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Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery

Wheat (Triticum aestivum L.) growing areas in many regions of the world are subject to heat waves which are predicted to increase in frequency because of climate change. The engineering of crop plants can be a useful strategy to mitigate heat stress-caused yield losses. Previously, we have shown tha...

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Autores principales: Kalaipandian, Sundaravelpandian, Powell, Jonathan, Karunakaran, Aneesh, Stiller, Jiri, Adkins, Steve, Kage, Udaykumar, Kazan, Kemal, Fleury, Delphine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9967677/
https://www.ncbi.nlm.nih.gov/pubmed/36834507
http://dx.doi.org/10.3390/ijms24043099
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author Kalaipandian, Sundaravelpandian
Powell, Jonathan
Karunakaran, Aneesh
Stiller, Jiri
Adkins, Steve
Kage, Udaykumar
Kazan, Kemal
Fleury, Delphine
author_facet Kalaipandian, Sundaravelpandian
Powell, Jonathan
Karunakaran, Aneesh
Stiller, Jiri
Adkins, Steve
Kage, Udaykumar
Kazan, Kemal
Fleury, Delphine
author_sort Kalaipandian, Sundaravelpandian
collection PubMed
description Wheat (Triticum aestivum L.) growing areas in many regions of the world are subject to heat waves which are predicted to increase in frequency because of climate change. The engineering of crop plants can be a useful strategy to mitigate heat stress-caused yield losses. Previously, we have shown that heat shock factor subclass C (TaHsfC2a-B)-overexpression significantly increased the survival of heat-stressed wheat seedlings. Although previous studies have shown that the overexpression of Hsf genes enhanced the survival of plants under heat stress, the molecular mechanisms are largely unknown. To understand the underlying molecular mechanisms involved in this response, a comparative analysis of the root transcriptomes of untransformed control and TaHsfC2a-overexpressing wheat lines by RNA-sequencing have been performed. The results of RNA-sequencing indicated that the roots of TaHsfC2a-overexpressing wheat seedlings showed lower transcripts of hydrogen peroxide-producing peroxidases, which corresponds to the reduced accumulation of hydrogen peroxide along the roots. In addition, suites of genes from iron transport and nicotianamine-related gene ontology categories showed lower transcript abundance in the roots of TaHsfC2a-overexpressing wheat roots than in the untransformed control line following heat stress, which are in accordance with the reduction in iron accumulation in the roots of transgenic plants under heat stress. Overall, these results suggested the existence of ferroptosis-like cell death under heat stress in wheat roots, and that TaHsfC2a is a key player in this mechanism. To date, this is the first evidence to show that a Hsf gene plays a key role in ferroptosis under heat stress in plants. In future, the role of Hsf genes could be further studied on ferroptosis in plants to identify root-based marker genes to screen for heat-tolerant genotypes.
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spelling pubmed-99676772023-02-27 Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery Kalaipandian, Sundaravelpandian Powell, Jonathan Karunakaran, Aneesh Stiller, Jiri Adkins, Steve Kage, Udaykumar Kazan, Kemal Fleury, Delphine Int J Mol Sci Article Wheat (Triticum aestivum L.) growing areas in many regions of the world are subject to heat waves which are predicted to increase in frequency because of climate change. The engineering of crop plants can be a useful strategy to mitigate heat stress-caused yield losses. Previously, we have shown that heat shock factor subclass C (TaHsfC2a-B)-overexpression significantly increased the survival of heat-stressed wheat seedlings. Although previous studies have shown that the overexpression of Hsf genes enhanced the survival of plants under heat stress, the molecular mechanisms are largely unknown. To understand the underlying molecular mechanisms involved in this response, a comparative analysis of the root transcriptomes of untransformed control and TaHsfC2a-overexpressing wheat lines by RNA-sequencing have been performed. The results of RNA-sequencing indicated that the roots of TaHsfC2a-overexpressing wheat seedlings showed lower transcripts of hydrogen peroxide-producing peroxidases, which corresponds to the reduced accumulation of hydrogen peroxide along the roots. In addition, suites of genes from iron transport and nicotianamine-related gene ontology categories showed lower transcript abundance in the roots of TaHsfC2a-overexpressing wheat roots than in the untransformed control line following heat stress, which are in accordance with the reduction in iron accumulation in the roots of transgenic plants under heat stress. Overall, these results suggested the existence of ferroptosis-like cell death under heat stress in wheat roots, and that TaHsfC2a is a key player in this mechanism. To date, this is the first evidence to show that a Hsf gene plays a key role in ferroptosis under heat stress in plants. In future, the role of Hsf genes could be further studied on ferroptosis in plants to identify root-based marker genes to screen for heat-tolerant genotypes. MDPI 2023-02-04 /pmc/articles/PMC9967677/ /pubmed/36834507 http://dx.doi.org/10.3390/ijms24043099 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
Kalaipandian, Sundaravelpandian
Powell, Jonathan
Karunakaran, Aneesh
Stiller, Jiri
Adkins, Steve
Kage, Udaykumar
Kazan, Kemal
Fleury, Delphine
Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery
title Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery
title_full Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery
title_fullStr Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery
title_full_unstemmed Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery
title_short Transcriptome Analysis of Heat Shock Factor C2a Over-Expressing Wheat Roots Reveals Ferroptosis-like Cell Death in Heat Stress Recovery
title_sort transcriptome analysis of heat shock factor c2a over-expressing wheat roots reveals ferroptosis-like cell death in heat stress recovery
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9967677/
https://www.ncbi.nlm.nih.gov/pubmed/36834507
http://dx.doi.org/10.3390/ijms24043099
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