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The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis

SIMPLE SUMMARY: Boron is an essential micronutrient for plants; however, boron toxicity has long been identified as a common nutritional problem on a global scale and is attracting increasing interest. Excessive concentrations of B significantly reduce crop yield, including that of wheat, which is a...

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Autores principales: Kaval, Ali, Yılmaz, Halil, Tunca Gedik, Sedef, Yıldız Kutman, Bahar, Kutman, Ümit Barış
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10452518/
https://www.ncbi.nlm.nih.gov/pubmed/37626984
http://dx.doi.org/10.3390/biology12081098
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author Kaval, Ali
Yılmaz, Halil
Tunca Gedik, Sedef
Yıldız Kutman, Bahar
Kutman, Ümit Barış
author_facet Kaval, Ali
Yılmaz, Halil
Tunca Gedik, Sedef
Yıldız Kutman, Bahar
Kutman, Ümit Barış
author_sort Kaval, Ali
collection PubMed
description SIMPLE SUMMARY: Boron is an essential micronutrient for plants; however, boron toxicity has long been identified as a common nutritional problem on a global scale and is attracting increasing interest. Excessive concentrations of B significantly reduce crop yield, including that of wheat, which is a staple food throughout the world. Wheat cultivation is particularly common in arid and semi-arid regions where climate change and irrigation can aggravate the risk and severity of B toxicity. Serendipita indica is a versatile root endophytic fungus. Studies show that plants colonized by Serendipita indica exhibit a wide range of beneficial effects, encompassing enhanced growth and yield, higher tolerance to various biotic and abiotic stresses, and improved water and nutrient balance. The present study revealed that under B toxicity, the growth, membrane integrity, tissue P content, and yield of wheat can be significantly improved by this endophyte without reducing toxic B concentrations in the shoot. Considering that Serendipita indica can be axenically produced on a large scale, this endophyte can be used as a microbiological agent for promoting sustainable agriculture under adverse soil conditions like boron toxicity. Further studies are needed to evaluate the potential and specific mechanisms of Serendipita indica under field conditions. ABSTRACT: While the importance of beneficial soil microorganisms for soil health and crop performance has been receiving ever-increasing attention, Serendipita indica has been widely studied as a fungal root endophyte with significant potential for increasing the stress tolerance of host plants. Boron (B) toxicity as an adverse soil condition is particularly prevalent in arid and semi-arid regions and threatens crop production. Studies on S. indica-wheat symbiosis are limited, and effects of S. indica on crops have never been reported in the context of B toxicity. Here, two pot experiments were conducted under greenhouse conditions to investigate the effects of S. indica on the growth and yield parameters of bread (Triticum aestivum) and durum wheat (Triticum durum) grown at different levels of B toxicity in native vs. sterilized soil, and parameters related to root colonization, membrane damage, oxidative stress, chlorophyll, and mineral nutrition were measured to elucidate the physiological mechanisms of damage and benefit. Boron toxicity decreased early vegetative growth and grain yield, but it did not affect the straw dry weight of mature plants, whereas S. indica significantly enhanced the vegetative growth, straw dry weight, and the grain number of both wheat species. Membrane damage as demonstrated by increased lipid peroxidation and relative electrolyte leakage was caused by B toxicity and alleviated by S. indica. The benefits provided by S. indica could not be attributed to any significant changes in tissue concentrations of B or other minerals such as phosphorus. Soil sterilization generally improved plant performance but it did not consistently strengthen or weaken the effects of S. indica. The presented results suggest that S. indica may be used as an effective microbial inoculant to enhance wheat growth under adverse soil conditions such as B toxicity through mechanisms that are possibly unrelated to mineral homeostasis.
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spelling pubmed-104525182023-08-26 The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis Kaval, Ali Yılmaz, Halil Tunca Gedik, Sedef Yıldız Kutman, Bahar Kutman, Ümit Barış Biology (Basel) Article SIMPLE SUMMARY: Boron is an essential micronutrient for plants; however, boron toxicity has long been identified as a common nutritional problem on a global scale and is attracting increasing interest. Excessive concentrations of B significantly reduce crop yield, including that of wheat, which is a staple food throughout the world. Wheat cultivation is particularly common in arid and semi-arid regions where climate change and irrigation can aggravate the risk and severity of B toxicity. Serendipita indica is a versatile root endophytic fungus. Studies show that plants colonized by Serendipita indica exhibit a wide range of beneficial effects, encompassing enhanced growth and yield, higher tolerance to various biotic and abiotic stresses, and improved water and nutrient balance. The present study revealed that under B toxicity, the growth, membrane integrity, tissue P content, and yield of wheat can be significantly improved by this endophyte without reducing toxic B concentrations in the shoot. Considering that Serendipita indica can be axenically produced on a large scale, this endophyte can be used as a microbiological agent for promoting sustainable agriculture under adverse soil conditions like boron toxicity. Further studies are needed to evaluate the potential and specific mechanisms of Serendipita indica under field conditions. ABSTRACT: While the importance of beneficial soil microorganisms for soil health and crop performance has been receiving ever-increasing attention, Serendipita indica has been widely studied as a fungal root endophyte with significant potential for increasing the stress tolerance of host plants. Boron (B) toxicity as an adverse soil condition is particularly prevalent in arid and semi-arid regions and threatens crop production. Studies on S. indica-wheat symbiosis are limited, and effects of S. indica on crops have never been reported in the context of B toxicity. Here, two pot experiments were conducted under greenhouse conditions to investigate the effects of S. indica on the growth and yield parameters of bread (Triticum aestivum) and durum wheat (Triticum durum) grown at different levels of B toxicity in native vs. sterilized soil, and parameters related to root colonization, membrane damage, oxidative stress, chlorophyll, and mineral nutrition were measured to elucidate the physiological mechanisms of damage and benefit. Boron toxicity decreased early vegetative growth and grain yield, but it did not affect the straw dry weight of mature plants, whereas S. indica significantly enhanced the vegetative growth, straw dry weight, and the grain number of both wheat species. Membrane damage as demonstrated by increased lipid peroxidation and relative electrolyte leakage was caused by B toxicity and alleviated by S. indica. The benefits provided by S. indica could not be attributed to any significant changes in tissue concentrations of B or other minerals such as phosphorus. Soil sterilization generally improved plant performance but it did not consistently strengthen or weaken the effects of S. indica. The presented results suggest that S. indica may be used as an effective microbial inoculant to enhance wheat growth under adverse soil conditions such as B toxicity through mechanisms that are possibly unrelated to mineral homeostasis. MDPI 2023-08-07 /pmc/articles/PMC10452518/ /pubmed/37626984 http://dx.doi.org/10.3390/biology12081098 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Kaval, Ali
Yılmaz, Halil
Tunca Gedik, Sedef
Yıldız Kutman, Bahar
Kutman, Ümit Barış
The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis
title The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis
title_full The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis
title_fullStr The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis
title_full_unstemmed The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis
title_short The Fungal Root Endophyte Serendipita indica (Piriformospora indica) Enhances Bread and Durum Wheat Performance under Boron Toxicity at Both Vegetative and Generative Stages of Development through Mechanisms Unrelated to Mineral Homeostasis
title_sort fungal root endophyte serendipita indica (piriformospora indica) enhances bread and durum wheat performance under boron toxicity at both vegetative and generative stages of development through mechanisms unrelated to mineral homeostasis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10452518/
https://www.ncbi.nlm.nih.gov/pubmed/37626984
http://dx.doi.org/10.3390/biology12081098
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