Ectomycorrhizal diversity in a mature pedunculate oak stand near Morović, Serbia

doi:10.3832/ifor4362-016

Ectomycorrhizal diversity in a mature pedunculate oak stand near Morović, Serbia

Marina Milović, Branislav Kovačević, Milan Drekić, Andrej Pilipović, Saša Pekeč, Lazar Kesić, Milutin Dilas, Velisav Karaklić, Zoran Galić

iForest - Biogeosciences and Forestry, Volume 16, Issue 6, Pages 345-351 (2023)
doi: https://doi.org/10.3832/ifor4362-016
Published: Nov 22, 2023 - Copyright © 2023 SISEF

Research Articles

PDF Version

Full Text

Citation

Geo-mapping

Pedunculate oak is among the most economically important deciduous forest tree species in Europe and is also a host for many important ectomycorrhizal (ECM) fungi. The aim of this study was to analyse the ECM fungal community in a mature pedunculate oak stand near Morović, Serbia in spring and autumn. ECM fungi were determined by combining morpho-anatomical characterization of ectomycorrhizas with molecular analysis based on PCR amplification of the internal transcribed spacer region of fungal nuclear ribosomal DNA. The number of ECM fungal taxa and the number of different categories of fine roots were counted, diversity indices were calculated, and ECM fungi were classified into exploration types. Twenty-one ECM fungal taxa were recorded in the studied mature pedunculate oak stand, 19 in spring and 13 in autumn. ECM communities consisted of one dominant taxon and a larger number of rare taxa. Lactarius quietus was the most abundant ECM fungus in both seasons which made association with more than half of ECM root tips. At the stand near Morović, contact exploration type (ET) dominated, short-distance ET was less abundant, while medium-distance fringe ET and long-distance ET were rare in both seasons. The most pronounced difference between seasons is recorded in the number of ECM fungal taxa. The number of ECM fungal taxa and diversity indices recorded in the studied pedunculate oak stand were lower or similar compared to values obtained in stands of oak species across Europe.

Keywords

Ectomycorrhizal Fungi, Quercus robur L., Morpho-Anatomical Characterization, ITS Region

Authors’ address

(1)

0000-0003-2993-1637
0000-0002-9125-0659
0000-0002-8189-7993
0000-0002-9458-0581
0000-0002-3803-2978
0000-0003-2643-9727
0000-0003-1324-9545
0000-0003-1264-9934
0000-0002-0748-9203
University of Novi Sad, Institute of Lowland Forestry and Environment, Antona Cehova 13, 21000 Novi Sad (Serbia)

Corresponding author

katanicm@uns.ac.rs

Citation

Milović M, Kovačević B, Drekić M, Pilipović A, Pekeč S, Kesić L, Dilas M, Karaklić V, Galić Z (2023). Ectomycorrhizal diversity in a mature pedunculate oak stand near Morović, Serbia. iForest 16: 345-351. - doi: 10.3832/ifor4362-016

Academic Editor

Daniela Baldantoni

Paper history

Received: Apr 11, 2023
Accepted: Sep 20, 2023

First online: Nov 22, 2023
Publication Date: Dec 31, 2023
Publication Time: 2.10 months

Open Access

This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 2344
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 854
Abstract Page Views: 789
PDF Downloads: 590
Citation/Reference Downloads: 3
XML Downloads: 108

Web Metrics
Days since publication: 365
Overall contacts: 2344
Avg. contacts per week: 44.95

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

(No citations were found up to date. Please come back later)

(no Plumx Metrics available for this paper)

Publication Metrics

by Dimensions ^©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

(1)

Agerer R (1991)
Characterisation of ectomycorrhiza. Techniques for the study of mycorrhiza In: “Methods in Microbiology vol. 23” (Norris JR, Read DJ, Varma AK eds). Academic Press, London, UK, pp. 25-72.
Gscholar

(2)

Agerer R (2001)
Exploration types of ectomycorrhizae. A proposal to classify ECM mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11 (2): 107-114.
CrossRef | Gscholar

(3)

Agerer R (2008)
Colour atlas of ectomycorrhizae (13th edn). Einhorn-Verlag, Schwäbisch Gmünd, Germany.
Gscholar

(4)

Agerer R, Rambold G (2022)
DEEMY - An information system for characterization and determination of ectomycorrhizae. München, Germany, web site.
Online | Gscholar

(5)

Anthony MA, Crowther TW, Van Der Linde S, Suz LM, Bidartondo MI, Cox F, Schaub M, Rautio P, Ferretti M, Vesterdal L, De Vos B, Dettwiler M, Eickenscheidt N, Schmitz A, Meesenburg H, Andreae H, Jacob F, Dietrich HP, Waldner P, Gessler A, Frey B, Schramm O, Van Den Bulk P, Hensen A, Averill C (2022)
Forest tree growth is linked to mycorrhizal fungal composition and function across Europe. The ISME Journal 16 (5): 1327-1336.
CrossRef | Gscholar

(6)

Atlas R, Bartha R (1981)
Introduction to microbiology. Addison-Wesley Publishing Company, Reading, UK, pp. 242-244.
Gscholar

(7)

Banković S, Medarević M, Pantić D, Petrović N (2009)
Nacionalna inventura šuma Republike Srbije - šumski fond Republike Srbije [National forest inventory of the Republic of Serbia - Forest growing stock of the Republic of Serbia]. Ministarstvo poljoprivrede šumarstva i vodoprivrede Republike Srbije - Uprava za šume, Beograd, Serbia. [in Serbian]
Gscholar

(8)

Barsoum N, O’Hara SW, Cottrell JE, Forster J, San Jose Garcia M, Schonrogge K, Shaw L (2021)
Root ectomycorrhizal status of oak trees symptomatic and asymptomatic for acute oak decline in southern Britain. Forest Ecology Management 482: 118800.
CrossRef | Gscholar

(9)

Bartlett MS (1936)
The square root transformation in analysis of variance. Journal of the Royal Statistical Society 3: 68-78.
CrossRef | Gscholar

(10)

Bzdyk RM, Olchowik J, Studnicki M, Nowakowska JA, Oszako T, Urban A, Hilszczanska D (2019)
Ectomycorrhizal colonisation in declining oak stands on the Krotoszyn Plateau, Poland. Forests 10 (30): 1-21.
CrossRef | Gscholar

(11)

Courty PE, Bréda N, Garbaye J (2007)
Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biology and Biochemistry 39 (7): 1655-1663.
CrossRef | Gscholar

(12)

Courty PE, Franc A, Pierrat JC, Garbaye J (2008)
Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate oak forest. Applied and Environmental Microbiology 74 (18): 5792-5801.
Gscholar

(13)

De Román M, De Miguel AM (2005)
Post-fire, seasonal and annual dynamics of the ectomycorrhizal community in a Quercus ilex L. forest over a 3-year period. Mycorrhiza 15: 471-482.
CrossRef | Gscholar

(14)

Ducousso A, Bordacs S (2004)
EUFORGEN Technical Guidelines for genetic conservation and use for pedunculate and sessile oaks (Quercus robur and Q. petraea). International Plant Genetic Resources Institute, Rome, Italy, pp. 1-6.
Online | Gscholar

(15)

Eaton E, Caudullo G, Oliveira S, De Rigo D (2016)
Quercus robur and Quercus petraea in Europe: distribution, habitat, usage and threats. In: “European Atlas of Forest Tree Species” (San-Miguel-Ayanz J, De Rigo D, Caudullo G, Houston Durrant T, Mauri A eds). Publication Office EU, Luxembourg, pp. 160-163.
Gscholar

(16)

Galić Z, Ponjarac R, Kiš A, Novčić Z (2015)
Karakteristike zemljišta u GJ Ristovača [Soil types in management unite Ristovača] Topola/Poplar 195- 196: 5-13. [in Serbian]
Gscholar

(17)

Gardes M, Bruns TD (1993)
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
CrossRef | Gscholar

(18)

Hall IR, Brown GT, Zambonelli A (2007)
Taming the truffle. The history, lore, and science of the ultimate mushroom. Timber Press, Inc., Portland, OR, USA, pp. 304.
Gscholar

(19)

Hobbie EA, Agerer R (2010)
Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327: 71-83.
CrossRef | Gscholar

(20)

Katanić M, Marković M, Pap P, Zlatković M, Pekeč S, Kovačević B (2017)
Biologija i uzgoj tartufa u svetu i Srbiji [Biology and cultivation of truffles in the world and Serbia]. Topola/Poplar 199/ 200: 175-190. [In Serbian]
Gscholar

(21)

Keizer PJ, Arnolds E (1994)
Succession of ectomycorrhizal fungi in roadside verges planted with common oak (Quercus robur L.) in Drenthe, The Netherlands. Mycorrhiza 4: 147-159.
CrossRef | Gscholar

(22)

Kesić L, Stojnić S, Orlović S, Pavlović L, Lozjanin R, Tepavac A, Vaštag E (2018)
Varijabilnost morfoloških karaktera žira hrasta lužnjaka (Quercus robur L.), kitnjaka (Q. petraea (Matt.) Lieb.) i cera (Q. cerris L.) [Variability of the morphological charateristics of pedunculate (Quercus robur L.), sessile (Q. petraea (Matt.) Lieb.) and Turkey oak (Q. cerris L.) acorns]. Topola/Poplar 201/ 202: 187-201. [In Serbian]
Gscholar

(23)

Kovacs G, Pausch M, Urban A (2000)
Diversity of ectomycorrhizal morphotypes and oak decline. Phyton 40 (4): 109-116.
Gscholar

(24)

Kraigher H (1996)
Tipi mikorize: taksonomija, pomen, aplikacija [Types of ectomycorrhizae - their taxonomy, role, and application]. Zbornik Gozdarstva in Lesarstva 49: 33-66. [In Slovenian]
Gscholar

(25)

Kraigher H, Petkovšek SA (2011)
Mycobioindication of stress in forest ecosystems. In: “Diversity and Biotechnology of Ectomycorrhizae, vol. 25” (Rai M, Varma A eds), Soil Biology, Springer, Berlin, Heidelberg, Germany, pp. 301-322.
CrossRef | Gscholar

(26)

Kyaschenko J, Clemmensen KE, Hagenbo A, Karltun E, Lindahl BD (2017)
Shift in fungal communities and associated enzyme activities along an age gradient of managed Pinus sylvestris stands. The ISME Journal 11 (4): 863-874.
CrossRef | Gscholar

(27)

Last FT, Dighton J, Mason PA (1987)
Successions of sheathing mycorrhizal fungi. Trends in Ecology and Evolution 2: 157-161.
Gscholar

(28)

Lilleskova EA, Hobbie EA, Horton TR (2011)
Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fungal Ecology 4: 174-183.
CrossRef | Gscholar

(29)

Milović M, Kebert M, Orlović S (2021a)
How mycorrhizas can help forests to cope with ongoing climate change? Sumarski List 145 (5-6): 279-286.
CrossRef | Gscholar

(30)

Milović M, Vasić V, Drekić M, Kovačević B, Pekeč S, Galić Z, Orlović S (2021b)
Diversity of ectomycorrhizal fungi associated with Quercus petraea in the national park Fruška Gora in the Republic of Serbia. Sumarski List 145(11-12): 547-555.
CrossRef | Gscholar

(31)

Milović M, Orlović S, Grebenc T, Bajc M, Kovačević B, Kraigher H (2021c)
Ectomycorrhizal fungal community in mature white poplar plantation. iForest 14: 540-547.
CrossRef | Gscholar

(32)

Milović M, Kovačević B, Pekeč S, Pilipović A, Kesić L, Gavranović Markić A, Orlović S (2022)
Diversity of ectomycorrhizal fungi in young pedunculate oak stand from Morović, Serbia. South-east European forestry 13 (1): 19-25.
CrossRef | Gscholar

(33)

NCBI (2021)
GenBank. National Center for Biotechnology Information - NCBI, Bethesda, ML, USA, web site.
Online | Gscholar

(34)

Nilsson RH, Larsson K-H, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K (2018)
The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research 47: 259-26.
CrossRef | Gscholar

(35)

O’Hanlon R, Harrington TJ (2012)
Similar taxonomic richness but different communities of ectomycorrhizas in native forests and non-native plantation forests. Mycorrhiza 22 (5): 371-382.
CrossRef | Gscholar

(36)

Olchowik J, Hilszczanska D, Bzdyk RM, Studnicki M, Malewski T, Borowski Z (2019)
Effect of deadwood on ectomycorrhizal colonisation of old-growth oak forests. Forests 10 (6): 480.
CrossRef | Gscholar

(37)

Radević V, Pap P, Vasić V (2020)
Gazdovanje šumama hrasta lužnjaka u Ravnom Sremu: juče, danas, sutra [Management of the common oak forests in Ravni Srem: yesterday, today, tomorrow]. Topola/Poplar 206: 41-52 [In Serbian]
Gscholar

(38)

Rosinger C, Sandén H, Matthews B, Mayer M, Godbold DL (2018)
Patterns in ectomycorrhizal diversity, community composition, and exploration types in European beech, pine, and spruce forests. Forests 9 (8): 445.
CrossRef | Gscholar

(39)

RSHS (2020)
Home page. Hydrometeorological Service - RSHS, Beograd, Republic of Serbia, web site.
Online | Gscholar

(40)

Schirkonyer U, Bauer C, Rothe G (2013)
Ectomycorrhizal diversity at five different tree species in forests of the Taunus Mountains in Central Germany. Open Journal of Ecology 3 (1): 66-81.
CrossRef | Gscholar

(41)

Selosse MA, Richard F, He X, Simard SW (2006)
Mycorrhizal networks: les liaisons dangereuses? Trends in Ecology and Evolution 21 (11): 621-628.
CrossRef | Gscholar

(42)

Smith SE, Read DJ (2008)
Mycorrhizal symbiosis (3rd edn). ElsevierAcademic Press, London, UK, pp. 787.
Gscholar

(43)

Snedecor W, Cochran WG (1976)
Statistical methods. Iowa State University Press, IA, USA, pp. 524.
Gscholar

(44)

Stojanović DB, Orlović S, Zlatković M, Kostić S, Vasić V, Miletić B, Kesić L, Matović B, Boanić D, Pavlović L, Milović M, Pekeč S (2021)
Climate change within Serbian forests: current state and future perspectives. Topola/Poplar 208: 39-56.
Gscholar

(45)

Suz LM, Barsoum N, Benham S, Dietrich HP, Fetzer KD, Fischer R, García P, Gehrman J, Kristöfel F, Manninger M, Neagu S, Nicolas M, Oldenburger J, Raspe S, Sánchez G, Schröck HW, Schubert A, Verheyen K, Verstraeten A, Bidartondo MI (2014)
Environmental drivers of ectomycorrhizal communities in Europe’s temperate oak forests. Molecular Ecology 23 (22): 5628-5644.
CrossRef | Gscholar

(46)

Taylor AFS, Martin F, Read DJ (2000)
Fungal diversity in ectomycorrhizal communities of Norway spruce (Picea abies (L.) Karst.) and beech (Fagus sylvatica L.) along north-south transects in Europe. In: “Carbon and Nitrogen Cycling in European Forest Ecosystems” (Schulze ED ed). Ecological Studies 142, Springer-Verlag, Berlin Heidelberg, Germany, pp. 343-365.
Gscholar

(47)

Voríšková J, Brabcová V, Cajthaml T, Baldrian P (2014)
Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytologist 201 (1): 269-278.
CrossRef | Gscholar

(48)

White TJ, Bruns T, Lee S, Taylor J (1990)
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: “PCR Protocols. A Guide to Methods and Applications” (Innis MA, Gelfand DH, Sninsky JJ, White TJ eds). Academic Press, San Diego, CA, USA, pp. 315-322.
CrossRef | Gscholar

iForest - Biogeosciences and Forestry

Contents

Search

Journal Info

Journal Subjects and Fields

For Authors

For Reviewers

For Readers

SISEF Publishing

Search iForest Contents