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BY-NC-ND 3.0 license Open Access Published by De Gruyter Open Access November 16, 2016

Ectomycorrhizal communities in a Tuber aestivum Vittad. orchard in Poland

  • Dorota Hilszczańska EMAIL logo , Hanna Szmidla , Jakub Horak and Aleksandra Rosa-Gruszecka
From the journal Open Life Sciences

Abstract

Cultivation of the Burgundy truffle, Tuber aestivum Vittad., has become a new agricultural alternative in Poland. For rural economies, the concept of landscaping is often considerably more beneficial than conventional agriculture and promotes reforestation, as well as land-use stability. Considering examples from France, Italy, Hungary and Spain, truffle cultivation stimulates economic and social development of small, rural communities. Because there is no long tradition of truffle orchards in Poland, knowledge regarding the environmental factors regulating the formation of fruiting bodies of T. aestivum is limited. Thus, knowledge concerning ectomycorrhizal communities of T. aestivum host species is crucial to ensuring successful Burgundy truffle production. We investigated the persistence of T. aestivum ectomycorrhizae on roots of hazel (Corylus avellana L.) and oak (Quercus robur L.) and checked the host-species influence on community structure of ectomycorrhizal fungi. The study was conducted in an experimental plantation located in eastern Poland and established in 2008. We demonstrated that the number of fungal taxa was not significantly different between oak and hazel. However, the species composition differed between these two host trees. During the three-year study, we observed that species richness did not increase with the age of the plantation.

1 Introduction

Burgundy truffle (Tuber aestivum Vittad.) is an ectomycorrhizal fungus that forms edible hypogeous ascocarps of considerable economic value. It is well-documented in literature that T aestivum grows in an ectomycorrhizal symbiosis with many different trees and shrubs belonging to genera such as Carpinus, Fagus, Tilia, Populus, Quercus and Corylus [13].

Cultivation of the fungus is starting to become a promising agroforestry alternative for rural areas in Poland. For a long time, truffles, especially the species praised by chefs and gourmets for their scent and taste, were considered rare in Poland, and the Burgundy truffle was recorded only once after the Second World War [4]. In the last decade, new data on the distribution of T aestivum and other species of truffles have been reported from Poland [5,6], as well as from other countries of Central, Eastern and Northern Europe [711].

The persistence of truffle ectomycorrhizae on inoculated seedlings outplanted in the field is one of the most important factors of truffle cultivation success [1214]. However, in many cases, the targeted truffle ectomycorrhizae is replaced by other competitive ectomycorrhizal species [15,16]. Understanding the conditions that promote truffle fructification is essential for detecting species that have a high possibility of outcompeting targeted truffles [16]. Knowledge about the diversity of species is crucial for successful conservation efforts and future plantation management. Comparison of the ectomycorrhizal fungi that are associated with different host species within environments with the same conditions would help clarify the importance of host preference in structuring the ectomycorrhizal community [17].

The aims of our study were i) to examine whether and how differently T aestivum mycorrhizae persist in roots of hazel (Corylus avellana L.) and oak (Quercus robur L.), ii) to characterize other (non-Tuber) species present in the orchard, and iii) to estimate, based on the ectomycorrhizal fungi community (ECM), the future T aestivum fructification in the orchard.

2 Materials and Methods

2.1 Study area

The study was conducted in a plantation located in eastern Poland (latitude 51° 8’ 51”; longitude 23° 28’ 29”) at 200 m a.s.l. where the soil parent material is Triassic Muschelkalk. The climate is continental with a mean annual rainfall of 550 mm and mean annual temperature of 8.0°C. The truffle orchard was established in 2008 by planting 134 seedlings of Quercus robur and 150 seedlings of Corylus avellana, all of which were inoculated with spores of native Tuber aestivum [18]. The soil physical and chemical properties are shown in Table 1 and were similar in all areas of the orchard.

Table 1

Physical and chemical properties of the soil in the plantation

Measured parameter
Sand (0.2-0.063 mm) %32.62
Clay (0.002 mm) %35.29
Silt (0.063-0.002 mm) %32.09
P205 g kg-12.52
Calcium cmol+kg127.96
Magnesium cmol+kg10.32
Potassium cmol+kg10.60
water pH7.6
CaCO3 %19.56
Organic matter %2.3
C/N24.3

The experimental plantation of 0.44 ha was established on land that had been abandoned for 19 years prior to outplanting of seedlings inoculated with of T. aestivum. Before outplanting of seedlings, the soil was ploughed to a depth of 50 cm to promote deep soil aeration, and superficial tilling with several passes was later applied to remove herbaceous vegetation. The site was chosen because truffle species, such as Tuber rufum and T excavatum, had been found in the forest surrounding the area. This forest was mainly composed of Q. robur, Carpinus betulus and Populus tremula, with C. avellana in the understorey. Seedlings were arranged with 3 m between the rows and 4.5 between individuals within the rows. Green woven polypropylene fabrics (99 g m-2) were used in rows for reducing herbaceous cover in this plantation. In order to control the rapid growth of weeds, soil tilling with cultivator tines set at 15 cm depth and manual weed control with a hoe were performed every year - namely, in May and in August or September, depending on weed growth.

2.2 Sampling and morphological analyses

To analyse the ectomycorrhizal morphotypes present in root tips, five hazel trees and five oaks were randomly chosen (every year, analyses of mycorrhizae were performed on the same chosen trees). Three soil cores (6 cm diameter, 20 cm deep) were obtained 25 cm from the base of each tree. These three cores per tree were combined to yield a single composite sample. The samples were collected every year of the study (2012-2014), in September. Each composite sample was individually soaked overnight in tap water and sieved to separate the root fragments and ectomycorrhizae (ECM) from the soil. The clean roots were placed in Petri dishes filled with water. Only vital roots (identified as swollen, without root hair or covered by fungal mantles) were considered ECM-colonized roots. The different types of ectomycorrhizae found in each sample were morphotyped using a stereomicroscope and a light microscope, with the anatomo-morphological characteristics described by Agerer [19,20] and two online databases, EctoMycorrhizal Community DataBase (www.emyco.uniss.it) and DEEMY (http://www.deemy.de), as references [21,22].

Morphotypes were identified by colour and shape of the mycorrhiza, characteristics of the mantel surface, ramification system, and presence and structure of rhizomorphs, emanating hyphae and other elements. The morphology and colour of the ECMs were evaluated with a dissecting microscope on freshly isolated ectomycorrhizal tips. The ectomycorrhizae formed by T. aestivum were identified by its ochreous and chestnut brown colour and by the presence of swollen fine roots with tips embedded in radially twisted hyphae. The number of living mycorrhizae of each morphotype was recorded separately for each sample. Roots were cut into 2-cm pieces and a total of 100 vital tips were counted.

2.3 Data analysis

The diversity of ectomycorrhizae on hazel and oak was expressed as the number of identified ectomycorrhizal species (species richness). The relative abundance of each morphotype (number of root tips of each morphotype / total number of mycorrhizae) was calculated separately for each sample. Ecological indicators, such as species richness, Shannon diversity index and Simpson dominance index, were calculated using EcoComPaC Version 1 [23] (http://prf.osu.cz/kbe/dokumenty/sw/ ComEcoPaC/ComEcoPaC.xls) in Excel.

Statistical analyses were performed in Estimates 8.2. and CANOCO 4.5. We focused on predictors that were testable only within a limited spatial scale. Unreplicated treatments were the only option for our study [24]. We controlled this problem by using randomized techniques for taxa richness data [25], as recommended and used elsewhere [2628].

For the analysis of species richness and for comparisons between tree species and over time, we used sample-based species rarefactions (Mao Tau function) with 95% confidence intervals [29]. The number of randomizations was set at 1,000 in Estimates.

Data on species composition were log transformed. The length of the gradient in detrended correspondence analysis (DCA) was lower than 3. Redundancy analysis (RDA), instead of canonical correspondence analysis (CCA), is often considered an appropriate method for shorter gradient lengths [30]. However, RDA is inappropriate for abundance data involving null abundances [31]; hence, CCA was used as the most appropriate method for analyses of species composition. CCA was computed using a randomized (9,999 randomizations) split-plot design in CANOCO.

3 Results

In all tested oak and hazel samples, mycorrhizal colonization was nearly 100%. Very small proportions of distorted root tips were omitted in the laboratory analysis.

Morphological observations revealed a total of 14 fungal taxa: 10 in oak and 10 in hazel (Table 2 and Fig. 1 a-n). Of these, one was assigned at the order level (Pezizales), seven at the genus level (Inocybe sp., Lactarius sp. 1, Lactarius sp. 2, Tomentella sp., Geopora sp., Peziza sp. and Alnicola sp.) and five at the species level (Tuber aestivum, Amphinema byssoide, Cenococcum geophilum, Scleroderma areolatum, Laccaria tortilis and Thelephora terrestris). In our study, T. aestivum ectomycorrhizae were present in all 3 years.

Table 2

Relative abundance (%) of ectomycorrhizal taxa associated with roots of oak (Quercus robur L.) and hazel (Corylus avellana L.) in Tuber aestivum plantations in Chełm.

Relative abundance of mycorrhizal fungal taxa
Taxa of mycorrhizal fungi201220132014
OakHazelOakHazelOakHazel
Tuber aestivum35.8117.0732.6048.4133.9643.18
Inocybe sp.37.080.0049.800.0064.690.00
Lactarius sp. 10.0027.990.000.000.000.00
Lactarius sp. 27.640.000.000.000.000.00
Amphinema byssoides1.470.000.000.000.000.00
Cenococcum geophilum6.610.000.000.001.3531.59
Scleroderma areolatum3.201.400.000.000.000.00
Geopora sp.2.970.000.000.000.000.00
Tomentella sp.2.943.3613.800.000.0013.18
Laccaria tortilis2.270.000.000.000.000.00
Peziza sp.0.005.743.800.000.000.00
Pezizales sp.0.0036.320.000.000.000.00
Thelephora terrestris0.008.120.0048.860.0012.05
Alnicola sp.0.000.000.002.730.000.00
Figure 1 Plan views of mycorrhizae observed on hazel (Corylus avellana L.) and oak(Quercus robur L.) from Tuber aestivum plantations in Chełm; Tuber aestivum (a), Inocybe sp. (b), Lactarius sp. 1 (c), Lactarius sp. 2 (d), Amphinema byssoides (e), Cenococcum geophilum (f), Scleroderma areolatum (g), Geopora sp. (h), Tomentella sp. (i), Laccaria tortilis (j), Peziza sp. (k), Pezizales sp. (l), Thelephora terrestris (m), and Alnicola sp. (n).
Figure 1

Plan views of mycorrhizae observed on hazel (Corylus avellana L.) and oak(Quercus robur L.) from Tuber aestivum plantations in Chełm; Tuber aestivum (a), Inocybe sp. (b), Lactarius sp. 1 (c), Lactarius sp. 2 (d), Amphinema byssoides (e), Cenococcum geophilum (f), Scleroderma areolatum (g), Geopora sp. (h), Tomentella sp. (i), Laccaria tortilis (j), Peziza sp. (k), Pezizales sp. (l), Thelephora terrestris (m), and Alnicola sp. (n).

The overall species richness of identified ECM fungal taxa was variable and ranged from three to nine for oak and from three to seven for hazel, depending on the year (Table 3). The highest mean species richness per sample was noted in 2012 (5.20 for oak and 4.40 for hazel) and the lowest was noted in 2013 (2.40 for oak and 1.80 for hazel). The highest diversity index was noted in 2012 for both oak (1.58) and hazel (1.57). The evenness index was highest in 2013 for oak (0.80) and in 2014 for hazel (0.90). The highest species dominance index was observed for oak in 2014 (0.53) and for hazel in 2013 (0.47).

Table 3

Species richness, Shannon diversity, evenness and Simpson dominance indices of ectomycorrhizal communities associated with oak (Quercus robur L.) and hazel (Corylus avellana L.) in Tuber aestivum plantations in Chełm.

201220132014
OakHazelOakHazelOakHazel
Number of samples5.005.005.005.005.005.00
Total species richness9.007.004.003.003.004.00
Average species richness5.204.402.401.802.003.00
Shannon diversity index (H’)1.581.571.110.800.711.25
Evenness (J’)0.720.810.800.730.640.90
Simpson dominance index (λ)0.280.250.370.470.530.32

The number of fungal taxa was not significantly different between oak and hazel samples (Fig. 2 a-d). The results showed rich colonization of sapling roots by pioneer fungi. The number of fungal species significantly decreased in 2013 and 2014 (Fig. 3).

Figure 2 Number of fungal taxa found on roots of oak and hazel in the orchard studied here. Number of taxa found in (a) 2012, (b) 2013, (c) 2014 and (d) all years together. Black squares represent oak samples; grey circles represent hazel; whiskers show 95% confidence intervals; 1,000 randomizations were used.
Figure 2

Number of fungal taxa found on roots of oak and hazel in the orchard studied here. Number of taxa found in (a) 2012, (b) 2013, (c) 2014 and (d) all years together. Black squares represent oak samples; grey circles represent hazel; whiskers show 95% confidence intervals; 1,000 randomizations were used.

Figure 3 Total number of ectomycorrhizal taxa associated with oak and hazel in the three study years. Sample-based rarefactions (solid lines) and 95% confidence intervals (dashed lines) are shown. The number of species in 2012 (green), 2013 (orange) and 2014 (blue) is shown
Figure 3

Total number of ectomycorrhizal taxa associated with oak and hazel in the three study years. Sample-based rarefactions (solid lines) and 95% confidence intervals (dashed lines) are shown. The number of species in 2012 (green), 2013 (orange) and 2014 (blue) is shown

Similarity among samples according to species composition is indicated in Fig. 4 a-d, and the first axis of the CCA explained 42.19% of the variance in the data in 2012, 37.21% in 2013, 55.16% in 2014 and 43.94% in all years together. The second axis explained 16.51% of the variance in 2012, 21.59% in 2013, 27.84% in 2014 and 18.88% in all years together. Similarities among samples from oak and hazel indicated that there was a clear difference between samples from these two species in the first and third year, with only one diverging sample from hazel in the second year. The same result as for the first and third year was observed for all years analysed together. In total, samples from oak appeared to be more similar than those from hazel.

Figure 4 Similarity of samples from oak (black) and hazel (grey) roots according to ectomycorrhizal species composition. First and second axis of the detrended correspondence analyses for (a) 2012, (b) 2013, (c) 2014 and (d) all years together.
Figure 4

Similarity of samples from oak (black) and hazel (grey) roots according to ectomycorrhizal species composition. First and second axis of the detrended correspondence analyses for (a) 2012, (b) 2013, (c) 2014 and (d) all years together.

Ectomycorrhizal species composition on roots of hazel and oak differed significantly in all studied years, based on canonical correspondence analyses, in 2012 (F = 5.46; ? < 0.001), 2013 (F = 3.62; ? < 0.001) and 2014 (F = 7.58; ? < 0.001). The total explained variance was highest in 2013 (85.97%), followed by 2014 (48.70%) and 2012 (40.54%). Composition of the entire fungal communities during three seasons explained 43.20% of the variance (F = 6.09; ? < 0.001). Ectomycorrhizae, such as Inocybe sp., Lactarius sp. 2, Geopora sp., Laccaria tortilis, Scleroderma areolatum and Amphinema byssoides, colonized the largest number of tips of oak roots. Peziza sp., Lactarius sp. 1, Thelephora terrestris, Pezizales sp. and Alnicola sp. were more abundant on roots of hazel. The preference of T. aestivum, Cenococcum geophilum and Tomentella sp. was rather indifferent for oak and hazel (Fig. 5). Taxon richness did not increase with the age of the plantation.

Figure 5 Similarity between oak and hazel according to composition of ectomycorrhizal taxa. First and second axis of canonical correspondence analysis.
Figure 5

Similarity between oak and hazel according to composition of ectomycorrhizal taxa. First and second axis of canonical correspondence analysis.

4 Discussion

To the best of our knowledge, this report describes the first study in Poland in which the fungal below-ground community of oak and hazel inoculated with T. aestivum was examined. Ectomycorrhizal communities on root tips in natural and cultivated truffle plantations in the Mediterranean region have been amply investigated [16, 3241].

From our data, we determined that ectomycorrhizae of Peziza sp., Lactarius sp., T. terrestris, Pezizales sp. and Alnicola sp. were more frequent on the roots of hazel than on those of oak. Benucci et al. [16] investigated ectomycorrhizae of hornbeam and hazel in a T. aestivum orchard and found fungi belonging to Thelephoraceae and Peziza michelli exclusively on the roots of hazel trees. Host effects may be important factors that determine the structure of ectomycorrhizal diversity. A preference for a certain host taxon over other taxa can affect the ectomycorrhizal fungi community directly, and this preference is stronger for host species occurring later in plant community succession [42]. Examples of a preference for a particular host plant have also been found. For example, lotti et al. [39] found that, in the case of T. borchii, the ectomycorrhizae on oak roots differed significantly from those on pine roots.

Ectomycorrhizal species belonging to Inocybe and Lactarius are fairly common in various plant communities [43] and in environments in which truffles are produced [44,45]. Thelephoraceae species are common morphotypes on root tips in boreal forests [45] and in environments of truffle production [16, 3436, 39, 41, 47]. The genus Tomentella is widespread in orchards with Tuber spp. [16, 34, 36, 37, 39, 41,47]. Additionally, the species Cenococcum geophilum is a well-known cosmopolitan ectomycorrhizal fungus living in a wide range of environmental conditions [48,49] and is very abundant in truffle plantations [37]. The common presence of this fungus is related to its ubiquity on tree roots of the surrounding forest areas [50].

According to several authors [37,51], Cenococcum has only been detected in mature plantations. In our plantation, however, morphotypes of this fungus were present on roots of 4-year-old oaks and, in the case of hazel, they appeared on roots of 6-year-old saplings. Perhaps the difference is due to the nearby old deciduous stand. The presence of forests near a plantation, up to 75 m [13], may be a factor that clearly influences the fungal diversity in truffle orchards.

In our study, T. aestivum ectomycorrhizae were present in all 3 years and we observed that species richness did not increase with the age of the plantation. This result is surprising since usually the number of fungal species in plantations increases with time [43,52]. This may be due to the plantation management. Findings of Sanchez [52] showed that tillage can decrease the presence of Scleroderma sp. and other ectomycorrhizae belonging to the long-distance exploration type, as rhizomorphs are broken in the process. In 2013, the tillage was performed twice, in spring and autumn, to limit rapid growth of weeds and increase the soil aeration, which possibly favoured the development of T. aestivum ectomycorrhizae. However, tillage practices (that had been done in the orchards, such as mulching, weed control, plougthing) could cause a detriment of ectomycorrhizal diversity as well. Most ECM roots are located in the top layer of soil (down to 20 cm depth), due to the richness in organic matter and the high concentration of nutrients in this layer [5355]. This soil layer was clearly affected by soil tillage, and hence recolonization of broken roots by fast-growing fungal species might be the main cause of reduction in ECM fungal diversity. Such an explanation is supported by results obtained in two T. magnatum truffle orchards, where after tillage, the number of fungal species decreased from 45 to 2 in one and from 22 to 18 in the other [56].

We found that ectomycorrhizae of Scleroderma areolatum were present on roots of oak and hazel only in the first year of this study when the plantation was 4 years old. However, the presence of Scleroderma species did not cause any damage to truffles or prevent their fructification [57]. Similarly, ectomycorrhizae of Lactarius spp. were present in the 4-year-old plantation and disappeared after the fourth year of seedling growth. The lack of ectomycorrhizae formed by Hebeloma should be promising for future fructification of T. aestivum since, in certain cases, species of this fungus can stop the truffle from developing correctly [38]. Hebeloma is one of the genera that could endanger truffle production due to its high competitiveness. Species in this genus often have a broad host range and an extensive distribution in temperate forests. Marmeisse et al. [58] consider Hebeloma a cosmopolitan genus that appears in both early and late stages of plantations and is probably favoured by the open space created in stand management. Given that other species belonging to Laccaria and Russula have been mostly associated with unproductive truffle orchards [57], their lack of presence in our orchard bodes well for the future of T. aestivum fructification. Another factor that justifies this conclusion is the presence of a T. rufum fruiting body that was discovered in August 2014 very close to the stem of a hazel tree. According to Olivier et al. [14], its appearance is an indicator of future good production of T. melanosporum. T. rufum Pico grows in many truffle orchards and has been repeatedly noted in French and Spanish plantations and, to a lesser extent, in Italy and the USA [57].

Acknowledgments

This research was funded by the State Forest National Forest Holding (Project No OR 271.3.6.2015), the Polish Ministry of Science and Higher Education (Project No 240 318) and the Forest Research Institute (Project No 260102).

Authors’ contributions

Participation of authors: DH designed the study, interpreted the data and wrote the paper; HS carried out mycorrhizae analysis and helped to draft the manuscript; JH performed the statistical analysis and interpreted the data; and ARG helped to draft the manuscript.

  1. Conflict of interest: The authors declare nothing to disclose.

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Received: 2016-7-6
Accepted: 2016-10-27
Published Online: 2016-11-16
Published in Print: 2016-1-1

© 2016 Dorota Hilszczánska et al., published by De Gruyter Open

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

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