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Article

Peronosporales Species Associated with Strawberry Crown Rot in the Czech Republic

by
Matěj Pánek
1,*,
Marie Maňasová
2,
Jana Wenzlová
2,
Miloslav Zouhar
2 and
Jana Mazáková
2
1
Team of Ecology and Diagnostics of Fungal Plant Pathogens, Crop Research Institute, Drnovská 507/73, 161 06 Prague, Czech Republic
2
Department of Plant Protection, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 129, 165 00 Prague, Czech Republic
*
Author to whom correspondence should be addressed.
J. Fungi 2022, 8(4), 346; https://doi.org/10.3390/jof8040346
Submission received: 21 February 2022 / Revised: 23 March 2022 / Accepted: 25 March 2022 / Published: 26 March 2022
(This article belongs to the Topic Infectious Diseases)
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Abstract

:
The symptoms of crown rot on strawberry plants are considered typical for the pathogen Phytophthora cactorum, which causes high losses of this crop. However, an unknown number of related species of pathogens of Peronosporales cause symptoms quite similar to those caused by P. cactorum. To determine their spectrum and importance, strawberry plants were sampled from 41 farms in the Czech Republic. The cultures were isolated from the symptomatic plants using the baiting method, with subsequent cultivation on a semiselective medium. Isolates were identified to the species level using nuclear ribosomal internal transcribed spacer (ITS) barcoding after preliminary morphological determination. In total, 175 isolates of 24 species of Phytophthora, Phytopythium, Pythium, and Globisporangium were detected. The most represented was Phytophthora cactorum, with 113 (65%) isolates, which was recorded in 61% of farms, and the Pythium dissotocum complex with 20 (11%) isolates, which was recorded in 27% of farms. Other species were represented in units of percent. Large differences between farms in the species spectra were ascertained. The differences between species in cardinal growth temperatures and different management of the farms are discussed as a main reason for such a diversification. Regarding the dissimilar sensitivity of various species of Peronosporales against fungicides, the proper determination of the cause of disease is of crucial significance in plant protection.

1. Introduction

Strawberries, which are grown in convenient environments of temperate climate zones worldwide, are important crops. The most devastating pathogens of this plant species include fungi such as Botrytis cinerea and Verticilium dahliae [1,2], but one of the most serious pathogens is an oomycete of the order Peronosporales—Phytophthora cactorum (Lebert and Cohn) J. Schröt. This polyphagous pathogen causes damage to strawberry plants by attacking the roots and rhizomes and inflicting extensive necroses [3]; under some circumstances, it also infects fruits [4,5]. Under the weather conditions convenient for disease development, losses can reach up to tens of percent [6]. The typical symptoms of infection are the wilting of leaves and the creation of reddish to brownish lesions often visible on the cross-section of the rhizome. The symptoms on underground plant organs are necroses on gradually blackening roots, which simultaneously lose their ability to supply the plant with water and nutrition [4]. Under conditions beneficial for pathogen development, the infected plants often die in a few days. On the affected fruits, P. cactorum causes leather rot and softening of the fruit. The ability of P. cactorum to spread via actively movable flagellated zoospores is immense under circumstances convenient for spreading, i.e., in water or water-saturated soil [7,8]. Additionally, the ability to survive viable in soil via thick-walled oospores is significant [9,10,11]. Although the detrimental influence of this pathogen on the health of strawberry plants has been known for a long time [4], considerably less is known about the importance of related species of soil-borne pathogens of the same order, Peronosporales, which are characterized by similar abilities [8]. As the exact causes of diseases caused by various species of these pathogens are difficult to distinguish from each other based only on symptoms, part of the damage caused by those pathogens is probably incorrectly attributed to P. cactorum [8].
During the last few decades, in different parts of the world, many pathogenic species of the order Peronosporales have been documented in association with strawberry plants. Dissimilar to P. cactorum, none of them seemed to have a similar regular association with strawberries. Nine species have been documented from the genus Phytophthora, which are associated with strawberries, including some of the most important polyphagous pathogens, such as P. fragariae, P. plurivora, P. citophthora, P. nicotianae, P. cryptogea, P. bisheria, P. nagaii, P. fragariaefolia, and P. capsici [12,13,14,15,16,17,18,19]. Associations with strawberries have been documented in other soil pathogens of the related genera Globisporangium, Elongisporangium, Pythium, and Phytopythium. Some of their members were only recently separated from the former genus designation Pythium [20,21]. As a cause of strawberry disease, the following species were identified: Globisporangium ultimum (all Globisporangium spp. in association with strawberry plants were originally documented as Pythium spp.), G. intermedium, G. violae, several members of the G. sylvaticum complex, G. spinosum, G. echinulatum, G. paroecandrum, G. carolinianum, G. spinosum, G. intermedium, G. mastophorum and G. polymastum, Elongisporangium (as Pythium) anandrum, Pythium afertile, Py. angustatum, Py. apleroticum, Py. inflatum, Py. torulosum, Py. aphanidermatum, Py. myriotylum, Phytopythium helicoides, and Phy. megacarpum [20,22,23,24,25,26,27,28,29]. Some of these species, together with several members of the fungal genera Fusarium and Rhizoctonia as well as nematodes, such as Pratylenchus penetrans, are believed to participate in strawberry black rot disease, which is a complex disease of strawberry plants [30,31,32,33].
Since the ability of many of these P. cactorum relatives to survive and spread is similar to that of P. cactorum alone [8,34,35,36], it is reasonable to evaluate the importance of these pathogens for strawberry disease development. The aim of the current study is to evaluate the presence of soil-borne pathogens of Peronosporales in association with strawberry plants showing symptoms resembling disease caused by P. cactorum in farms in the Czech Republic. The study is based on the isolation of pathogen strains from plant roots using the leaf baiting method with subsequent cultivation on semiselective media. Species determination was performed by the commonly used method, nuclear ribosomal internal transcribed spacer (ITS) DNA barcoding [36,37,38,39,40], after preliminary morphological classification.

2. Materials and Methods

2.1. Sampling

A total of 41 strawberry farms in the Czech Republic was sampled, covering the whole spectrum from small farms comprising only a few fields to the largest ones, focused on intensive commercial strawberry production. Strawberry plants showing typical symptoms of Phytophthora crown rot (wilting, greyish leaves, necrotic roots, or reddish-brown lesions on cross sections of rhizomes) [4] were found on the farms, and samples of plants showing such symptoms were taken. The pathogens were isolated using the leaf baiting method [41]. The roots and rhizomes of symptomatic strawberry plants were washed with tap water and flooded with demineralised water in a plastic dish. The baiting leaves of susceptible plant species (Fagus silvatica, Hedera helix, Castanea sativa, Rhododendron sp.) were placed on the water’s surface. After the necrotic lesions developed on these leaves, the whole leaves were washed with tap water and surface sterilized with 70% ethanol for 30 s. The border regions between the affected and healthy tissues on the margins of lesions were cut out and placed on the semiselective medium PARPNH V8 [42,43]. The cultures developed from the specimens of plant tissues were then maintained on V8 agar plates. The isolates were deposited in the culture collection of agriculturally important fungi of the Crop Research Institute, VURV-F.

2.2. Species Determination

After a morphological determination based on the morphology of reproductive structures present (oogonia, zoosporangia, chlamydospores), all cultures were classified into species using ITS DNA barcoding [44]. For molecular processing, the cultures were cultivated on V8 agar plates covered by cellophane wrap. After the colony was developed, the mycelium was scraped from the surface of the cellophane, and a small piece was placed into a microcentrifuge tube in 20 µL of a dilution buffer of the Phire Plant Direct PCR Kit (Thermo Fisher Scientific, Inc., Waltham, MA, USA). This kit was also used to perform the PCR according to the manufacturer’s instructions; 2 µL of dilution buffer containing the sample DNA was added to the total volume of 25 µL of Phire Plant PCR Master Mix, including 0.2 mM primers ITS1 and ITS4 [45]. The reaction was performed in an Eppendorf Mastercycler Nexus Thermal Cycler (Eppendorf AG, Hamburg, Germany) under the following settings: 98 °C for 2 min; 35 cycles of 98 °C for 30 s; 55 °C for 30 s; 72 °C for 60 s; then, 72 °C for 10 min. The purification and sequencing of the PCR product were performed by Macrogen, Inc. (Seoul, Korea). The DNA sequences were determined both in the forward and reverse directions; the consensual sequences were used in subsequent analyses. The identity of the species was determined by comparing the DNA sequences to the NCBI database using the BLAST algorithm. In the final species determination, the preliminary ascertained morphological characteristics were also taken into consideration.

2.3. Evaluation of Soil-Inhabiting Species Spectra of Peronosporales Present in Particular Localities

During sampling in the field, the number of samples of symptomatic plants taken from each farm, the number of isolates, and the number of species from each sample were recorded. Only one member of each species isolated from one plant was considered an individual isolate. The number of isolates of each species found was expressed as a percentage of the total number of isolates from each farm and from all farms. The number of farms in which no isolate/only P. cactorum/P. cactorum accompanied by other species/only other species was found were expressed in absolute values and percentages. The correlation between the number of samples, isolates, and species found on each farm was ascertained using the software Statistica 14.0 (Tibco Software Inc., Palo Alto, CA, USA). To express the degree of correlation of these numbers, the Spearman coefficient was calculated, and the same numbers were displayed on the line chart.

3. Results

The number of samples taken from particular farms was 1 to 94 depending on the size of the farm and on the number of symptomatic plants found; the average number of sampled plants per farm was 16. In total, 459 strawberry plants were taken showing typical symptoms of infection by Phytophthora cactorum. After the isolation of mycelial cultures from plant specimens, 24 species were identified (Table 1). The detailed list of all isolates and the NCBI GenBank accession numbers of sequences of their ITS rDNA region used in species determination are given in Supplementary Table S1. Since the unambiguous identification of some species closely related to Pythium dissotocum was not possible on the basis of either sequencing or morphology [46], these isolates were labelled the Pythium dissotocum complex, which was in agreement with the solution used in other works [36,47].
Considering only one member of each species isolated from one plant as an individual isolate, a total of 175 cultures was isolated. In only six cases, two different pathogen species were isolated from one plant. The majority (113, i.e., 65%) of isolates were identified as Phytophthora cactorum; other frequently represented isolates included members of a Pythium dissotocum complex (20, i.e., 11%). Apart from those two species, the other species were represented by less than ten percent (Table 1). The proportion of farms where only P. cactorum was sampled was 32%; in another 29% of farms, this species was accompanied by other pathogens of the genera Pythium, Phytopythium, or Globisporangium. In 22% of farms, only pathogens other than P. cactorum were revealed; in seven farms (17%), no soil-borne pathogens of Peronosporales were isolated (Table 2). Regardless of the species to which they belong, the number of isolates sampled in farms was mostly one to four, with an average of four per farm. The maximum number of isolates originating from one farm was 24; this number represented three species. The maximum number of species originating from one farm was nine, although such a high number was found in only one farm (2%). Only one species was found in twenty farms (49%), while two species were found in nine farms (24%) (Table 3, Supplementary Table S1). These results not only demonstrate that P. cactorum substantially predominates over other soil-borne Peronosporales pathogens, but also indicate the significant participation of at least another 1–3 species of this family in plant losses.
A correlation was found between the number of isolates and the number of species originating from the same farm (Spearman r = 0.74, p < 0.05, Table 4, Figure 1). The correlation between the number of sampled plants on each farm and the number of isolates was lower (r = 0.48, p < 0.05); the correlation between the number of sampled plants and the number of species found was even lower (r = 0.19, p < 0.05).

4. Discussion

The species spectra recorded in particular farms substantially differed from each other, although the distances between farms sampled were lower than a few hundred kilometres. Regardless of the incomparably lower sensitivity of the method we used, i.e., baiting/cultivation, in comparison to the currently widely used metabarcoding, this method had the advantage of capturing only substantially vigorous organisms [48,49]. However, this limitation was common for all sampled farms. In contrast, the metabarcoding method has the disadvantage of a lower ability to clearly differentiate between some species, but most importantly, this method does not have the ability to differentiate between dead and living microorganisms [48]. As follows from the correlation analysis (Table 4, Figure 1), the number of species we found on farms only indirectly and loosely depended on the sampling intensity. Except for the frequency of the occurrence of symptomatic plants, the sampling intensity roughly reflected the size of the farm. Therefore, in the current study, the approximate capture of the true spectrum of oomycete pathogen species present in the rhizosphere of strawberry plants could be assumed, and the total number of species found probably would not have increased substantially even if more plants had been sampled.
In the study, 24 species belonging to four genera of Peronosporales were isolated from symptomatic strawberry plants. All of these species have a global distribution, and all of them have a relatively wide host spectrum; the majority also included strawberries, although in some species, the host spectrum has not yet been well explored in detail [29,30,31,47,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77].
The most important strawberry pathogen we found was Phytophthora cactorum, which was found in 61% of the farms. Although this species dominated in the majority of farms we sampled, in 22% of farms, we did not find this species, while other soil-borne pathogens of Peronosporales (Phytophthora pluvivora, P. cryptogea, Pythium dissotocum complex, Py. nodosum, Py. ultimum, Py. aphanidermatum, Py. heterothallicum, Py. salpingophorum, and Phytopythium montanum) were successfully isolated. In an additional 15% of farms, we did not find any of these pathogens, although unsuccessful baiting cannot be simply interpreted as evidence of their absence. Regardless, it seems that P. cactorum could be missing for a significant proportion of farms, where the symptoms on plants could have been caused by other related members of Peronosporales. Thus, the distribution of P. cactorum did not meet the basic assumption of a standard distribution model, i.e., the equilibrium of the distribution of indigenous organisms with the environmental conditions [78]. Since this is a typical feature of invasive species, such an irregular distribution supports the conception of the non-European origin of this pathogen. The origin of the entire Phytophthora Clade 1, including P. cactorum, is assumed to be North America [79], although it has not yet been unambiguously evidenced. The relatively short coevolution time between strawberry plants and P. cactorum has been documented by the exclusive presence of only one of five known genetic lineages of this species on strawberry plants in the Czech Republic [80], although other lineages are also present on woody host species in this region [81]. Such an exclusive presence of one lineage on strawberries has already been evidenced and explained in association with the intraspecific host specificity developed in P. cactorum [82,83,84].
Three members of Clade 6 [85] of the genus Phytophthora were found in strawberry farms; P. bilorbang, P. lacustris, and P. cryptogea. The association of P. lacustris with strawberry plants was documented only recently [86], while to our knowledge, the association of P. bilorbang with strawberries has not yet been recorded. However, since this species was originally described as a pathogen of Rubus anglocandicans (Rosaceae) [87], its association with the strawberry, a member of the same plant family, is not surprising. Both of these two pathogen species are associated with wetlands or periodically flooded localities. They are the most frequently found in association with (semi)natural stands of riparian forests throughout Europe [50,51,52,53,54]. The possible explanation of their occurrence in strawberry farms could, thus, be hypothesized as a consequence of irrigation with unfiltered water from watercourses or ponds contaminated by these Phytophthora species, by flooding of fields by contaminated water in association with some climatic extremes, or by any other accidental event. In contrast to these two previous species, P. cryptogea, which has also been mentioned to occasionally be associated with strawberry plants [88,89], has an evidenced frequent occurrence in agriculture, although it occurs in forestry and nurseries as well [55,56]. In Europe, this species is common on crops and ornamental plant species, as well as in varied natural stands of woody plants [79,90]. Strains of P. cryptogea differ from each other in their host range [91], i.e., host specificity is evolved in this species. Some isolates are also pathogenic to wheat and other crops, which is congruent with their presence in agricultural lands [92].
The members of Phytophthora Clade 6 are considered usually saprophytic or only occasionally pathogenic in their original forest habitats under normal conditions [93], although the importance of some of them may be underestimated, and some of them are also able to cause significant plant damage [94]. For some Clade 6 Phytophthora spp. such as P. lacustris and P. bilorbang, the development of the infection is also hypothesized to be highly influenced by the temperature. These species switch to a pathogenic lifestyle from that saprophytic lifestyle only under highly optimal environmental conditions [94].
In contrast to the previous species, P. plurivora is considered one of the most important Phytophthora pathogens worldwide, which is associated mainly with forests [79]. This species was suggested by Schoebel et al. [95] to be indigenous to Europe, but given its asymptomatic occurrence on trees in local undisturbed native forests as an indirect indication of long-term coevolution [96], the origin of P. plurivora and all of Phytophthora Clade 2 seems more likely to be in Southeast Asia [97,98]. Nevertheless, P. plurivora is one of the most frequently sampled Phytophthora species in European forests in diverse natural and seminatural stands, as well as in ornamental and horticultural nurseries [79], while its occurrence in association with agriculture and strawberry farms is only rare [18,99]. The other member of Clade 2 we sampled, P. citrophthora, has a main distribution area in the Mediterranean basin and similar regions in association with various Citrus species [100]. Although P. citrophthora causes the greatest damage to Citrus spp., it also has a wide spectrum of other hosts, including the strawberry [55,57]. However, even this pathogen has not yet been shown to be a regular threat to this crop.
Although the origin of the majority of the mentioned Phytophthora species remains unknown, the origin of all other members of the order Peronosporales that we isolated is even less clear. Based on the number of strains we isolated, the second most important pathogen after P. cactorum was the Py. dissotocum complex. Comparing the results of the current study to the other one performed by Toljamo et al. [27] in strawberry fields in Finland, the spectrum of species of the order Peronosporales was shown to be completely different from the spectra found in the current study, where only P. cactorum and Py. dissotocum were isolated equally. Pythium dissotocum and other related pathogens were recently shown to be able to cause necrosis on strawberry plants of similar size as P. cactorum [101]. Since Py. dissotocum was isolated from symptomatic plants in 11 farms (i.e., more than one-quarter of them), and more than 10% of all isolates belong to this species, this should not be considered an unimportant pathogen of strawberry plants. This species, together with Py. aphanidermatum, belongs to the most serious pathogens of this genus for crop production. Both species are associated mainly with vegetables [102]; however, the association with strawberry plants has also been documented [58,59]. We isolated two other members of this genus, Py. intermedium and Py. mamillatum, which are already known pathogens of strawberries [59,103]. The total host spectrum of the majority of other Pythium spp. we isolated (Py. rotratifingens, Py. montanum, Py. conidiophorum, Py. nodosum, Py. perplexum, Py. salpingophorum, Py. Nodosum, and Py. torulosum) remains unknown, and the pathogenicity of some of them against particular host species is not clear. This is obvious in the example of Py. perplexum, which is documented as both pathogenic and nonpathogenic on beans [104,105]. To our knowledge, this was the first report of all eight Pythium species being associated with strawberry plants. Since we did not perform an exact test of their pathogenic role on this crop, theoretically, their role in strawberry roots could be saprotrophic. However, their phytopathogenic nature is well known in many other host species, and since they were isolated from strawberry plant tissues, their role in damage to this host is quite probable.
The differences in species spectra recorded in the particular farms we investigated (Table S1), as well as the noticeable differences between the entire species spectrum found in the current study and in that of Toljamo et al. [27] in Finland, can be explained as a result of a combination of two phenomena. Mainly during the biotrophic phase of infection, the formation and severity of plant disease greatly depend on the temperature [102,106]. This phenomenon has already been mentioned by Littrell et al. [107] for Pythium aphanidermatum, by Watanabe et al. [29] for Globisporangium ultimum, and by Grove et al. [108] for Phytophthora cactorum. This optimal temperature for infection can be quite different from the optimal temperature for growth [29]. The growth temperatures of the species of Peronosporales we found differed considerably, which was documented by the range between the lowest and highest optimum temperatures of these species as wide as 20–35 °C [51,59,61,63,68,72,87,97,103,109]. Although little is known about the temperatures beneficial for infection, the optimal temperature for the development of infection by Globisporangium ultimum is between 9 and 20 °C [29], while that of Pythium aphanidermatum is between 30 and 35 °C [59]. The total range of the cardinal temperatures of a whole species spectrum we isolated was even wider. The composition of the entire community of these pathogens very likely reflects such differences, which pose a threat considering potential climate changes, because the increased temperatures have the potential to cause alterations in the local spectra of pathogens. Such a change could also cause some of the originally rather saprotrophic Peronosporales to switch to a pathogenic lifestyle, as was described for the case of Phytophthora spp. of Clade 6 [94]—P. lacustris and P. bilorbang, the species that we also found. In addition, these two species are also considered tolerant to higher temperatures [51,87], which is potentially beneficial for them in changed environmental conditions.
Another phenomenon probably participating in differences between the species spectra we identified lies in the long-term accumulation of pathogenic species in soil in cases where one crop is cultivated in the same field for a long time. This phenomenon was described for Pythium species in maize and soya fields [110,111] and for many plant pathogens, including some Peronosporales in strawberries [103]. Our observations appeared to be in accordance with these conclusions, as fields used for intensive and long-term commercial strawberry production on farms using pregrown plant stocks are the most severely contaminated with soil Peronosporales pathogens (data not shown), while small fields are less affected.
Both of the mentioned explanations of the presence of different species spectra, whose combination is a probable principal cause of the presence of such a wide total species spectrum and of differences between local spectra, constitute a certain danger for strawberry production. Except for temperatures favouring some non-native species, the joint presence of allopatric species in one field poses a risk of the hybridization of such species [112], with accompanying effects, such as changes in the host species range, increased invasiveness, changes in the ecological requirements of the new hybrid, or the transmission of the genes of resistance to fungicides into a new context. The instability of newly created genomes [113], also associated with potential polyploidy or aneuploidy, enables the increased development of adaptations [114], improved fitness, and the creation of new properties of hybrid progenies [115,116], although the detrimental influence on the progeny, such as the increased oospore abortion rate of some of the descendants or their decreased fitness, could also be the result of hybridization [113]. Such a development can be particularly increased if the progenies further reproduce asexually or substantially asexually [117,118]. The environmental changes, together with the quite different temperature demands of participating parental species, present favourable conditions for such development. The small, genetically plastic populations [119] potentially represented by only a few newly arisen genotypes are able to readily respond to the changing environment.
Most of the Phytophthora species we found have not yet been shown to be systematically associated with strawberry plants, and in the current study, they were recorded only sporadically. Thus, the ascertained occurrence of P. plurivora and P. citrophthora on strawberry plants seems to be more likely the result of an accidental infection from some surrounding sources than the systemic infection spread, for example, by planting stock. However, similar to P. cactorum, species such as P. cryptogea and P. plurivora [84,91,120,121] and probably P. citrophthora as well [122,123] have evolved host specificity at the intraspecific level, meaning that particular pathogen species strains have an uneven ability to infect diverse host species, with one lineage having an increased ability to infect one host species. Due to their immense capacity for clonal reproduction, after accidental contact with strawberry plants, the particular strain of these Phytophthora species or some new hybrids coincidentally better adapted to this host could give rise to a strawberry-specific lineage with increased pathogenic potential against this crop. The association of these species with strawberry plants has also been documented in other works [18,55,57], and the spread of Phytophthora species from nurseries to plantings has also been described [79]. The ability of some members of the genera Phytophthora, Pythium, Phytopythium, and Globisporangium to cause strawberry plant damage comparable to that caused by P. cactorum has been demonstrated [101], and these species are also differently sensitive to fungicides [124]. In the case of the adaptation of these species to strawberry plants, due to the common use of pregrown plantings replanted from infested fields, the fast spread of such lineages can be expected.

5. Conclusions

The results of our research showed that in addition to Phytophthora cactorum, many other related species participate in damage to strawberry plants, which were formerly almost exclusively attributed to P. cactorum. These polyphagous species are members of Phytophthora, Pythium, Phytopythium, and Globisporangium. Some of these species are known as important pathogens associated with some crops, including strawberries, or more generally with agriculture. The other species we also found have been considered to be associated with natural and seminatural habitats. Their presence in fields poses risks in terms of their potential change from the mainly saprotrophic to a parasitic mode, which could be mediated by climate change. Another risk is the potentially accidental development of their lineages specific to strawberry plants, as well as the potential for the creation of hybrid species through hybridization between formerly allopatric parental species. The different sensitivity to fungicides of various, often nonindigenous, species poses another important threat associated with their presence in strawberry fields.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jof8040346/s1, Table S1: the list of all isolates of Peronosporales found in strawberry fields in the Czech Republic. The names of sampled localities and NCBI accession numbers of ITS sequences of all isolates are given.

Author Contributions

Conceptualization, M.P. and M.Z.; methodology, M.P.; formal analysis, M.P.; investigation, M.M., J.W. and M.Z.; resources, M.P.; data curation, M.P.; writing—original draft preparation, M.P.; writing—review and editing, M.P.; visualization, M.P.; supervision, J.M. and M.Z.; project administration, M.P. and M.Z.; funding acquisition, M.P. and M.Z. All authors have read and agreed to the published version of the manuscript.

Funding

The work was financially supported by the project of the Ministry of Agriculture of the Czech Republic within the framework of the National Agency for Agricultural Research, project no QK1710377, and by institutional support MZE-RO0418.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Jarvis, W.R. The infection of strawberry and raspberry fruits by Botrytis cinerea Fr. Ann. Appl. Biol. 1962, 50, 569–575. [Google Scholar] [CrossRef]
  2. Pegg, G.F. The impact of Verticillium diseases in agriculture. Phytopathol. Mediterr. 1984, 23, 176–192. [Google Scholar]
  3. Eikemo, H.; Stensvand, A.; Davik, J.; Tronsmo, A.M. Resistance to crown rot (Phytophthora cactorum) in strawberry cultivars and in offspring from crosses between cultivars differing in susceptibility to the disease. Ann. Appl. Biol. 2003, 142, 83–89. [Google Scholar] [CrossRef]
  4. Deutschmann, F. Eine Wurzelfäule an Erdbeeren, hervorgerufen durch Phytophthora cactorum (Leb. et Cohn) Schroet. Nachr. Dtsch. Pflanzenschutzd. 1954, 6, 7–9. [Google Scholar]
  5. Hantula, J.; Lilja, A.; Parikka, P. Genetic variation and host specificity of Phytophthora cactorum isolated in Europe. Mycol. Res. 1997, 101, 565–572. [Google Scholar] [CrossRef]
  6. Winterbottom, C.; Westerlund, F.; Mircetich, J.; Galper, L.; Welch, N. Evaluation of relative resistance of different strawberry cultivars to Phytophthora and Verticillium dahliae as a potential alternative to methyl bromide. In Proceedings of the Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions, Orlando, FL, USA, 4–6 November 1996; pp. 36-31–36-35. [Google Scholar]
  7. Delmas, C.E.; Mazet, I.D.; Jolivet, J.; Delière, L.; Delmotte, F. Simultaneous quantification of sporangia and zoospores in a biotrophic oomycete with an automatic particle analyzer: Disentangling dispersal and infection potentials. J. Microbiol. Methods 2014, 107, 169–175. [Google Scholar] [CrossRef] [PubMed]
  8. Raftoyannis, Y.; Dick, M.W. Zoospore encystment and pathogenicity of Phytophthora and Pythium species on plant roots. Microbiol. Res. 2006, 161, 1–8. [Google Scholar] [CrossRef]
  9. Darmono, T.W.; Parke, J.L. Chlamydospores of Phytophthora cactorum: Their production, structure, and infectivity. Can. J. Bot. 1990, 68, 640–645. [Google Scholar] [CrossRef]
  10. Harris, D.C. Survival of Phytophthora syringae oospores in and on apple orchard soil. Trans. Br. Mycol. Soc. 1985, 85, 153–155. [Google Scholar] [CrossRef]
  11. Sneh, B.; McIntosh, D.L. Studies on the behavior and survival of Phytophthora cactorum in soil. Can. J. Bot. 1974, 52, 795–802. [Google Scholar] [CrossRef]
  12. Abad, Z.G.; Abad, J.A.; Coffey, M.D.; Oudemans, P.V.; Man in’t Veld, W.A.; de Gruyter, H.; Cunnington, J.; Louws, F.J. Phytophthora bisheria sp. nov., a new species identified in isolates from the Rosaceous raspberry, rose and strawberry in three continents. Mycologia 2008, 100, 99–110. [Google Scholar] [CrossRef] [PubMed]
  13. Barboza, E.A.; Fonseca, M.E.N.; Boiteux, L.S.; Reis, A. First worldwide report of a strawberry fruit rot disease caused by Phytophthora capsici isolates. Plant Dis. 2017, 101, 259. [Google Scholar] [CrossRef]
  14. Hickman, C.J. The red core root disease of the strawberry caused by Phytophthora fragariae n.sp. J. Pomol. Hortic. Sci. 1941, 18, 89–118. [Google Scholar] [CrossRef]
  15. Irzykowska, L.; Irzykowski, W.; Jarosz, A.; Golebniak, B. Association of Phytophthora citricola with leather rot disease of strawberry. J. Phytopathol. 2005, 153, 680–685. [Google Scholar] [CrossRef]
  16. Parikka, P.K.; Vestberg, M.; Karhu, S.T.; Haikonen, T.; Hautsalo, J. Possibilities for biological control of red core (Phytophthora fragariae). VIII Int. Strawb. Symp. 2017, 1156, 751–756. [Google Scholar] [CrossRef]
  17. Rahman, M.Z.; Uematsu, S.; Takeuchi, T.; Shirai, K.; Ishiguro, Y.; Suga, H.; Kageyama, K. Two new species, Phytophthora nagaii sp. nov. and P. fragariaefolia sp. nov., causing serious diseases on rose and strawberry plants, respectively, in Japan. J. Gen. Plant Pathol. 2014, 80, 348–365. [Google Scholar] [CrossRef]
  18. Rytkönen, A.; Lilja, A.; Vercauteren, A.; Sirkiä, S.; Parikka, P.; Soukainen, M.; Hantula, J. Identity and potential pathogenicity of Phytophthora species found on symptomatic Rhododendron plants in a Finnish nursery. Can. J. Plant Pathol. 2012, 34, 255–267. [Google Scholar] [CrossRef]
  19. Suzui, T.; Makino, T.; Ogoshi, A. Phytophthora rot of strawberry caused by Phytophthora nicotianae var. parasitica in Shizuoka. Jap. J. Phytopathol. 1980, 46, 169–178. [Google Scholar] [CrossRef] [Green Version]
  20. De Cock, A.W.; Lodhi, A.M.; Rintoul, T.L.; Bala, K.; Robideau, G.P.; Abad, Z.G.; Coffey, M.D.; Shahzad, S.; Lévesque, C.A. Phytopythium: Molecular phylogeny and systematics. Persoonia 2015, 34, 25–39. [Google Scholar] [CrossRef] [Green Version]
  21. Uzuhashi, S.; Tojo, M.; Kakishima, M. Phylogeny of the genus Pythium and description of new genera. Mycoscience 2010, 51, 337–365. [Google Scholar] [CrossRef]
  22. Eden, M.A.; Hill, R.A. First record of Pythium mastophorum in New Zealand and its pathogenicity relative to other Pythium spp. N. Z. J. Crop Hortic. Sci. 1998, 26, 253–256. [Google Scholar] [CrossRef] [Green Version]
  23. Ishiguro, Y.; Otsubo, K.; Watanabe, H.; Suzuki, M.; Nakayama, K.; Fukuda, T.; Fujinaga, M.; Suga, H.; Kageyama, K. Root and crown rot of strawberry caused by Pythium helicoides and its distribution in strawberry production areas of Japan. J. Gen. Plant Pathol. 2014, 80, 423–429. [Google Scholar] [CrossRef]
  24. Marin, M.V.; Seijo, T.; Mertely, J.; Peres, N.A. First report of crown rot caused by Phytopythium helicoides on strawberry in the Americas. Plant Dis. 2019, 103, 2696. [Google Scholar] [CrossRef]
  25. Mouden, N.; Benkirane, R.; Ouazzani Touhami, A.; Douira, A. Fungal species associated with collapsed strawberry plants cultivated in strawberries plantations in Morocco. Int. J. Curr. Res. 2016, 8, 29108–29117. [Google Scholar]
  26. Shennan, C.; Muramoto, J.; Koike, S.; Baird, G.; Fennimore, S.; Samtani, J.; Bolda, M.; Dara, S.; Daugovish, O.; Lazarovits, G.; et al. Anaerobic soil disinfestation is an alternative to soil fumigation for control of some soilborne pathogens in strawberry production. Plant Pathol. 2018, 67, 51–66. [Google Scholar] [CrossRef]
  27. Toljamo, A.R.; Granlund, L.J.; Kokko, H.I. DNA barcode identification and virulence testing of Phytophthora spp. and Pythium spp. isolated from soil of strawberry fields. VIII Int. Strawb. Symp. 2017, 1156, 727–734. [Google Scholar] [CrossRef]
  28. Watanabe, T. Pathogenicity of Pythium myriotylum isolated from strawberry roots in Japan. Ann. Phytopath. Soc. Jpn. 1977, 43, 306–309. [Google Scholar] [CrossRef] [Green Version]
  29. Watanabe, T.; Hashimoto, K.; Sato, M. Pythium species associated with strawberry roots in Japan, and their role in the strawberry stunt disease. Phytopathology 1977, 67, 1324–1332. [Google Scholar] [CrossRef]
  30. Fang, X.L.; Phillips, D.; Li, H.; Sivasithamparam, K.; Barbetti, M.J. Severity of crown and root diseases of strawberry and associated fungal and oomycete pathogens in Western Australia. Australas. Plant Pathol. 2011, 40, 109–119. [Google Scholar] [CrossRef]
  31. Fang, X.L.; Phillips, D.; Li, H.; Sivasithamparam, K.; Barbetti, M.J. Comparisons of virulence of pathogens associated with crown and root diseases of strawberry in Western Australia with special reference to the effect of temperature. Sci. Hortic. 2011, 131, 39–48. [Google Scholar] [CrossRef]
  32. LaMondia, J. Strawberry black root rot. Adv. Strawb. Res. 2004, 23, 1–10. [Google Scholar]
  33. Martin, F.N. Strawberry root rot and the recovery of Pythium and Rhizoctonia spp. In Proceedings of the Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions, San Diego, CA, USA, 1–4 November 1999. [Google Scholar]
  34. Burdon, J.J.; Chilvers, G.A. Epidemiology of damping-off disease (Pythium irregulare) in relation to density of Lepidium sativum seedlings. Ann. Appl. Biol. 1975, 81, 135–143. [Google Scholar] [CrossRef]
  35. Green, H.; Jensen, D.F. Disease progression by active mycelial growth and biocontrol of Pythium ultimum var. ultimum studied using a rhizobox system. Phytopathology 2000, 90, 1049–1055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Redekar, N.R.; Eberhart, J.L.; Parke, J.L. Diversity of Phytophthora, Pythium, and Phytopythium species in recycled irrigation water in a container nursery. Phytobiomes J. 2019, 3, 31–45. [Google Scholar] [CrossRef] [Green Version]
  37. Lookabaugh, E.C.; Ivors, K.L.; Shew, B.B. Mefenoxam sensitivity, aggressiveness, and identification of Pythium species causing root rot on floriculture crops in North Carolina. Plant Dis. 2015, 99, 1550–1558. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Htun, Z.M.; Rotchanapreeda, T.; Rujirawat, T.; Lohnoo, T.; Yingyong, W.; Kumsang, Y.; Sae-Chew, P.; Payattikul, P.; Yurayart, C.; Limsivilai, O.; et al. Loop-mediated isothermal amplification (LAMP) for identification of Pythium insidiosum. Int. J. Infect. Dis. 2020, 101, 149–159. [Google Scholar] [CrossRef]
  39. Olson, J.D.; Damicone, J.P.; Kahn, B.A. Identification and characterization of isolates of Pythium and Phytophthora spp. from snap beans with cottony leak. Plant Dis. 2016, 100, 1446–1453. [Google Scholar] [CrossRef]
  40. Radmer, L.; Anderson, G.; Malvick, D.M.; Kurle, J.E.; Rendahl, A.; Mallik, A. Pythium, Phytophthora, and Phytopythium spp. associated with soybean in Minnesota, their relative aggressiveness on soybean and corn, and their sensitivity to seed treatment fungicides. Plant Dis. 2017, 101, 62–72. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  41. Themann, K.; Werres, S. Baiting of Phytophthora sp. with the Rhododendron leaf test. In Proceedings of the First International Meeting on Phytophthoras in Forest and Wildland Ecosystems, Grants Pass, OR, USA, 30 August–3 September 1999. [Google Scholar]
  42. Balcì, Y.; Halmschlager, E. Phytophthora species in oak ecosystems in Turkey and their association with declining oak trees. Plant Pathol. 2003, 52, 694–702. [Google Scholar] [CrossRef]
  43. Tsao, P.H. Factors affecting isolation and quantitation of Phytophthora from soil. In Phytophthora: Its Biology, Taxonomy, Ecology, and Pathology, 1st ed.; Erwin, D.C., Bartnicki-Garcia, S., Tsao, P.H., Eds.; American Phytopathological Society: St. Paul, MN, USA, 1983; pp. 219–236. [Google Scholar]
  44. Kageyama, K. Molecular taxonomy and its application to ecological studies of Pythium species. J. Gen. Plant Pathol. 2014, 80, 314–326. [Google Scholar] [CrossRef]
  45. White, T.J.; Bruns, T.; Lee, S.; Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications, 1st ed.; Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., Eds.; Academic Press, Inc.: San Diego, CA, USA, 1990; pp. 315–322. [Google Scholar]
  46. Lévesque, C.A.; de Cock, A.W. Molecular phylogeny and taxonomy of the genus. Pythium. Mycol. Res. 2004, 108, 1363–1383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Petkowski, J.E.; de Boer, R.F.; Norng, S.; Thomson, F.; Minchinton, E.J. Pythium species associated with root rot complex in winter-grown parsnip and parsley crops in south eastern Australia. Australas. Plant Pathol. 2013, 42, 403–411. [Google Scholar] [CrossRef]
  48. Bose, T.; Wingfield, M.J.; Roux, J.; Vivas, M.; Burgess, T.I. Community composition and distribution of Phytophthora species across adjacent native and non-native forests of South Africa. Fungal Ecol. 2018, 36, 17–25. [Google Scholar] [CrossRef] [Green Version]
  49. Khaliq, I.; Hardy, G.E.S.J.; White, D.; Burgess, T.I. eDNA from roots: A robust tool for determining Phytophthora communities in natural ecosystems. FEMS Microbiol. Ecol. 2018, 94, fiy048. [Google Scholar] [CrossRef] [Green Version]
  50. Matsiakh, I.; Kramarets, V.; Cleary, M. Occurrence and diversity of Phytophthora species in declining broadleaf forests in western Ukraine. For. Pathol. 2021, 51, e12662. [Google Scholar] [CrossRef]
  51. Nechwatal, J.; Bakonyi, J.; Cacciola, S.O.; Cooke, D.E.L.; Jung, T.; Nagy, Z.Á.; Vannini, A.; Vettraino, A.M.; Brasier, C.M. The morphology, behaviour and molecular phylogeny of Phytophthora taxon Salixsoil and its redesignation as Phytophthora lacustris sp. nov. Plant Pathol. 2013, 62, 355–369. [Google Scholar] [CrossRef] [Green Version]
  52. Reeser, P.W.; Sutton, W.; Hansen, E.M.; Remigi, P.; Adams, G.C. Phytophthora species in forest streams in Oregon and Alaska. Mycologia 2011, 103, 22–35. [Google Scholar] [CrossRef] [PubMed]
  53. Santilli, E.; Riolo, M.; La Spada, F.; Pane, A.; Cacciola, S.O. First report of root rot caused by Phytophthora bilorbang on Olea europaea in Italy. Plants 2020, 9, 826. [Google Scholar] [CrossRef] [PubMed]
  54. Scanu, B.; Linaldeddu, B.; Pérez-Sierra, A.; Deidda, A.; Franceschini, A. Phytophthora ilicis as a leaf and stem pathogen of Ilex aquifolium in Mediterranean islands. Phytopathol. Mediterr. 2014, 53, 480–490. [Google Scholar] [CrossRef]
  55. Erwin, D.C.; Ribeiro, O.K. Phytophthora Diseases Worldwide, 1st ed.; American Phytopathological Society: St Paul, MN, USA, 1996; p. 592. [Google Scholar]
  56. Mostowfizadeh-Ghalamfarsa, R.; Panabieres, F.; Banihashemi, Z.; Cooke, D.E.L. Phylogenetic relationship of Phytophthora cryptogea Pethybr. & Laff and P. drechsleri Tucker. Fungal Biol. 2010, 114, 325–339. [Google Scholar] [CrossRef] [PubMed]
  57. Cohen, S.; Allasia, V.; Venard, P.; Notter, S.; Vernière, C.; Panabières, F. Intraspecific variation in Phytophthora citrophthora from citrus trees in Eastern Corsica. Eur. J. Plant Pathol. 2003, 109, 791–805. [Google Scholar] [CrossRef]
  58. Nemec, S. Histopathology of Pythium infected strawberry roots. Can. J. Bot. 1972, 50, 1091–1096. [Google Scholar] [CrossRef]
  59. Van der Plaats-Niterink, A.J. Monograph of the Genus Pythium, 1st ed.; Centraalbureau voor Schimmelcultures: Baarn, The Netherlands, 1981; p. 244. [Google Scholar]
  60. Badali, F.; Abrinbana, M.; Abdollahzadeh, J.; Khaledi, E. Molecular and morphological taxonomy of Pythium species isolated from soil in West Azarbaijan province (N.W. Iran). Rostaniha 2016, 17, 78–91. [Google Scholar] [CrossRef]
  61. De Cock, A.W.A.M.; Lévesque, C.A. New species of Pythium and Phytophthora. Stud. Mycol. 2004, 50, 481–487. [Google Scholar]
  62. Ekwamu, A.; Mukalazi, J.; Buruchara, R.A. Pythium Species in Bean Fields in Uganda, 1st ed.; LAP LAMBERT Academic Publishing: Chisinau, Moldova, 2013; p. 136. [Google Scholar]
  63. Hosseini Badrbani, A.; Abbasi, S.; Bolboli, Z.; Jamali, S.; Sharifi, R. Morphological and molecular characterization of Oomycetes associated with root and crown rot of cucurbits in Kermanshah province, Iran. Mycol. Iran. 2018, 5, 15–27. [Google Scholar] [CrossRef]
  64. Chen, J.J.; Yu, J.; Zhou, Y.H.; Yang, H.J. Pythium glomeratum and Py. nodosum, two new records from China. J. Microbiol. Exp. 2020, 8, 24–28. [Google Scholar] [CrossRef]
  65. Le, D.P.; Smith, M.K.; Aitken, E.A.B. An assessment of Pythium spp. associated with soft rot disease of ginger (Zingiber officinale) in Queensland, Australia. Australas. Plant Pathol. 2016, 45, 377–387. [Google Scholar] [CrossRef]
  66. Li, Y.P.; You, M.P.; Barbetti, M.J. Species of Pythium associated with seedling root and hypocotyl disease on common bean (Phaseolus vulgaris) in Western Australia. Plant Dis. 2014, 98, 1241–1247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. McLeod, A.; Botha, W.J.; Meitz, J.C.; Spies, C.F.; Tewoldemedhin, Y.T.; Mostert, L. Morphological and phylogenetic analyses of Pythium species in South Africa. Mycol. Res. 2009, 113, 933–951. [Google Scholar] [CrossRef]
  68. Nechwatal, J.; Oßwald, W.F. Pythium montanum sp. nov., a new species from a spruce stand in the Bavarian Alps. Mycol. Prog. 2003, 2, 73–80. [Google Scholar] [CrossRef]
  69. Paul, B.; Galland, D.; Bhatnagar, T.; Dulieu, H. A new species of Pythium isolated from the Burgundy region in France. FEMS Microbiol. Lett. 1998, 158, 207–213. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  70. Shrestha, S.K.; Zhou, Y.H.; Lamour, K. Oomycetes baited from streams in Tennessee 2010–2012. Mycologia 2013, 105, 1516–1523. [Google Scholar] [CrossRef] [PubMed]
  71. Weiland, J.E.; Beck, B.R.; Davis, A. Pathogenicity and virulence of Pythium species obtained from forest nursery soils on Douglas-fir seedlings. Plant Dis. 2013, 97, 744–748. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  72. Belbahri, L.; McLeod, A.; Paul, B.; Calmin, G.; Moralejo, E.; Spies, C.F.J.; Botha, W.J.; Clemente, A.; Descals, E.; Sánchez-Hernández, E.; et al. Intraspecific and within-isolate sequence variation in the ITS rRNA gene region of Pythium mercuriale sp. nov. (Pythiaceae). FEMS Microbiol. Lett. 2008, 284, 17–27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  73. Bouket, A.C.; Babai-Ahari, A.; Arzanlou, M.; Tojo, M. Morphological and molecular characterization of Phytopythium litorale and Pp. oedochilum from Iran. Nova Hedwig. 2015, 102, 257–270. [Google Scholar] [CrossRef]
  74. Javadi, N.; Sharifnabi, B. Phytopythium litorale, the causal agent of almond root and crown rot in Iran. In Proceedings of the 22nd Iranian Plant Protection Congress, Karaj, Iran, 27–30 August 2016. [Google Scholar]
  75. Nam, B.; Choi, Y.J. Phytopythium and Pythium species (Oomycota) isolated from freshwater environments of Korea. Mycobiology 2019, 47, 261–272. [Google Scholar] [CrossRef] [Green Version]
  76. Redekar, N.R.; Bourret, T.B.; Eberhart, J.L.; Johnson, G.E.; Pitton, B.J.L.; Haver, D.L.; Oki, L.R.; Parke, J.L. The population of oomycetes in a recycled irrigation water system at a horticultural nursery in southern California. Water Res. 2020, 183, 116050. [Google Scholar] [CrossRef]
  77. Rezaei, S.; Abrinbana, M.; Ghosta, Y. Taxonomic and pathogenic characterization of Phytopythium species from West Azarbaijan, Iran, and description of two new species. Mycologia 2021, 113, 612–628. [Google Scholar] [CrossRef] [PubMed]
  78. Lischke, H.; Guisan, A.; Fischlin, A.; Williams, J.; Bugmann, H. Vegetation responses to climate change in the Alps: Modeling studies. In Views from the Alps. Regional Perspectives on Climate Change, 1st ed.; Cebon, P., Dahinden, U., Davies, H., Imboden, D., Jaeger, C.C., Eds.; MIT Press: Cambridge, MA, USA, 1998; pp. 309–350. [Google Scholar]
  79. Jung, T.; Orlikowski, L.; Henricot, B.; Abad-Campos, P.; Aday, A.G.; Aguín Casal, O.; Bakonyi, J.; Cacciola, S.O.; Cech, T.; Chavarriaga, D.; et al. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. For. Pathol. 2016, 46, 134–163. [Google Scholar] [CrossRef] [Green Version]
  80. Pánek, M.; Střížková, I.; Zouhar, M.; Kudláček, T.; Tomšovský, M. Mixed-mating model of reproduction revealed in European Phytophthora cactorum by ddRADseq and effector gene sequence data. Microorganisms 2021, 9, 345. [Google Scholar] [CrossRef] [PubMed]
  81. Pánek, M.; Fér, T.; Mráček, J.; Tomšovský, M. Evolutionary relationships within the Phytophthora cactorum species complex in Europe. Fungal Biol. 2016, 120, 836–851. [Google Scholar] [CrossRef] [PubMed]
  82. Hantula, J.; Lilja, A.; Nuorteva, H.; Parikka, P.; Werres, S. Pathogenicity, morphology and genetic variation of Phytophthora cactorum from strawberry, apple, rhododendron, and silver birch. Mycol. Res. 2000, 104, 1062–1068. [Google Scholar] [CrossRef]
  83. Bhat, R.G.; Colowit, P.M.; Tai, T.H.; Aradhya, M.K.; Browne, G.T. Genetic and pathogenic variation in Phytophthora cactorum affecting fruit and nut crops in California. Plant Dis. 2006, 90, 161–169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Eikemo, H.; Klemsdal, S.S.; Riisberg, I.; Bonants, P.; Stensvand, A.; Tronsmo, A.M. Genetic variation between Phytophthora cactorum isolates differing in their ability to cause crown rot in strawberry. Mycol. Res. 2004, 108, 317–324. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Cooke, D.E.; Drenth, A.; Duncan, J.M.; Wagels, G.; Brasier, C.M. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet. Biol. 2000, 30, 17–32. [Google Scholar] [CrossRef]
  86. Christova, P.; Lyubenova, A.; Kostov, K.; Slavov, S. Diversity and pathogenicity of Phytophthora species, isolated from Osam River. J. Mt. Agric. Balk. 2018, 21, 179–191. [Google Scholar]
  87. Aghighi, S.; Hardy, G.E.S.J.; Scott, J.K.; Burgess, T.I. Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia. Eur. J. Plant Pathol. 2012, 133, 841–855. [Google Scholar] [CrossRef] [Green Version]
  88. Ilieva, E.; Jamart, G.; Kamoen, O. Characterisation of some isolates of Phytophthora cryptogea. Parasitica 1992, 48, 113–122. [Google Scholar]
  89. Meszka, B.; Michalecka, M. Identification of Phytophthora spp. isolated from plants and soil samples on strawberry plantations in Poland. J. Plant Dis. Prot. 2016, 123, 29–36. [Google Scholar] [CrossRef] [Green Version]
  90. Jung, T.; La Spada, F.; Pane, A.; Aloi, F.; Evoli, M.; Horta Jung, M.; Scanu, B.; Faedda, R.; Rizza, C.; Puglisi, I.; et al. Diversity and distribution of Phytophthora species in protected natural areas in Sicily. Forests 2019, 10, 259. [Google Scholar] [CrossRef] [Green Version]
  91. Olson, H.A.; Benson, D.M. Host specificity and variations in aggressiveness of North Carolina isolates of Phytophthora cryptogea and P. drechsleri in greenhouse ornamental plants. Plant Dis. 2013, 97, 74–80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Larsson, M.; Gerhardson, B. Isolates of Phytophthora cryptogea pathogenic to wheat and some other crop plants. J. Phytopathol. 1990, 129, 303–315. [Google Scholar] [CrossRef]
  93. Hansen, E.M.; Reeser, P.W.; Sutton, W. Phytophthora beyond agriculture. Annu. Rev. Phytopathol. 2012, 50, 359–378. [Google Scholar] [CrossRef] [PubMed]
  94. Brasier, C.M.; Cooke, D.E.; Duncan, J.M.; Hansen, E.M. Multiple new phenotypic taxa from trees and riparian ecosystems in Phytophthora gonapodyides–P. megasperma ITS Clade 6, which tend to be high-temperature tolerant and either inbreeding or sterile. Mycol. Res. 2003, 107, 277–290. [Google Scholar] [CrossRef] [PubMed]
  95. Schoebel, C.N.; Stewart, J.; Grünwald, N.J.; Rigling, D.; Prospero, S. Population history and pathways of spread of the plant pathogen Phytophthora plurivora. PLoS ONE 2014, 9, e85368. [Google Scholar] [CrossRef] [Green Version]
  96. Ko, W.H.; Chang, M.S.; Su, H.J. Isolates of Phytophthora cinnamomi from Taiwan as evidence for an Asian origin of the species. Trans. Br. Mycol. Soc. 1978, 71, 496–499. [Google Scholar] [CrossRef]
  97. Jung, T.; Burgess, T.I. Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia 2009, 22, 95–110. [Google Scholar] [CrossRef] [Green Version]
  98. Jung, T.; Scanu, B.; Brasier, C.M.; Webber, J.; Milenković, I.; Corcobado, T.; Tomšovský, M.; Pánek, M.; Bakonyi, J.; Maia, C.; et al. A survey in natural forest ecosystems of Vietnam reveals high diversity of both new and described Phytophthora taxa including P. ramorum. Forests 2020, 11, 93. [Google Scholar] [CrossRef] [Green Version]
  99. Lilja, A.; Rytkönen, A.; Hantula, J.; Müller, M.; Kurkela, T. Phytophthora cactorum, P. ramorum, P. plurivora, Melampsoridium hiratsukamum, Dothiostroma septosporum and Chalara fraxinea, non-native pathogens in Finland. In Proceedings of the 7th Meeting of IUFRO Working Party 7.03.04 Diseases and Insects in Forest Nurseries, Hilo, HI, USA, 13–17 July 2010; pp. 55–62. [Google Scholar]
  100. Laviola, C.; Somma, V.; Evola, C. Present status of Phytophthora species in the Mediterranean area, especially in relation to citrus. EPPO Bull. 1990, 20, 1–9. [Google Scholar] [CrossRef]
  101. Pánek, M.; Střížková, I. A comparison of the virulence of selected Pythium, Globisporangium, Phytopythium and Phytophthora species against strawberry plants. J. Plant Dis. Prot. 2021, 128, 1447–1458. [Google Scholar] [CrossRef]
  102. Sutton, J.C.; Sopher, C.R.; Owen-Going, T.N.; Liu, W.; Grodzinski, B.; Hall, J.C.; Benchimol, R.L. Etiology and epidemiology of Pythium root rot in hydroponic crops: Current knowledge and perspectives. Summa Phytopathol. 2006, 32, 307–321. [Google Scholar] [CrossRef] [Green Version]
  103. Lugauskas, A.; Repečkiene, J.; Uselis, N.; Rašinskiene, A. Problems on a longtime strawberry growing in one plot. Hortum Cultus 2003, 2, 59–68. [Google Scholar]
  104. Rojas, J.A.; Jacobs, J.L.; Napieralski, S.; Karaj, B.; Bradley, C.A.; Chase, T.; Esker, P.D.; Giesler, L.J.; Jardine, D.J.; Malvick, D.K.; et al. Oomycete species associated with soybean seedlings in North America—part I: Identification and pathogenicity characterization. Phytopathology 2017, 107, 280–292. [Google Scholar] [CrossRef] [PubMed]
  105. Zitnick-Anderson, K.K.; Nelson, B.D., Jr. Identification and pathogenicity of Pythium on soybean in North Dakota. Plant Dis. 2015, 99, 31–38. [Google Scholar] [CrossRef] [Green Version]
  106. Granke, L.L.; Hausbeck, M.K. Effects of temperature, concentration, age, and algaecides on Phytophthora capsici zoospore infectivity. Plant Dis. 2010, 94, 54–60. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  107. Littrell, R.H.; McCarter, S.M. Effect of soil temperature on virulence of Pythium aphanidermatum and Pythium myriotylum to rye and tomato. Phytopathology 1970, 60, 704–707. [Google Scholar] [CrossRef]
  108. Grove, G.G.; Madden, L.V.; Ellis, M.A. Splash dispersal of Phytophthora cactorum from infected strawberry fruit. Phytopathology 1985, 75, 611–615. [Google Scholar] [CrossRef]
  109. Ali-Shtayeh, M.S. Taxonomic notes on three Pythium species. Trans. Br. Mycol. Soc. 1986, 86, 659–663. [Google Scholar] [CrossRef]
  110. Zhang, B.Q.; Chen, W.D.; Yang, X.B. Occurrence of Pythium species in long-term maize and soybean monoculture and maize/soybean rotation. Mycol. Res. 1998, 102, 1450–1452. [Google Scholar] [CrossRef]
  111. Zhang, Z.G.; Li, Y.Q.; Fan, H.; Wang, Y.C.; Zheng, X.B. Molecular detection of Phytophthora capsici in infected plant tissues, soil and water. Plant Pathol. 2006, 55, 770–775. [Google Scholar] [CrossRef]
  112. Van Poucke, K.; Haegeman, A.; Goedefroit, T.; Focquet, F.; Leus, L.; Jung, M.H.; Nave, C.; Redondo, M.A.; Husson, C.; Kostov, K.; et al. Unravelling hybridization in Phytophthora using phylogenomics and genome size estimation. IMA Fungus 2021, 12, 16. [Google Scholar] [CrossRef] [PubMed]
  113. Martin, F. Meiotic instability of Pythium sylvaticum as demonstrated by inheritance of nuclear markers and karyotype analysis. Genetics 1995, 139, 1233–1246. [Google Scholar] [CrossRef] [PubMed]
  114. Li, Y.; Shen, H.; Zhou, Q.; Qian, K.; van der Lee, T.; Huang, S. Changing ploidy as a strategy: The Irish potato famine pathogen shifts ploidy in relation to its sexuality. Mol. Plant-Microbe Interact. 2017, 30, 45–52. [Google Scholar] [CrossRef] [PubMed]
  115. Christova, P.K.; Kostov, K.V.; Lyubenova, A.B.; Slavov, S.B. A new hybrid of Phytophthora from Southeast Europe. Mycologia 2021, 113, 734–747. [Google Scholar] [CrossRef]
  116. Sheltzer, J.M.; Blank, H.M.; Pfau, S.J.; Tange, Y.; George, B.M.; Humpton, T.J.; Brito, I.L.; Hiraoka, Y.; Niwa, O.; Amon, A. Aneuploidy drives genomic instability in yeast. Science 2011, 333, 1026–1030. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  117. Shaver, A.C.; Dombrowski, P.G.; Sweeney, J.Y.; Treis, T.; Zappala, R.M.; Sniegowski, P.D. Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 2002, 162, 557–566. [Google Scholar] [CrossRef]
  118. Sniegowski, P.D.; Gerrish, P.J.; Lenski, R.E. Evolution of high mutation rates in experimental populations of E. coli. Nature 1997, 387, 703–705. [Google Scholar] [CrossRef] [PubMed]
  119. Xue, B.K.; Leibler, S. Benefits of phenotypic plasticity for population growth in varying environments. Proc. Natl. Acad. Sci. USA 2018, 115, 12745–12750. [Google Scholar] [CrossRef] [Green Version]
  120. De Cara, M.; Palmero, D.; Durán, C.; Lacasa, C.; Santos, M.; Coffey, M.D.; Tello, J.C. Phytophthora parasitica showing host specificity and pathogenic ability on tomato and sweet pepper. In Microorganisms in Industry and Environment from Scientific and Industrial Research to Consumer Products, 1st ed.; Mendez-Vilas, A., Ed.; World Scientific Publishing Co.: Lisbon, Portugal, 2010; pp. 101–105. [Google Scholar]
  121. Wang, Y.; Meng, Y.; Zhang, M.; Tong, X.; Wang, Q.; Sun, Y.; Quan, J.; Govers, F.; Shan, W. Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity. Mol. Plant Pathol. 2011, 12, 187–201. [Google Scholar] [CrossRef]
  122. McHau, G.R.A.; Coffey, M.D. An integrated study of morphological and isozyme patterns found within a worldwide collection of Phytophthora citrophthora and a redescription of the species. Mycol. Res. 1994, 98, 1291–1299. [Google Scholar] [CrossRef]
  123. Spies, C.F.; Meitz-Hopkins, J.C.; Langenhoven, S.D.; Pretorius, M.C.; McLeod, A. Two clonal lineages of Phytophthora citrophthora from citrus in South Africa represent a single phylogenetic species. Mycologia 2014, 106, 1106–1118. [Google Scholar] [CrossRef] [PubMed]
  124. Pánek, M.; Helmer, Š.; Ali, A. Use of metalaxyl against some soil plant pathogens of the class Peronosporomycetes—A review and two case studies. Plant Prot. Sci. 2022, in press. [Google Scholar] [CrossRef]
Jof 08 00346 g001 550
Figure 1. The correlation between numbers of sampled plants, numbers of isolates of Peronosporales and numbers of species of Peronosporales isolated from symptomatic strawberry plants on the farms in the Czech Republic.
Figure 1. The correlation between numbers of sampled plants, numbers of isolates of Peronosporales and numbers of species of Peronosporales isolated from symptomatic strawberry plants on the farms in the Czech Republic.
Jof 08 00346 g001
Table
Table 1. List of the species of the order Peronosporales isolated in strawberry fields in the Czech Republic.
Table 1. List of the species of the order Peronosporales isolated in strawberry fields in the Czech Republic.
Species NameNo. of Isolates Obtained% of Particular Species
on the Total No. of Isolates
Globisporangium irregulare31.71
Globisporangium ultimum31.71
Phytophthora bilorbang10.57
Phytophthora cactorum11364.57
Phytophthora citrophthora21.14
Phytophthora cryptogea10.57
Phytophthora lacustris10.57
Phytophthora plurivora10.57
Phytopythium citrinum10.57
Phytopythium mercuriale10.57
Phytopythium montanum10.57
Phytopythium vexans52.86
Phytopythium litorale10.57
Pythium aphanidermatum10.57
Pythium conidiophorum10.57
Pythium dissotocum complex2011.43
Pythium heterothallicum31.71
Pythium intermedium42.29
Pythium mamillatum21.14
Pythium nodosum52.86
Pythium perplexum10.57
Pythium rostratifingens10.57
Pythium salpingophorum10.57
Pythium torulosum21.14
Table
Table 2. The numbers and percentages of strawberry farms in the Czech Republic in which P. cactorum and other species of the order Peronosporales were recorded.
Table 2. The numbers and percentages of strawberry farms in the Czech Republic in which P. cactorum and other species of the order Peronosporales were recorded.
Presence of Pythiaceae PathogensNo. of Localities% of Localities
Not any species found717.1
Only P. cactorum found1331.7
Only other species than P. cactorum found922.0
P. cactorum and other species found1229.3
Table
Table 3. Numbers of plant samples, isolates, and species recorded in strawberry farms in the Czech Republic.
Table 3. Numbers of plant samples, isolates, and species recorded in strawberry farms in the Czech Republic.
No.No. of Plantations
with the Given Number of Sampled Plants		No. of Plantations
with the Given Number of Isolates		No. of Plantations
with the Given Number of Species
0077
11820
2279
3143
4340
5010
6211
7220
8110
9101
10110
11210
12010
13010
14300
15500
16100
17200
18300
19300
20200
21010
22100
23000
24110
Table
Table 4. Spearman correlation coefficient r expressing the correlation between the numbers of isolates, species, and sampled plants in strawberry farms.
Table 4. Spearman correlation coefficient r expressing the correlation between the numbers of isolates, species, and sampled plants in strawberry farms.
No. of IsolatesNo. of Species
Identified		No. of Plants
Sampled
No. of isolates1.0000000.7424870.485586
No. of species
identified		0.7424871.0000000.191530
No. of plants
sampled		0.4855860.1915301.000000
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Pánek, M.; Maňasová, M.; Wenzlová, J.; Zouhar, M.; Mazáková, J. Peronosporales Species Associated with Strawberry Crown Rot in the Czech Republic. J. Fungi 2022, 8, 346. https://doi.org/10.3390/jof8040346

AMA Style

Pánek M, Maňasová M, Wenzlová J, Zouhar M, Mazáková J. Peronosporales Species Associated with Strawberry Crown Rot in the Czech Republic. Journal of Fungi. 2022; 8(4):346. https://doi.org/10.3390/jof8040346

Chicago/Turabian Style

Pánek, Matěj, Marie Maňasová, Jana Wenzlová, Miloslav Zouhar, and Jana Mazáková. 2022. "Peronosporales Species Associated with Strawberry Crown Rot in the Czech Republic" Journal of Fungi 8, no. 4: 346. https://doi.org/10.3390/jof8040346

APA Style

Pánek, M., Maňasová, M., Wenzlová, J., Zouhar, M., & Mazáková, J. (2022). Peronosporales Species Associated with Strawberry Crown Rot in the Czech Republic. Journal of Fungi, 8(4), 346. https://doi.org/10.3390/jof8040346

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