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High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines

BACKGROUND: High temperature shock is becoming increasingly common in our climate, affecting plant growth and productivity. The ability of a plant to survive stress is a complex phenomenon. One of the essential tissues for plant performance under various environmental stimuli is the crown. However,...

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Autores principales: Mikołajczak, Krzysztof, Kuczyńska, Anetta, Ogrodowicz, Piotr, Kiełbowicz-Matuk, Agnieszka, Ćwiek-Kupczyńska, Hanna, Daszkowska-Golec, Agata, Szarejko, Iwona, Surma, Maria, Krajewski, Paweł
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8897901/
https://www.ncbi.nlm.nih.gov/pubmed/35246029
http://dx.doi.org/10.1186/s12864-022-08410-1
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author Mikołajczak, Krzysztof
Kuczyńska, Anetta
Ogrodowicz, Piotr
Kiełbowicz-Matuk, Agnieszka
Ćwiek-Kupczyńska, Hanna
Daszkowska-Golec, Agata
Szarejko, Iwona
Surma, Maria
Krajewski, Paweł
author_facet Mikołajczak, Krzysztof
Kuczyńska, Anetta
Ogrodowicz, Piotr
Kiełbowicz-Matuk, Agnieszka
Ćwiek-Kupczyńska, Hanna
Daszkowska-Golec, Agata
Szarejko, Iwona
Surma, Maria
Krajewski, Paweł
author_sort Mikołajczak, Krzysztof
collection PubMed
description BACKGROUND: High temperature shock is becoming increasingly common in our climate, affecting plant growth and productivity. The ability of a plant to survive stress is a complex phenomenon. One of the essential tissues for plant performance under various environmental stimuli is the crown. However, the molecular characterization of this region remains poorly investigated. Gibberellins play a fundamental role in whole-plant stature formation. This study identified plant stature modifications and crown-specific transcriptome re-modeling in gibberellin-deficient barley sdw1.a (BW827) and sdw1.d (BW828) mutants exposed to increased temperature. RESULTS: The deletion around the sdw1 gene in BW827 was found to encompass at least 13 genes with primarily regulatory functions. A bigger genetic polymorphism of BW828 than of BW827 in relation to wild type was revealed. Transcriptome-wide sequencing (RNA-seq) revealed several differentially expressed genes involved in gibberellin metabolism and heat response located outside of introgression regions. It was found that HvGA20ox4, a paralogue of the HvGA20ox2 gene, was upregulated in BW828 relative to other genotypes, which manifested as basal internode elongation. The transcriptome response to elevated temperature differed in the crown of sdw1.a and sdw1.d mutants; it was most contrasting for HvHsf genes upregulated under elevated temperature in BW828, whereas those specific to BW827 were downregulated. In-depth examination of sdw1 mutants revealed also some differences in their phenotypes and physiology. CONCLUSIONS: We concluded that despite the studied sdw1 mutants being genetically related, their heat response seemed to be genotype-specific and observed differences resulted from genetic background diversity rather than single gene mutation, multiple gene deletion, or allele-specific expression of the HvGA20ox2 gene. Differences in the expressional reaction of genes to heat in different sdw1 mutants, found to be independent of the polymorphism, could be further explained by in-depth studies of the regulatory factors acting in the studied system. Our findings are particularly important in genetic research area since molecular response of crown tissue has been marginally investigated, and can be useful for wide genetic research of crops since barley has become a model plant for them. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08410-1.
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spelling pubmed-88979012022-03-14 High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines Mikołajczak, Krzysztof Kuczyńska, Anetta Ogrodowicz, Piotr Kiełbowicz-Matuk, Agnieszka Ćwiek-Kupczyńska, Hanna Daszkowska-Golec, Agata Szarejko, Iwona Surma, Maria Krajewski, Paweł BMC Genomics Research BACKGROUND: High temperature shock is becoming increasingly common in our climate, affecting plant growth and productivity. The ability of a plant to survive stress is a complex phenomenon. One of the essential tissues for plant performance under various environmental stimuli is the crown. However, the molecular characterization of this region remains poorly investigated. Gibberellins play a fundamental role in whole-plant stature formation. This study identified plant stature modifications and crown-specific transcriptome re-modeling in gibberellin-deficient barley sdw1.a (BW827) and sdw1.d (BW828) mutants exposed to increased temperature. RESULTS: The deletion around the sdw1 gene in BW827 was found to encompass at least 13 genes with primarily regulatory functions. A bigger genetic polymorphism of BW828 than of BW827 in relation to wild type was revealed. Transcriptome-wide sequencing (RNA-seq) revealed several differentially expressed genes involved in gibberellin metabolism and heat response located outside of introgression regions. It was found that HvGA20ox4, a paralogue of the HvGA20ox2 gene, was upregulated in BW828 relative to other genotypes, which manifested as basal internode elongation. The transcriptome response to elevated temperature differed in the crown of sdw1.a and sdw1.d mutants; it was most contrasting for HvHsf genes upregulated under elevated temperature in BW828, whereas those specific to BW827 were downregulated. In-depth examination of sdw1 mutants revealed also some differences in their phenotypes and physiology. CONCLUSIONS: We concluded that despite the studied sdw1 mutants being genetically related, their heat response seemed to be genotype-specific and observed differences resulted from genetic background diversity rather than single gene mutation, multiple gene deletion, or allele-specific expression of the HvGA20ox2 gene. Differences in the expressional reaction of genes to heat in different sdw1 mutants, found to be independent of the polymorphism, could be further explained by in-depth studies of the regulatory factors acting in the studied system. Our findings are particularly important in genetic research area since molecular response of crown tissue has been marginally investigated, and can be useful for wide genetic research of crops since barley has become a model plant for them. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08410-1. BioMed Central 2022-03-04 /pmc/articles/PMC8897901/ /pubmed/35246029 http://dx.doi.org/10.1186/s12864-022-08410-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Mikołajczak, Krzysztof
Kuczyńska, Anetta
Ogrodowicz, Piotr
Kiełbowicz-Matuk, Agnieszka
Ćwiek-Kupczyńska, Hanna
Daszkowska-Golec, Agata
Szarejko, Iwona
Surma, Maria
Krajewski, Paweł
High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines
title High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines
title_full High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines
title_fullStr High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines
title_full_unstemmed High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines
title_short High-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines
title_sort high-throughput sequencing data revealed genotype-specific changes evoked by heat stress in crown tissue of barley sdw1 near-isogenic lines
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8897901/
https://www.ncbi.nlm.nih.gov/pubmed/35246029
http://dx.doi.org/10.1186/s12864-022-08410-1
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