A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak

The drought sensitivity of the pedunculate oak (<i>Quercus robur</i> L.) poses a threat to its survival in light of climate change. Mycorrhizal fungi, which orchestrate biogeochemical cycles and particularly have an impact on the plant’s defense mechanisms and metabolism of carbon, nitro...

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Main Authors: Marko Kebert, Saša Kostić, Srđan Stojnić, Eleonora Čapelja, Anđelina Gavranović Markić, Martina Zorić, Lazar Kesić, Victor Flors
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/8/7510
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author Marko Kebert
Saša Kostić
Srđan Stojnić
Eleonora Čapelja
Anđelina Gavranović Markić
Martina Zorić
Lazar Kesić
Victor Flors
author_facet Marko Kebert
Saša Kostić
Srđan Stojnić
Eleonora Čapelja
Anđelina Gavranović Markić
Martina Zorić
Lazar Kesić
Victor Flors
author_sort Marko Kebert
collection DOAJ
description The drought sensitivity of the pedunculate oak (<i>Quercus robur</i> L.) poses a threat to its survival in light of climate change. Mycorrhizal fungi, which orchestrate biogeochemical cycles and particularly have an impact on the plant’s defense mechanisms and metabolism of carbon, nitrogen, and phosphorus, are among the microbes that play a significant role in the mitigation of the effects of climate change on trees. The study’s main objectives were to determine whether ectomycorrhizal (ECM) fungi alleviate the effects of drought stress in pedunculate oak and to investigate their priming properties. The effects of two levels of drought (mild and severe, corresponding to 60% and 30% of field capacity, respectively) on the biochemical response of pedunculate oak were examined in the presence and absence of ectomycorrhizal fungi. To examine whether the ectomycorrhizal fungi modulate the drought tolerance of pedunculate oak, levels of plant hormones and polyamines were quantified using UPLC-TQS and HPLC-FD techniques in addition to gas exchange measurements and the main osmolyte amounts (glycine betaine-GB and proline-PRO) which were determined spectrophotometrically. Droughts increased the accumulation of osmolytes, such as proline and glycine betaine, as well as higher polyamines (spermidine and spermine) levels and decreased putrescine levels in both, mycorrhized and non-mycorrhized oak seedlings. In addition to amplifying the response of oak to severe drought in terms of inducible proline and abscisic acid (ABA) levels, inoculation with ECM fungi significantly increased the constitutive levels of glycine betaine, spermine, and spermidine regardless of drought stress. This study found that compared to non-mycorrhized oak seedlings, unstressed ECM-inoculated oak seedlings had higher levels of salicylic (SA) and abscisic acid (ABA) but not jasmonic acid (JA), indicating a priming mechanism of ECM is conveyed via these plant hormones. According to a PCA analysis, the effect of drought was linked to the variability of parameters along the PC1 axe, such as osmolytes PRO, GB, polyamines, and plant hormones such as JA, JA-Ile, SAG, and SGE, whereas mycorrhization was more closely associated with the parameters gathered around the PC2 axe (SA, ODPA, ABA, and E). These findings highlight the beneficial function of the ectomycorrhizal fungi, in particular <i>Scleroderma citrinum</i>, in reducing the effects of drought stress in pedunculate oak.
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spelling doaj.art-5072e034008b48aeaec2f4f0a0c45b4e2023-11-17T19:41:29ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-04-01248751010.3390/ijms24087510A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate OakMarko Kebert0Saša Kostić1Srđan Stojnić2Eleonora Čapelja3Anđelina Gavranović Markić4Martina Zorić5Lazar Kesić6Victor Flors7Institute of Lowland Forestry and Environment, University of Novi Sad, Antona Čehova 13d, 21000 Novi Sad, SerbiaInstitute of Lowland Forestry and Environment, University of Novi Sad, Antona Čehova 13d, 21000 Novi Sad, SerbiaInstitute of Lowland Forestry and Environment, University of Novi Sad, Antona Čehova 13d, 21000 Novi Sad, SerbiaFaculty of Science, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, SerbiaDivision for Silviculture, Croatian Forest Research Institute, Cvjetno Naselje 41, 10450 Jastrebarsko, CroatiaInstitute of Lowland Forestry and Environment, University of Novi Sad, Antona Čehova 13d, 21000 Novi Sad, SerbiaInstitute of Lowland Forestry and Environment, University of Novi Sad, Antona Čehova 13d, 21000 Novi Sad, SerbiaPlant Immunity and Biochemistry Group, Department of Biology, Biochemistry, and Natural Sciences, Jaume I University, 12071 Castellón de la Plana, SpainThe drought sensitivity of the pedunculate oak (<i>Quercus robur</i> L.) poses a threat to its survival in light of climate change. Mycorrhizal fungi, which orchestrate biogeochemical cycles and particularly have an impact on the plant’s defense mechanisms and metabolism of carbon, nitrogen, and phosphorus, are among the microbes that play a significant role in the mitigation of the effects of climate change on trees. The study’s main objectives were to determine whether ectomycorrhizal (ECM) fungi alleviate the effects of drought stress in pedunculate oak and to investigate their priming properties. The effects of two levels of drought (mild and severe, corresponding to 60% and 30% of field capacity, respectively) on the biochemical response of pedunculate oak were examined in the presence and absence of ectomycorrhizal fungi. To examine whether the ectomycorrhizal fungi modulate the drought tolerance of pedunculate oak, levels of plant hormones and polyamines were quantified using UPLC-TQS and HPLC-FD techniques in addition to gas exchange measurements and the main osmolyte amounts (glycine betaine-GB and proline-PRO) which were determined spectrophotometrically. Droughts increased the accumulation of osmolytes, such as proline and glycine betaine, as well as higher polyamines (spermidine and spermine) levels and decreased putrescine levels in both, mycorrhized and non-mycorrhized oak seedlings. In addition to amplifying the response of oak to severe drought in terms of inducible proline and abscisic acid (ABA) levels, inoculation with ECM fungi significantly increased the constitutive levels of glycine betaine, spermine, and spermidine regardless of drought stress. This study found that compared to non-mycorrhized oak seedlings, unstressed ECM-inoculated oak seedlings had higher levels of salicylic (SA) and abscisic acid (ABA) but not jasmonic acid (JA), indicating a priming mechanism of ECM is conveyed via these plant hormones. According to a PCA analysis, the effect of drought was linked to the variability of parameters along the PC1 axe, such as osmolytes PRO, GB, polyamines, and plant hormones such as JA, JA-Ile, SAG, and SGE, whereas mycorrhization was more closely associated with the parameters gathered around the PC2 axe (SA, ODPA, ABA, and E). These findings highlight the beneficial function of the ectomycorrhizal fungi, in particular <i>Scleroderma citrinum</i>, in reducing the effects of drought stress in pedunculate oak.https://www.mdpi.com/1422-0067/24/8/7510droughtpedunculate oakectomycorrhizal fungipolyaminesplant hormonesosmolytes
spellingShingle Marko Kebert
Saša Kostić
Srđan Stojnić
Eleonora Čapelja
Anđelina Gavranović Markić
Martina Zorić
Lazar Kesić
Victor Flors
A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak
International Journal of Molecular Sciences
drought
pedunculate oak
ectomycorrhizal fungi
polyamines
plant hormones
osmolytes
title A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak
title_full A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak
title_fullStr A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak
title_full_unstemmed A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak
title_short A Fine-Tuning of the Plant Hormones, Polyamines and Osmolytes by Ectomycorrhizal Fungi Enhances Drought Tolerance in Pedunculate Oak
title_sort fine tuning of the plant hormones polyamines and osmolytes by ectomycorrhizal fungi enhances drought tolerance in pedunculate oak
topic drought
pedunculate oak
ectomycorrhizal fungi
polyamines
plant hormones
osmolytes
url https://www.mdpi.com/1422-0067/24/8/7510
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