Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress Defense

Plants are frequently challenged by a variety of microorganisms. To protect themselves against harmful invaders, they have evolved highly effective defense mechanisms, including the synthesis of numerous types of antimicrobial peptides (AMPs). Snakins are such compounds, encoded by the <i>GASA...

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Main Authors: Mohamed Taieb Bouteraa, Walid Ben Romdhane, Alina Wiszniewska, Narjes Baazaoui, Mohammad Y. Alfaifi, Anis Ben Hsouna, Miroslava Kačániová, Stefania Garzoli, Rania Ben Saad
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Language:English
Published: MDPI AG 2025-01-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/1/112
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author Mohamed Taieb Bouteraa
Walid Ben Romdhane
Alina Wiszniewska
Narjes Baazaoui
Mohammad Y. Alfaifi
Anis Ben Hsouna
Miroslava Kačániová
Stefania Garzoli
Rania Ben Saad
author_facet Mohamed Taieb Bouteraa
Walid Ben Romdhane
Alina Wiszniewska
Narjes Baazaoui
Mohammad Y. Alfaifi
Anis Ben Hsouna
Miroslava Kačániová
Stefania Garzoli
Rania Ben Saad
author_sort Mohamed Taieb Bouteraa
collection DOAJ
description Plants are frequently challenged by a variety of microorganisms. To protect themselves against harmful invaders, they have evolved highly effective defense mechanisms, including the synthesis of numerous types of antimicrobial peptides (AMPs). Snakins are such compounds, encoded by the <i>GASA</i> (Gibberellic Acid-Stimulated Arabidopsis) gene family, and are involved in the response to biotic and abiotic stress. Here, we examined the function of the newly identified TdGASA1 gene and its encoded protein in <i>Triticum durum</i> subjected to different biotic stress-related simulants, such as mechanical injury, methyl jasmonate (MeJA), indole-3-acetic acid (IAA), salicylic acid (SA), hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), as well as infection with pathogenic fungi <i>Fusarium graminearum</i> and <i>Aspergillus niger</i>. We found that in durum wheat, <i>TdGASA1</i> transcripts were markedly increased in response to these stress simulants. Isolated and purified TdGASA1 protein exhibited significant antifungal activity in the growth inhibition test conducted on eight species of pathogenic fungi on solid and liquid media. Transgenic <i>Arabidopsis</i> lines overexpressing <i>TdGASA1</i> obtained in this study showed higher tolerance to detrimental effects of H<sub>2</sub>O<sub>2</sub>, MeJA, and ABA treatment. In addition, these lines exhibited resistance to <i>Fusarium graminearum</i> and <i>Aspergillus niger</i>, which was linked to a marked increase in antioxidant activity in the leaves under stress conditions. This resistance was correlated with the upregulation of pathogenesis-related genes (<i>AtPDF1.2a</i>, <i>AtERF1</i>, <i>AtVSP2</i>, <i>AtMYC2</i>, <i>AtPR1</i>, <i>AtACS6</i>, <i>AtETR1</i>, and <i>AtLOX2</i>) in the transgenic lines. Overall, our results indicate that TdGASA1 gene and its encoded protein respond ubiquitously to a range of biotic stimuli and seem to be crucial for the basal resistance of plants against pathogenic fungi. This gene could therefore be a valuable target for genetic engineering to enhance wheat resistance to biotic stress.
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spelling doaj-art-5b9f532432cc4aab8482233dec3c5f512025-01-10T13:19:47ZengMDPI AGPlants2223-77472025-01-0114111210.3390/plants14010112Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress DefenseMohamed Taieb Bouteraa0Walid Ben Romdhane1Alina Wiszniewska2Narjes Baazaoui3Mohammad Y. Alfaifi4Anis Ben Hsouna5Miroslava Kačániová6Stefania Garzoli7Rania Ben Saad8Biotechnology and Plant Improvement Laboratory, Centre of Biotechnology of Sfax, University of Sfax, P.O. Box 1177, Sfax 3018, TunisiaPlant Production Department, College of Food and Agricultural Sciences, King Saud University, P.O. Box 2460, Riyadh 11451, Saudi ArabiaDepartment of Botany, Physiology and Plant Protection, University of Agriculture in Kraków, Al. Mickiewicza 21, 31-120 Kraków, PolandBiology Department, Faculty of Science, King Khalid University, Abha 61421, Saudi ArabiaBiology Department, Faculty of Science, King Khalid University, Abha 61421, Saudi ArabiaBiotechnology and Plant Improvement Laboratory, Centre of Biotechnology of Sfax, University of Sfax, P.O. Box 1177, Sfax 3018, TunisiaInstitute of Horticulture, Faculty of Horticulture and Landscape Engineering, Slovak University of Agriculture, Tr. A. Hlinku 2, 94976 Nitra, SlovakiaDepartment of Chemistry and Technologies of Drug, Sapienza University, P.le Aldo Moro 5, 00185 Rome, ItalyBiotechnology and Plant Improvement Laboratory, Centre of Biotechnology of Sfax, University of Sfax, P.O. Box 1177, Sfax 3018, TunisiaPlants are frequently challenged by a variety of microorganisms. To protect themselves against harmful invaders, they have evolved highly effective defense mechanisms, including the synthesis of numerous types of antimicrobial peptides (AMPs). Snakins are such compounds, encoded by the <i>GASA</i> (Gibberellic Acid-Stimulated Arabidopsis) gene family, and are involved in the response to biotic and abiotic stress. Here, we examined the function of the newly identified TdGASA1 gene and its encoded protein in <i>Triticum durum</i> subjected to different biotic stress-related simulants, such as mechanical injury, methyl jasmonate (MeJA), indole-3-acetic acid (IAA), salicylic acid (SA), hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), as well as infection with pathogenic fungi <i>Fusarium graminearum</i> and <i>Aspergillus niger</i>. We found that in durum wheat, <i>TdGASA1</i> transcripts were markedly increased in response to these stress simulants. Isolated and purified TdGASA1 protein exhibited significant antifungal activity in the growth inhibition test conducted on eight species of pathogenic fungi on solid and liquid media. Transgenic <i>Arabidopsis</i> lines overexpressing <i>TdGASA1</i> obtained in this study showed higher tolerance to detrimental effects of H<sub>2</sub>O<sub>2</sub>, MeJA, and ABA treatment. In addition, these lines exhibited resistance to <i>Fusarium graminearum</i> and <i>Aspergillus niger</i>, which was linked to a marked increase in antioxidant activity in the leaves under stress conditions. This resistance was correlated with the upregulation of pathogenesis-related genes (<i>AtPDF1.2a</i>, <i>AtERF1</i>, <i>AtVSP2</i>, <i>AtMYC2</i>, <i>AtPR1</i>, <i>AtACS6</i>, <i>AtETR1</i>, and <i>AtLOX2</i>) in the transgenic lines. Overall, our results indicate that TdGASA1 gene and its encoded protein respond ubiquitously to a range of biotic stimuli and seem to be crucial for the basal resistance of plants against pathogenic fungi. This gene could therefore be a valuable target for genetic engineering to enhance wheat resistance to biotic stress.https://www.mdpi.com/2223-7747/14/1/112stress tolerancedefense signalingTdGASA1 protein<i>Triticum durum</i>antifungal activitytransgenic <i>Arabidopsis</i>
spellingShingle Mohamed Taieb Bouteraa
Walid Ben Romdhane
Alina Wiszniewska
Narjes Baazaoui
Mohammad Y. Alfaifi
Anis Ben Hsouna
Miroslava Kačániová
Stefania Garzoli
Rania Ben Saad
Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress Defense
Plants
stress tolerance
defense signaling
TdGASA1 protein
<i>Triticum durum</i>
antifungal activity
transgenic <i>Arabidopsis</i>
title Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress Defense
title_full Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress Defense
title_fullStr Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress Defense
title_full_unstemmed Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress Defense
title_short Functional Analysis of Durum Wheat GASA1 Protein as a Biotechnological Alternative Against Plant Fungal Pathogens and a Positive Regulator of Biotic Stress Defense
title_sort functional analysis of durum wheat gasa1 protein as a biotechnological alternative against plant fungal pathogens and a positive regulator of biotic stress defense
topic stress tolerance
defense signaling
TdGASA1 protein
<i>Triticum durum</i>
antifungal activity
transgenic <i>Arabidopsis</i>
url https://www.mdpi.com/2223-7747/14/1/112
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