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Proceeding Paper

Phytophthora Diversity in a Sentinel Arboretum and in a Nature Reserve Area †

1
Department of Agriculture, Food and Environment, University of Catania, 95123 Catania, Italy
2
Council for Agricultural Research and Economics, Research Centre for Olive, Fruit and Citrus Crops (CREA-OFA), 87036 Rende, Italy
3
Department of Agriculture, Mediterranean University of Reggio Calabria, 89122 Reggio Calabria, Italy
4
Department of Agricultural, Food and Forest Sciences, University of Palermo, 90128 Palermo, Italy
5
Department of Biological, Geological and Environmental Sciences, Catania University, 95125 Catania, Italy
*
Authors to whom correspondence should be addressed.
Presented at the 1st International Electronic Conference on Plant Science, 1–15 December 2020; Available online: https://iecps2020.sciforum.net/.
These authors contributed equally to the study.
Biol. Life Sci. Forum 2021, 4(1), 51; https://doi.org/10.3390/IECPS2020-08748
Published: 1 December 2020
(This article belongs to the Proceedings of The 1st International Electronic Conference on Plant Science)

Abstract

:
Most soilborne Phytophthora species are invasive plant pathogens, and nursery plants for transplanting are considered a primary pathway for the introduction of exotic Phytophthora species into plant diversity conservation sites. As a preliminary contribution to the study of Phytophthora populations in plant conservation sites, we compared the diversity of Phytophthora in the protected natural area Complesso Speleologico Villasmundo S. Alfio Nature Reserve (NR) (Siracusa) and the botanical garden (BG) of the University of Catania, eastern Sicily (Italy). Samplings were carried out in spring 2019. Overall, 29 rhizosphere soil samples were collected, 17 from different types of vegetation in NR and 12 from different plant species in BG. Phytophthora species were recovered from soil samples by leaf baiting and isolation on a selective medium. Isolates were identified by combining morphological features with phylogenetic inferences from ITS-rDNA sequence analysis. Overall, 82 Phytophthora isolates, 30 from NR and 52 from BG, were characterized. Five Phytophthora species, P. pseudocryptogea, P. cryptogea, P. bilorbang, P. plurivora and P. gonapodyides, were recovered from NR, while only three species, P. nicotianae, P. multivora and P. parvispora, were found in BG. Factors contributing to shape Phytophthora populations of rhizosphere soil in these two vegetational contexts are discussed.

1. Introduction

With more than 180 known species and several other informally described provisional taxa [1,2], plant pathogens of Phytophthora genus (Pythiaceae, Peronosporales, Oomycota, Chromista) represent one of the main threats for forests and other ecosystems [3,4,5,6,7,8,9,10]. The genus includes species with a well-known polyphagous attitude, including P. nicotianae [11,12,13] and P. cryptogea [14], as well as pathogens with a restricted host range, such as P. prodigiosa and P. mekongensis [15], two recently described species associated to Citrus in south-eastern Asia [16].
Several studies reported exotic Phytophthora species from non-native regions as invasive pathogens [17,18,19,20,21,22,23,24,25,26]. The introduction of these species in new environments may have destabilizing effects on ecosystems and may threaten the diversity of vegetation and the survival of rare plant species [27,28,29,30]. The movement of plants from nurseries to natural and managed ecosystems represents one of the main pathways of spreading of non-native Phytophthora spp. as well as of their introduction in new environments [31,32,33]. In turn, the finding in forests and natural ecosystems of aggressive Phytophthosa spp., typically associated with cultivated plants, suggests plant diversity conservation sites may be reservoirs of Phytophthora inoculum for crops [29].
In this scenario, the circulation of non-native plants across naturalized and managed ecosystems represents the major means for the conveyance of exotic pests.
In Italy, the presence of some of the most destructive exotic Phytophthora species has been reported from various kinds of ecosystems [14,24,25,34,35,36,37,38,39,40,41,42,43,44]. Due to the polyphagy of these species and their ability to adapt to different environments, their communities in the wild show a great variability [24].
As a preliminary step toward understanding the ecological factors shaping the Phytophthora communities, we compared the diversity of populations of these oomycetes in two different types of plant diversity conservation sites, a nature reserve and a botanical garden in eastern Sicily (southern Italy) which can also be considered an arboretum.

2. Materials and Methods

2.1. Sampling Areas

Two sampling sites from the south east of Sicily, Italy, were selected for this study: (i) a natural reserve (Complesso Speleologico Villasmundo S. Alfio, Regional Natural Reserve—Melilli, Siracusa, Italy) and (ii) a managed semi-natural ecosystem represented by the botanical garden of Catania (Catania, Italy) (Figure 1). The botanical garden contains a living collections of trees partially destinated for scientific study; therefore, it can also be defined as arboretum. Sampling activities were carried out during the spring of 2019.

2.2. Sampling and Phytophthora Isolation

In total, 29 rhizosphere soil samples were examined (Table 1), 17 from both mature trees and herbaceous plants of the main vegetational types present in the nature reserve (total area ca. 71.7 ha) and 12 collected from 12 diverse trees in the botanical garden (total area ca 1.6 ha). Nine out of these twelve plants were exotic. In both sites, plants were sampled irrespective of the presence of symptoms.
Soil sampling and isolation were performed in accordance with Jung et al. [45]: four soil cores were collected under each tree or shrub, 50–150 from the rhizosphere cm away from the stem base, and rhizosphere soil from all four cores were bulked together (volume of each sample about 1 L).
For each sample, subsamples of 400 mL were used for baiting tests that were performed in a walk-in growth chamber with 12 h natural daylight at 20 °C. Young leaves of C. siliqua and Quercus spp. floated over flooded soil were used as baits. After 24–48 h incubation, necrotic segments (2 × 2 mm) from symptomatic leaves were plated in Petri dishes onto selective PARPNH-agar medium [46]. Petri dishes were incubated at 20 °C in the dark. Outgrowing Phytophthora hyphae were transferred onto V8-juice agar (V8A) under the stereomicroscope. All the Phytophthora isolates were maintained on V8-agar in the dark at temperature of 6 °C.

2.3. Morphological Characterization of Isolates

Cultures of seven days, grown on V8A at 20 °C in the dark, were used to group all isolates into morphotypes on the basis of their colony growth patterns. For each host-plant and plant community, the different morphological types were labelled with progressive numbering (Roman numbering); then, isolates belonging to the same sampling hosts have been tagged with the relative type number.
Moreover, morphological features of chlamydospores, sporangia, oogonia, antheridia and hyphal swellings, were carefully analyzed and compared with species descriptions in the literature [3,20,25,47].

2.4. Molecular Identification of Isolates

The DNA of the pure cultures of isolates obtained from soil was extracted by using PowerPlant® Pro DNA isolation Kit (MO BIO Laboratories, Inc., Carlsbad, CA, USA), following the manufacturer’s protocol. The DNA was preserved at −20 °C. The identification of Phytophthora species was performed by the analysis of Internal Transcribed Spacer (ITS) regions of ribosomal DNA (rDNA). DNA was amplified using forward primers ITS6 (5′-GAAGGTGAAGTCGTAACAAGG-3′) [48] and reverse primer ITS4 (5′-TCCTCCGCTTATTGATATGC-3′) [49]. The PCR amplification mix and thermocycler conditions were in accordance with Cooke et al. [48]. All PCRs were carried out in a 25 µL reaction mix containing PCR Buffer (1x), dNTP mix (0.2 mM), MgCl2 (1.5 mM), forward and reverse primers (0.5 mM each), Taq DNA Polymerase (1 U) and 100 ng of DNA. The thermocycler conditions were as it follows: 94 °C for 3 min; followed by 35 cycles of 94 °C for 30 s, 55 °C for 30 s, and 72 °C for 30 s; and then 72 °C for 10 min.
Amplicons were detected in 1% agarose gel and sequenced in both directions by an external service (Amsterdam, The Netherlands). Derived sequences were analyzed using FinchTV v.1.4.0 [50]. For species identification, blast searches in GenBank [51], in a local database containing sequences of ex-type or key isolates from published studies and in Phytophthora Database [52] were performed. Isolates were assigned to a species when their sequences were at least 99–100% identical to a reference isolate.

2.5. Soil Analysis and USDA Classification

Additional soil from the rhizosphere of the same plants sampled for the analysis of diversity of Phytophthora spp. was analyzed to determinate the following properties: pH-H2O, electrical conductivity at 25 °C, organic matter content, nitrates and soil texture (Table 2). The soil analyses were performed by an external service (Progetto Ambiente & C. s.a.s., Catania, Italy) following the “Official method of soil chemical analysis” in accordance with standard protocols defined by D.M. 13/09/1999, G.U. No. 248, 21/10/99 and D.M. 25/03/2002, G.U. No. 84, 10/04/2002.
The soil texture of each sample was determinated on the basis of the USDA classification method [53]. The percentage of each soil component (sand, clay and silt) has been used in order to assign each sample to a textural class.

3. Results

3.1. Composition of Phytophthora Communities

Thirteen out of 29 rhizosphere soil samples (six from the natural reserve and seven from the botanical garden) processed by baiting revealed the occurrence of Phytophthora species in both the surveyed sites. Overall, 82 Phytophthora isolates (30 from the natural reserve and 52 from the botanical garden) were obtained. Morphological and ITS sequence analyses made it possible to identify eight Phytophthora species (Table 2); in detail, P. bilorbang, P. cryptogea, P. gonapodyides, P. plurivora and P. pseudocryptogea were recovered in the nature reserve, while only three species, namely P. nicotianae, P. multivora and P. parvispora, were found in the botanical garden.
Baiting of rhizosphere soil samples from the natural reserve revealed the occurrence of 5 Phytophthora from six mature trees belonging to five plant species (Table 2). A single Phytophthora sp. was recovered from each sample. Phytophthora pseudocryptogea and P. cryptogea were the only species isolated from willow trees (Salix pedicellata), P. bilorbang was recorded from Platanus orientalis and P. plurivora from a mature specimen of evergreen oak (Q. ilex). Finally, P. gonapodyides was isolated both from Q. ilex and Q. pubescens s. l.
Overall, three Phytophthora species were isolated from seven out of 12 plant species from the botanical garden (Table 2). Phytophthora nicotianae and P. multivora occurred together from mature trees of Araucaria cokii, Phytolacca dioica, Q. suber and O. europaea. In addition, P. multivora was exclusively isolated from Sterculia diversifolia and from Zelkowa sicula. Finally, P. parvispora was isolated from Coffea arabica.

3.2. Analysis of Soil

Results of soil analysis are schematically summarized in Table 2.
In the natural reserve, values of soil pH ranged from 7.0 (Platanus orientalis—NR_1903_S3) to 7.7 (Salix pedicellata—NR_1903_S2); values of 7.5 were reported in soils from Cynara cardunculus (NR_1903_S6) and Asphodelus sp. (NR_1903_S7); with reference to the electrical conductivity at 25 °C obtained results showed an high variability, with values ranging from 796 ± 41 µS/cm (Pistacia lentiscus—NR_1903_S16) to 1617 ± 53 µS/cm (Q. ilex—NR_1903_S9). Five main soil textures were reported from the reserve: 1. sandy clay loam, from both sampled S. pedicellata (NR_1903_S1 and _S2), from P. orientalis (NR_1903_S4) and from the mixed soil sample of Pistacia lentiscus and Pyrus sp. (NR_1903_S15); 2. sandy clay, from P. orientalis (NR_1903_S3), Euphorbia dendroides (NR_1903_S5), Cynara cardunculus (NR_1903_S6), Asphodelus sp. (NR_1903_S7), Sarcopoterium spinosum (NR_1903_S12 and _S13) and P. lentiscus (NR_1903_S14, _S16 and S17); 3. clay loam, from Q. ilex (NR_1903_S8) and Quercus pubescens s. l. (NR_1903_S11); 4. sandy loam (Q. ilex—NR_1903_S10); 5. loamy sand (Q. ilex—NR_1903_S9). Similarly to the electrical conductivity, values of the content in nitrates had a high variability, ranging from 1.6 ± 0.2 mg/kg in soil of S. pedicellata (NR_1903_S2) to 17.0 ± 2 mg/kg in that of Q. ilex (NR_1903_S9). Finally, the content in organic matter was above the 25% in all the analyzed samples, with the highest value (21%) in the soil of one of the sampled Q. ilex (NR_1903_S9).
In the botanical garden, the values of soil pH in the majority of samples ranged from 7.99 (Eucalyptus citridora—BG_1903_S1) to 8.64 (P. lentiscus—BG_1903_S11); values under this range were observed only in soil from Pistacia atlantica—BG_1903_S5 (7.43) and Olea europaea—BG_1903_S10 (7.1). The electrical conductivity at 25 °C ranged mainly from 677.5 ± 50 µS/cm (Coffea arabica—BG_1903_S12) to 997.5 ± 43 µS/cm (Phytolacca dioica—BG_1903_S4); values in the range 1000–2000 µS/cm were recorded in the soil of O. europaea (BG_1903_S10) and Sterculia diversifolia (BG_1903_S8); finally, values above 3000 µS/cm were in the soil from Araucaria cooki (BG_1903_S2) and P. atlantica (BG_1903_S5). Four main soil textures were reported from the botanical garden: 1. loamy sand in soil from Grevillea robusta (BG_1903_S3), P. atlantica (BG_1903_S5), Quercus suber (BG_1903_S6) and Coffea arabica (BG_1903_S12); 2. sandy loam in soil from A. cooki (BG_1903_S2) and P. lentiscus (BG_1903_S11); 3. sandy clay loam in soil from P. dioica (BG_1903_S4), Zelkova sicula (BG_1903_S7) and O. europaea (BG_1903_S10); 4. clay loam in soil from S. diversifolia (BG_1903_S8) and Mangifera indica (BG_1903_S9). The values of the content in nitrates were mainly in the range 41–188.2 mg/kg: values in the range 1000–1400 mg/kg were observed for P. atlantica, A. cooki and S. diversifolia. Finally, the content in organic matter was under the 1.5% in all the soil samples.

4. Discussion

The number of Phytophthora species recovered from the rhizosphere soil of vegetation in the nature reserve was higher than the number of species recovered from rhizosphere soil of eight exotic and four native woody plants grown in the botanical garden. This may have been due to the different extension of the two surveyed sites. Very probably in the botanical garden of the University of Catania the presence in a restricted area of different potential woody host-plants grown in close proximity to each other favored the spread and prevalence of invasive as well polyphagous Phytophthora species, such as P. multivora and P. nicotianae. In most cases, these two species were isolated together from the same sample. Conversely, in the nature reserve of Villasmundo the presence of different vegetational types and peculiar ecological niches may have favored the diversity of Phytophthora community even in a relatively restricted area. This is exemplified by P. bilorbang, a typically aquatic species that only occasionally behaves as an opportunistic plant pathogen [25]. In the Complesso Speleologico Villasmundo S. Alfio, Regional Nature Reserve, P. bilorbang was isolated from the riparian vegetation associated with a water course.
The widespread occurrence of Phytophthora species in soils with different physico-chemical characteristics in both surveyed sites confirms the ability of these oomycetes to adapt to different environments and thrive in a wide range of ecological conditions [2,26,27,36,54,55]. Previous studies of other Authors demonstrated a correlation between soil characteristics and the impact of P. cinnamomi on forest vegetation [56]. However, it would be more difficult to demonstrate the effects of soil characteristics and other environmental factors on complex Phytophthora communities composed by several species with diverse ecological requirements and behaviors. Several recent studies addressing the diversity of Phytophthora communities in natural and semi-natural ecosystems grouped Phytophthora species on the basis of their life style and habitat, distinguishing between soil-inhabitant and preferentially aquatic species [2,24,26,54,57,58]. In this study, both types were isolated from soil samples collected in the Complesso Speleologico Villasmundo S. Alfio, Regional Nature Reserve while only typically soil-borne species were recovered from the botanical garden of the University of Catania. The species recovered from the largest number of host-plants in this site was P. multivora, which is regarded as an emerging plant pathogen worldwide and in particular a major pathogen of woody plants in urban environments in Australia [59,60]. In recent years, much attention has been paid to Phytophthora communites in natural and semi-natural ecosystems worldwide. Conversely, only few studies addressed the problem of Phytophthora spp. in botanical gardens, including arboreta. Yet, the presence or introduction of Phytophthora spp. in these sites can be a threat for the survival of rare plant species and have serious implications for the in situ conservation of plant diversity. Moreover, it has been recently stressed the potential role of botanical gardens and arboreta as sentinel sites for early detection of new tree diseases [37,61,62,63,64,65,66].

5. Conclusions

This study revealed the presence of several Phytophthora species in soil of plant diversity conservation sites. Most of these species are aggressive plant pathogens and two of them in particular P. multivora and P. nicotianae are invasive and polyphagous. This may explain why they were so widespread and prevailed over other species in a site with uniform and conducive environmental conditions. However, it cannot be ruled out that the predominance of these species was due, at least in part to the isolation method. Methods based on leaf baiting have the advantage of recovering living and culturable isolates, but could have the disadvantage to isolate some Phytophthora species selectively or preferentially. This limit can be excluded using in parallel detection methods based on next-generation sequencing (NGS) technology which are more sensitive to detecting Phytophthora species in environmental samples and are less influenced by environmental conditions [28,65]. NGS-based methods can help the fine tuning of studies aimed at exploring the complexity of Phytophthora communities in different ecosystems and the effects of ecological factors driving the diversity and the structure of these communities.

Supplementary Materials

The poster presentation is available online at https://www.mdpi.com/article/10.3390/IECPS2020-08748/s1.

Author Contributions

Conceptualization, S.O.C., F.L.S., F.A. and M.R.; methodology, A.P., E.S., F.L.S., F.A., M.R., G.G.d.G. and S.O.C.; analysis of results, F.L.S. and S.O.C.; resources, S.O.C. and A.P.; original—draft preparation, M.R., F.L.S. and S.O.C.; editing, S.O.C., F.A., M.R. and F.L.S.; supervision, S.O.C., G.G.d.G., A.P. and E.S. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

This research was funded by “MIUR-FFABR 2017” of S.O.C., grant number 5A725192051; University of Catania, “project DIFESA” of S.O.C., grant number 5A722192134, by the Ministry of Science and Innovation (PID2019-108070RB-100) of S.O.C. and A.P.; F.L.S. was supported by a Ph.D. fellowship funded by “PON Ricerca e Innovazione” 2014–2020 (CCI2014IT16M2OP005); M.R. has been granted a fellowship by CREA “OFA” (Rende), this study is part of his activity as PhD, Doctorate “Agricultural, Food, and Forestry Science”, University Mediterranea of Reggio Calabria, XXXV cycle. The authors wish to thank the director of CUTGANA (Protected Area Management), University of Catania, Giovanni Signorello, and the manager of the Regional Nature Reserve, Elena Amore, for their support and helpful assistance. The Authors are grateful to Ann Davies for the English revision of the text.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

The following abbreviations are used in this manuscript: MDPI: Multidisciplinary Digital Publishing Institute; DOAJ: Directory of open access journals; TLA: Three letter acronym; LD: linear dichroism.

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Figure 1. Geographical location of the surveyed areas included in this study.
Figure 1. Geographical location of the surveyed areas included in this study.
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Table 1. Geographic localization of the 29 soil samples in nature reserve and botanical garden and plant species sampled.
Table 1. Geographic localization of the 29 soil samples in nature reserve and botanical garden and plant species sampled.
Sampling SiteRhizosphere Soil Sample IDLocation—Municipality and Geographic Coordinates (DATUM WGS84)Plant Species
Complesso Speleologico Villasmundo S. Alfio Regional Nature ReserveNR_1903_S1Melilli—37°13′17.54″ N; 15°6′19.52″ ESalix pedicellata
NR_1903_S2Melilli—37°13′17.66″ N; 15°6′19.28″ ES. pedicellata
NR_1903_S3Melilli—37°13′17.753″ N; 15°6′18.93″ EPlatanus orientalis
NR_1903_S4Melilli—37°13′17.86″ N; 15°6′18.81″ EP. orientalis
NR_1903_S5Melilli—37°13′17.25″ N; 15°6′15.30″ EEuphorbia dendroides
NR_1903_S6Melilli—37°13′17.48″ N; 15°6′15.31″ ECynara cardunculus
NR_1903_S7Melilli—37°13′17.60″ N; 15°6′15.30″ EAsphodelus sp.
NR_1903_S8Melilli—37°13′11.75”N; 15° 6′1.20″ EQuercus ilex
NR_1903_S9Melilli—37°13′11.00″ N; 15°5′59.69″ EQ. ilex
NR_1903_S10Melilli—37°13′10.93″ N; 15°5′59.95″ EQ. ilex
NR_1903_S11Melilli—37°13′11.788″ N; 15°6′0.547″ EQ. pubescens sensu latu
NR_1903_S12Melilli—37°13′17.52″ N; 15°6′7.94″ ESarcopoterium spinosum
NR_1903_S13Melilli—37°13′17.50″ N; 15°6′8.57″ ES. spinosum
NR_1903_S14Melilli—37°13′17.28″ N; 15°6′4.77″ EPistacia lentiscus
NR_1903_S15Melilli—37°13′17.50″ N; 15°6′5.13″ EP. lentiscus + Pyrus sp., mixed sample
NR_1903_S16Melilli—37°13′16.94″ N; 15°6′7.66″ EP. lentiscus
NR_1903_S17Melilli—37°13′16.93″ N; 15°6′6.24″ EP. lentiscus
Botanical garden of CataniaBG_1903_S1Catania—37°30′57.29″ N; 15°5′2.27″ EAraucaria cokii
BG_1903_S2Catania—37°30′55.92″ N; 15°5′1.95″ EPhytolacca dioica
BG_1903_S3Catania—37°30′55.08″ N; 15°4′59.75″ EGrevillea robusta
BG_1903_S4Catania—37°30′57.56″ N; 15°5′1.47″ EPistacia atlantica
BG_1903_S5Catania—37°30′57.47″ N; 15°5′0.81″ ESterculia diversifolia
BG_1903_S6Catania—37°30′57.69″ N; 15°5′1.80″ EEucalyptus citridora
BG_1903_S7Catania—37°30′53.46″ N; 15°5′2.38″ EZelkowa sicula
BG_1903_S8Catania—37°30′53.35″ N; 15°5′1.89″ EQ. suber
BG_1903_S9Catania—37°30′53.19″ N; 15°5′2.42″ EOlea europea
BG_1903_S10Catania—37°30′53.34″ N; 15°5′2.40″ EPistacia lentiscus
BG_1903_S11Catania—37°30′57.92″ N; 15°5′0.74″ ECoffea arabica
BG_1903_S12Catania—37°30′57.95″ N; 15°5′0.86″ EMangifera indica
Table 2. Phytophthora spp. recovered from plant rhizosphere and physico-chemical soil properties in samples collected in two different plant diversity conservation sites (Nature Reserve and Arboretum).
Table 2. Phytophthora spp. recovered from plant rhizosphere and physico-chemical soil properties in samples collected in two different plant diversity conservation sites (Nature Reserve and Arboretum).
Sampling SiteRhizosphere Soil Sample ID.HostBaited Phytophthora spp. aSoil Properties
pHElectrical Conductivity at 25 °C (μS/cm)Soil TextureNitrates (mg/kg)Organic Matter (%)
Complesso Speleologico Villasmundo S. Alfio Regional Nature ReserveNR_1903_S1Salix pedicellataPSC7.6 ± 0.11497.0 ± 49Sandy clay loam11.0 ± 16.5 ± 0.3
NR_1903_S2S. pedicellataCRY7.7 ± 0.1938.0 ± 43Sandy clay loam1.6 ± 0.22.8 ± 0.1
NR_1903_S3Platanus orientalis-7.0 ± 0.1913.0 ± 43Sandy clay7.1 ± 0.74.9 ± 0.2
NR_1903_S4P. orientalisBIL7.1 ± 0.11023.0 ± 44Sandy clay loam6.9 ± 0.75.4 ± 0.3
NR_1903_S5Euphorbia dendroides-7.3 ± 0.1976.0 ± 44Sandy clay5.9 ± 0.67.1 ± 0.4
NR_1903_S6Cynara cardunculus-7.5 ± 0.1822.0 ± 41Sandy clay7.3 ± 0.75.5 ± 0.3
NR_1903_S7Asphodelus sp.-7.5 ± 0.11122.0 ± 45Sandy clay7.2 ± 0.75.4 ± 0.3
NR_1903_S8Quercus ilexGON7.3 ± 0.11463.0 ± 48Clay loam13.0 ± 113.1 ± 0.7
NR_1903_S9Q. ilexPLU7.4 ± 0.11617.0 ± 53Loamy sand17.0 ± 221.0 ± 1
NR_1903_S10Q. ilex-7.6 ± 0.11397.0 ± 46Sandy loam11.0 ± 116.3 ± 0.8
NR_1903_S11Q. pubescens sensu latuGON7.2 ± 0.11174.0 ± 45Clay loam11.0 ± 111.4 ± 0.6
NR_1903_S12Sarcopoterium spinosum-7.2 ± 0.1922.0 ± 42Sandy clay6.1 ± 0.55.1 ± 0.2
NR_1903_S13S. spinosum-7.3 ± 0.11102.0 ± 49Sandy clay7.1 ± 0.74.2 ± 0.1
NR_1903_S14Pistacia lentiscus-7.4 ± 0.1831.0 ± 41Sandy clay6.7 ± 0.78.2 ± 0.4
NR_1903_S15P. lentiscus + Pyrus sp., mixed sample-7.2 ± 0.1856.0 ± 43sandy clay loam5.3 ± 0.77.2 ± 0.2
NR_1903_S16P. lentiscus-7.3 ± 0.1796.0 ± 41Sandy clay1.7 ± 0.27.7 ± 0.4
NR_1903_S17P. lentiscus-7.3 ± 0.11056.0 ± 44Sandy clay3.6 ± 0.48.7 ± 0.4
Botanical garden of Catania (Arboretum)BG_1903_S1Eucalyptus citridoraMUL, NIC7.99 ± 0.1877.5 ± 48Loamy sand145.3 ± 0.41.07 ± 0.2
BG_1903_S2Araucaria cookiMUL, NIC8.19 ± 0.13437.5 ± 46Sandy loam1210.9 ± 0.61.29 ± 0.1
BG_1903_S3Gravillea robusta-8.14 ± 0.1852.5 ± 40Loamy sand145.3 ± 0.60.86 ± 0.1
BG_1903_S4Phytolacca dioica-8.26 ± 0.1997.5 ± 43Sandy clay loam188.2 ± 0.71.01 ± 0.1
BG_1903_S5Pistacia atlanticaMUL7.43 ± 0.13945.0 ± 45Loamy sand1076.6 ± 0.11.49 ± 0.1
BG_1903_S6Quercus suber-8.14 ± 0.1765.0 ± 45Loamy sand45.3 ± 0.21.48 ± 0.2
BG_1903_S7Zelkova siculaMUL8.55 ± 0.1970.0 ± 44Sandy clay loam103.9 ± 0.80.73 ± 0.1
BG_1903_S8Sterculia diversifoliaMUL, NIC8.10 ± 0.11675.0 ± 48Clay loam1366.6 ± 1.00.11 ± 0.05
BG_1903_S9Mangifera indicaMUL, NIC8.60 ± 0.1765.0 ± 41Clay loam176.7 ± 0.41.0 ± 0.1
BG_1903_S10Olea europaea-7.10 ± 0.11540.0 ± 43Sandy clay loam55.3 ± 0.40.66 ± 0.1
BG_1903_S11Pistacia lentiscusPAR8.64 ± 0.1867.5 ± 46Sandy loam148.2 ± 0.50.99 ± 0.1
BG_1903_S12Coffea arabica-8.40 ± 0.1677.5 ± 50Loamy sand41.0 ± 0.30.82 ± 0.1
a BIL = P. bilorbang; CRY = P. cryptogea; GON = P. gonapodyides; MUL = P. multivora; NIC = P. nicotianae; PLU = P. plurivora; PSC = P. pseudocryptogea; PAR = P. parvispora.
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Riolo, M.; La Spada, F.; Aloi, F.; Giusso del Galdo, G.; Santilli, E.; Pane, A.; Cacciola, S.O. Phytophthora Diversity in a Sentinel Arboretum and in a Nature Reserve Area. Biol. Life Sci. Forum 2021, 4, 51. https://doi.org/10.3390/IECPS2020-08748

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Riolo M, La Spada F, Aloi F, Giusso del Galdo G, Santilli E, Pane A, Cacciola SO. Phytophthora Diversity in a Sentinel Arboretum and in a Nature Reserve Area. Biology and Life Sciences Forum. 2021; 4(1):51. https://doi.org/10.3390/IECPS2020-08748

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Riolo, Mario, Federico La Spada, Francesco Aloi, Giampietro Giusso del Galdo, Elena Santilli, Antonella Pane, and Santa Olga Cacciola. 2021. "Phytophthora Diversity in a Sentinel Arboretum and in a Nature Reserve Area" Biology and Life Sciences Forum 4, no. 1: 51. https://doi.org/10.3390/IECPS2020-08748

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