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Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction

SIMPLE SUMMARY: There have been many breakthroughs in MIF function and mechanism investigation in vertebrates, but it has rarely been studied in plants. Here, we aimed to characterize the function of MIF in wheat and its potential role in Wheat-Stripe rust interaction. We showed that wheat MIF has s...

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Autores principales: Zhao, Mengxin, Chang, Qing, Liu, Yueni, Sang, Peng, Kang, Zhensheng, Wang, Xiaojie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8470491/
https://www.ncbi.nlm.nih.gov/pubmed/34571757
http://dx.doi.org/10.3390/biology10090878
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author Zhao, Mengxin
Chang, Qing
Liu, Yueni
Sang, Peng
Kang, Zhensheng
Wang, Xiaojie
author_facet Zhao, Mengxin
Chang, Qing
Liu, Yueni
Sang, Peng
Kang, Zhensheng
Wang, Xiaojie
author_sort Zhao, Mengxin
collection PubMed
description SIMPLE SUMMARY: There have been many breakthroughs in MIF function and mechanism investigation in vertebrates, but it has rarely been studied in plants. Here, we aimed to characterize the function of MIF in wheat and its potential role in Wheat-Stripe rust interaction. We showed that wheat MIF has some similarities with that MIF in vertebrates, such as subcellular localization in both the cytosol and nuclei, as well as significant tautomerase activity, and both can inhibit Bax-induced programmed cell death. In the wheat–Pst interaction, TaMIF1 is upregulated during Pst infection. Silencing TaMIF1 decreased Pst infection of wheat tissues, and the accumulation of ROS was increased in TaMIF1-silenced wheat leaves, which hinted that TaMIF1 mainly modulates the ROS signaling and then alters the subsequent immune responses. The function characterization of TaMIF1 provides significant insight into the role of MIFs across kingdoms and helpful in-depth functional mechanism analysis on these proteins. ABSTRACT: Macrophage migration inhibitory factor (MIF), named for its role in inhibiting macrophage/monocyte migration, has multiple functions in modulation of inflammation, cell proliferation, angiogenesis, and tumorigenesis in vertebrates. Although homologs of this gene can be found in plants, the function of MIF in plants remains obscure. Here, we characterized TaMIF1 in Triticum aestivum resembling the MIF secreted from Homo sapiens. Transcript analysis revealed that TaMIF1 responded to stripe rust infection of wheat and was upregulated during the infection stage. TaMIF1 was localized to both the cytosol and nuclei in wheat mesophyll protoplast. Additionally, TaMIF1 possessed significant tautomerase activity, indicating conservation of MIFs across kingdoms. Agrobacterium tumefaciens infiltration assay demonstrated that TaMIF1 was capable of suppressing programmed cell death hinting its role in plant immunity. Heterologous expression of TaMIF1 increased fission yeast sensitivity to oxidative stress. Silencing TaMIF1 decreased the susceptibility of wheat to Pst seemingly through increasing reactive oxygen species accumulation. In conclusion, functions of the TaMIF1 were investigated in this study, which provides significant insight into understanding the role of MIFs across kingdoms.
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spelling pubmed-84704912021-09-27 Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction Zhao, Mengxin Chang, Qing Liu, Yueni Sang, Peng Kang, Zhensheng Wang, Xiaojie Biology (Basel) Article SIMPLE SUMMARY: There have been many breakthroughs in MIF function and mechanism investigation in vertebrates, but it has rarely been studied in plants. Here, we aimed to characterize the function of MIF in wheat and its potential role in Wheat-Stripe rust interaction. We showed that wheat MIF has some similarities with that MIF in vertebrates, such as subcellular localization in both the cytosol and nuclei, as well as significant tautomerase activity, and both can inhibit Bax-induced programmed cell death. In the wheat–Pst interaction, TaMIF1 is upregulated during Pst infection. Silencing TaMIF1 decreased Pst infection of wheat tissues, and the accumulation of ROS was increased in TaMIF1-silenced wheat leaves, which hinted that TaMIF1 mainly modulates the ROS signaling and then alters the subsequent immune responses. The function characterization of TaMIF1 provides significant insight into the role of MIFs across kingdoms and helpful in-depth functional mechanism analysis on these proteins. ABSTRACT: Macrophage migration inhibitory factor (MIF), named for its role in inhibiting macrophage/monocyte migration, has multiple functions in modulation of inflammation, cell proliferation, angiogenesis, and tumorigenesis in vertebrates. Although homologs of this gene can be found in plants, the function of MIF in plants remains obscure. Here, we characterized TaMIF1 in Triticum aestivum resembling the MIF secreted from Homo sapiens. Transcript analysis revealed that TaMIF1 responded to stripe rust infection of wheat and was upregulated during the infection stage. TaMIF1 was localized to both the cytosol and nuclei in wheat mesophyll protoplast. Additionally, TaMIF1 possessed significant tautomerase activity, indicating conservation of MIFs across kingdoms. Agrobacterium tumefaciens infiltration assay demonstrated that TaMIF1 was capable of suppressing programmed cell death hinting its role in plant immunity. Heterologous expression of TaMIF1 increased fission yeast sensitivity to oxidative stress. Silencing TaMIF1 decreased the susceptibility of wheat to Pst seemingly through increasing reactive oxygen species accumulation. In conclusion, functions of the TaMIF1 were investigated in this study, which provides significant insight into understanding the role of MIFs across kingdoms. MDPI 2021-09-07 /pmc/articles/PMC8470491/ /pubmed/34571757 http://dx.doi.org/10.3390/biology10090878 Text en © 2021 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
Zhao, Mengxin
Chang, Qing
Liu, Yueni
Sang, Peng
Kang, Zhensheng
Wang, Xiaojie
Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction
title Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction
title_full Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction
title_fullStr Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction
title_full_unstemmed Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction
title_short Functional Characterization of the Wheat Macrophage Migration Inhibitory Factor TaMIF1 in Wheat-Stripe Rust (Puccinia striiformis) Interaction
title_sort functional characterization of the wheat macrophage migration inhibitory factor tamif1 in wheat-stripe rust (puccinia striiformis) interaction
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8470491/
https://www.ncbi.nlm.nih.gov/pubmed/34571757
http://dx.doi.org/10.3390/biology10090878
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