single potato tuber.

Isolate aggressiveness of Fusarium graminearum isolates originating from potato, sugarbeet and wheat towards potato tubers

Selected F. graminearum isolates recovered from diseased potatoes (n = 15), sugarbeets (n = 5), and wheat (n = 15) were tested for aggressiveness to potato tubers. To evaluate aggressiveness, healthy potato cv. Russet Burbank tubers were washed to eliminate excess soil and surface-sterilized for 5 min using a 0·5% sodium hypochlorite solution, and rinsed with distilled water before inoculation. A total of 15 tubers per Fusarium isolate were inoculated in each experiment. Potato tubers were inoculated by removing a plug of tissue 5 mm in diameter by approximately 10 mm deep using a cork borer, and replacing it with a 5-mm-diameter mycelial plug from a 5-day-old actively growing Fusarium culture. Two F. sambucinum isolates, 413-1a and 420-1c, which were originally isolated from potato tubers with dry rot, were included as positive controls, and a half-strength PDA agar plug was included as a negative control. Fungal morphology and restriction fragment length polymorphism endonuclease digestion patterns of the internal transcribed spacer region compared to known isolates of F. sambucinum from the Fusarium Research Center were used to confirm the identity of the F. sambucinum isolates (Rivera et al., 2008). After inoculation, five tubers were placed in a plastic box and a single layer of moist paper towels was placed on top of the tubers and boxes sealed with a plastic lid. The experiment was arranged in a randomized complete block design (Steele & Torrie, 1980) consisting of 38 treatments (37 isolates + one non-inoculated control). Each treatment consisted of five tubers and the treatments were replicated three times. Boxes were incubated in a climate-controlled room at 13°C in the dark for 4 weeks. The experiment was performed twice. Severity of disease was evaluated after 4 weeks by cutting the tubers longitudinally at the inoculation site and measuring the depth of decayed tissue in millimeters. Tissue was collected from infected tubers from each treatment and placed on APDA medium to confirm the presence of the inoculated pathogen and conclude Koch’s postulates.

Effect of wounding on infection by Fusarium graminearum in potato tubers

In order to establish how the degree of tuber injury affected the ability of F. graminearum to infect potato tubers relative to F. sambucinum, four injury levels – non-wounded, skinning, bruising and plug – were evaluated to determine the influence of wound severity on infection by each Fusarium species. Healthy potato cv. Russet Burbank tubers were selected from a field-grown crop and washed to eliminate excess soil, surface-sterilized for 5 min using a 0·5% sodium hypochlorite solution, and rinsed with distilled water prior to inoculation.

Non-wounded

Tubers were inoculated by placing a 5-mm mycelial plug from 5-day-old actively growing Fusarium cultures directly onto the non-wounded periderm.

Skinning injury

An area of tuber periderm approximately 10 × 10 mm was removed using a plastic scrub pad. The resulting wound was inoculated by placing a 5-mm mycelial plug from 5-day-old actively growing Fusarium cultures directly onto the abraded area. This wound simulated the degree of skinning frequently observed on potato tubers harvested in the north-central USA when potato haulms are not desiccated prior to harvest.

Bruise injury

Standardized bruising was created using a custom-made bruise machine designed for black spot bruise testing of potato cultivars (Taylor et al., 1993), which drops a 115-g steel ball from a height of 50 cm onto a stationary tuber. This wound provides no visible injury to the potato periderm but permits the entry of wound pathogens. A 5-mm-diameter mycelial plug from a 5-day-old actively growing Fusarium culture was placed directly on the bruised area.

Plug injury

Potato tubers were inoculated by removing a plug of tissue 5 mm in diameter by 10 mm deep using a cork borer, and replacing it with a 5-mm-diameter mycelial plug from 5-day-old actively growing Fusarium culture. This wound simulated an invasive injury encountered at harvest when stolons are removed abruptly from tubers on non-desiccated potato plants during mechanical harvesting. The tubers were placed in a plastic box and covered with a layer of moist paper towels. The boxes were then sealed with a plastic lid and incubated for 3 weeks at 13°C in the dark. Severity of infection was evaluated by cutting the potato tubers longitudinally at the inoculation site and measuring the depth of the lesion. A non-injured, inoculated control was also included in the experiment.

Two Fusarium isolates were used in the study: F. graminearum isolate 492–12 and F. sambucinum isolate 413-1a. These isolates were previously confirmed to be equal in aggressiveness, with disease severity means of 19·8 and 19·7 mm, lesion depth respectively, in aggressiveness trials on tubers (data not shown). Each treatment consisted of five tubers and each treatment was replicated four times. The treatments were arranged as a 2 (Fusarium sp.) × 4 (injury levels) factorial and the experiment was organized as a randomized complete block design and was performed twice.

Statistical analysis

All data were analysed using sas 9.0. Levene’s test for homogeneity of variances was performed to determine if trials could be combined prior to further analysis. Mean separation was done using Fisher’s least protected difference.

Results

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

Prevalence of Fusarium graminearum in stored potatoes with dry rot symptoms

Of the potato tubers collected with putative dry rot, approximately one-third either were not dry rot, or were dry rot with secondary soft rot; these were discarded. From another approximate third of the tubers collected, more than one Fusarium spp. was isolated in mixed cultures or a Fusarium spp. other than F. sambucinum or F. graminearum was recovered; these isolations were also discarded and not counted, since a general survey of Fusarium species was not the intent of the study. From the remaining approximate third of the tubers affected with dry rot, either F. sambucinum or F. graminearum was recovered; the relative proportions were 58%F. sambucinum and 42%F. graminearum (Table 1). Overall, of the tubers with dry rot symptoms, F. sambucinum alone was recovered from 19·0% of the samples collected from stores, and F. graminearum from 13·7% (Table 1).

Pathogenicity of Fusarium graminearum isolates from potato, sugarbeet and wheat to potato tubers

Levene’s test for homogeneity of variances indicated that variances among trials were not homogeneous; therefore data from each trial were analysed separately. All isolates of Fusarium from both species were pathogenic to potato tubers. Significant differences in disease severity were observed among isolates in both trials. Host origin had no significant impact on the disease severity of F. graminearum isolates in either trial. In trial 1, the depth of penetration of potato tubers inoculated with isolates of F. graminearum from three original hosts (wheat, potato and sugarbeets) ranged from 19·2 to 20·5 mm, and in trial 2, from 16·5 to 16·6 mm. A significant difference was observed in disease severity between F. sambucinum and F. graminearum in trial 1, but not trial 2. In trial 1, F. sambucinum isolates averaged a disease severity of 22·4 mm penetration, whilst F. graminearum isolates averaged 19·7 mm.

Effect of wounding on infection by Fusarium graminearum to potato tubers

Levene’s test for homogeneity demonstrated that variances were homogenous, therefore, the data from the two trials were combined for further analysis. A significant interaction was found among main effects for tuber injury and Fusarium species (< 0·05). Significant differences among the main effects of tuber injury (< 0·05) and between Fusarium species (< 0·05) were also observed. Both Fusarium species (F. graminearum or F. sambucinum) and tuber injury (none, skinning, bruising or plug) significantly affected disease incidence and severity (Table 2, Fig. 1). Fusarium sambucinum caused greater incidence of dry rot (>80%) than F. graminearum, regardless of the type of injury, and this difference was significant (< 0·05), except for plug injury. Low infection incidence (<20%) was observed when tubers were either skinned or bruised and subsequently inoculated with F. graminearum (Fig. 1). Both disease incidence and disease severity were significantly higher when tubers were inoculated with F. graminearum after a plug injury than either skinning or bruising injury. Disease severity caused by both Fusarium spp. was significantly greater after plug injury than after skinning and bruising (Fig. 1).

Table 2.   Effect of type of injury and Fusarium species on incidence and severity of dry rot of potato tubers
Variable Mean value (%)a
Disease incidenceDisease severity
  1. aWithin columns, means followed by the same letter are not significantly different (> 0·05).

InjuryNo injury10 c1·0 c
Skinning47·5 b5·2 b
Bruise51·3 b5·4 b
Plug92·5 a21·3 a
Fusarium speciessambucinum69·4 a10·1 a
graminearum31·3 b6·4 b
image

Figure 1.  Disease incidence (a) and severity (b) of dry rot in potato tubers inoculated with either Fusarium sambucinum or Fusarium graminearum and subjected to three types of injury.

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Discussion

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

This study demonstrated that a sizable proportion of potato dry rot in the north-central potato-producing region of the USA is caused by F. graminearum. This is somewhat surprising, since the customary cause of dry rot in this region for the past 25 years has been F. sambucinum (unpublished data). Both the symptoms and commercial losses of dry rot caused by F. graminearum in stored potato tubers are typical of dry rot caused by F. sambucinum, and further laboratory testing is necessary to determine which species is the cause of the dry rot. In this limited survey, the overall incidence of F. graminearum was 13·7% compared with 19% for F. sambucinum (42% vs. 58%, respectively, when only samples from which only those two species were isolated were compared). The low incidence of Fusarium recovered from survey samples could be the result of a number of factors, including sample collection bias, injuries and other diseases (i.e. Alternaria tuber rot) that resemble dry rot, contaminated cultures, mixtures of pathogenic and non-pathogenic Fusarium spp. that could not be separated, and secondary soft rot that prevented Fusarium growth. Nevertheless, it appears that dry rot caused by F. graminearum has the potential to be a serious problem which may persist in this region as an important storage disease.

Whilst F. graminearum has been associated with dry rot or shown to cause disease when inoculated to potato tubers in controlled trials in many other areas of the world, this is the first report of dry rot in the USA caused by F. graminearum, and may be the most thoroughly documented naturally occurring outbreak of dry rot caused by F. graminearum. In fact, Koch’s postulates were confirmed for isolates from three different hosts – wheat, sugarbeet and potato. To date, dry rot caused by F. graminearum has only been identified in North Dakota and Minnesota, which, coincidently, are the areas of the most severe fusarium head blight in the USA (McMullen et al., 1997).

The isolates of F. graminearum recovered from potato were generally less aggressive in causing dry rot disease than F. sambucinum, although there were individual isolates of F. graminearum that were nearly as aggressive as F. sambucinum. Given the lower aggressiveness of F. graminearum in causing dry rot, it was felt to be appropriate to investigate a possible mechanism for its recent appearance as a dry rot pathogen in the Upper Great Plains.

Fusarium graminearum has been present in wheat and barley fields in the potato-production area of North Dakota and Minnesota for many years, and potatoes are frequently grown in rotation with or adjacent to these wheat and barley fields. Since there are no previous reports of the pathogen causing dry rot in potato in the northern Great Plains region, the results suggest that changes have occurred in the pathogen, in cultural practices, or in the environment that predispose potato tubers to dry rot caused by F. graminearum.

It is unlikely that F. graminearum was simply overlooked as the pathogen, since routine isolations from dry-rot-affected tubers for over 30 years have failed to yield F. graminearum. Inoculum levels of F. graminearum could have increased over the years in fields by the repeated cultivation of the F. graminearum hosts wheat, barley and corn, although cropping systems in the north-central USA have changed little in the past 20 years. It is also possible that a genetic change in the pathogen population could be responsible. This explanation is unlikely, since studies with many of the same isolates (Burlakoti et al., 2008) showed low genetic variation between cereal and non-cereal populations, suggesting a single large population of F. graminearum affecting multiple crops in the north-central USA. Certainly, the increase in dry rot caused by F. graminearum is not the result of a difference in the host source of inoculum, since the present study showed that there was no significant difference in the ability of F. graminearum to cause dry rot of potato tubers whether the original host was wheat, potato or sugarbeet.

A change in environmental or cultural practices would seem to be the most likely explanation for the increased incidence of F. graminearum caused dry rot. A recent change in potato harvesting operations in North Dakota and Minnesota led to a preliminary hypothesis that perhaps this is contributing to infections of F. graminearum in potato tubers. Recent economic constraints on the potato industry have caused many potato producers for the processing market to abandon vine desiccation in favour of obtaining higher yields. Potato producers now allow potatoes to grow and then simply senesce slowly over time, or crops are mechanically vine-killed on the day of harvest. Vine desiccation has been an important component in potato production because it hastens periderm maturation and skin set, making tubers more resistant to injury during harvest (Knowles & Plissey, 2008), but it also allows natural dehiscence of the stolon from the tuber without injury. In the absence of vine desiccation, stolons are often forcibly torn from potato tubers, creating wounds that can act as infection courts for many tuber pathogens, including F. graminearum. This is especially true for very late-maturing cultivars, such as Russet Burbank, the most widely grown processing cultivar in the north-central region of the USA and the cultivar used in this study. The majority of tuber samples observed with dry rot caused by F. graminearum were affected at the stem end, where the stolon attaches to the tuber. An evaluation of the degree of injury needed for F. graminearum to cause disease compared to the injury size needed for F. sambucinum to infect seemed to confirm this change in vine killing as a probable cause of dry rot, but this hypothesis needs to be confirmed by additional trials. The results demonstrate that the degree of injury needed for F. graminearum to cause disease in potato tubers is greater than that required by F. sambucinum. There was very little infection when F. graminearum was inoculated after a minor bruise or skinning of the periderm, whilst F. sambucinum was able to infect and cause more severe dry rot lesions under those circumstances. Since cultural practices in harvesting potatoes have changed and growers are opting for green harvest with no vine desiccation, it is possible that this causes a tearing and removal of tuber tissue when the stolon is forcibly removed during the harvest operation, thus providing the wound necessary for F. graminearum infection. Based on the preliminary data presented here, future studies will attempt to further elucidate the role of cultural practices in the development of F. graminearum as a potato dry rot pathogen.

In contrast to most isolates of F. sambucinum in North America and Europe, which have become resistant to TBZ as a result of the widespread use of this fungicide, all tested isolates of F. graminearum recovered from potatoes with dry rot (n = 127) proved sensitive to TBZ. Postharvest application of TBZ remains an option for control of potato dry rot in storage caused by F. graminearum.

Acknowledgements

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

Support for this work was provided in part by JR Simplot Co., Lamb-Weston, Cavendish Farms and Offutt Farms. We thank Dr Juliet Windes, Dr Carol Windels and Dr Shakut Ali for F. graminearum isolates used in this study.

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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