Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein family

Crop diseases caused by pathogens critically affect global food security and plant ecology. Pathogens are well adapted to their host plants and have developed sophisticated mechanisms allowing successful colonization. Plants in turn have taken measures to counteract pathogen attacks resulting in an...

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Main Authors: Paul Klemm, Marvin Christ, Florian Altegoer, Johannes Freitag, Gert Bange, Marcus Lechner
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1034708/full
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author Paul Klemm
Marvin Christ
Florian Altegoer
Johannes Freitag
Gert Bange
Gert Bange
Marcus Lechner
author_facet Paul Klemm
Marvin Christ
Florian Altegoer
Johannes Freitag
Gert Bange
Gert Bange
Marcus Lechner
author_sort Paul Klemm
collection DOAJ
description Crop diseases caused by pathogens critically affect global food security and plant ecology. Pathogens are well adapted to their host plants and have developed sophisticated mechanisms allowing successful colonization. Plants in turn have taken measures to counteract pathogen attacks resulting in an evolutionary arms race. Recent studies provided mechanistic insights into how two plant Kiwellin proteins from Zea mays mitigate the activity of the chorismate mutase Cmu1, a virulence factor secreted by the fungal pathogen Ustilago maydis during maize infection. Formerly identified as human allergens in kiwifruit, the biological function of Kiwellins is apparently linked to plant defense. We combined the analysis of proteome data with structural predictions to obtain a holistic overview of the Kiwellin protein family, that is subdivided into proteins with and without a N-terminal kissper domain. We found that Kiwellins are evolutionarily conserved in various plant species. At median five Kiwellin paralogs are encoded in each plant genome. Structural predictions revealed that Barwin-like proteins and Kiwellins cannot be discriminated purely at the sequence level. Our data shows that Kiwellins emerged in land plants (embryophyta) and are not present in fungi as suggested earlier. They evolved via three major duplication events that lead to clearly distinguishable subfamilies. We introduce a systematic Kiwellin nomenclature based on a detailed evolutionary reconstruction of this protein family. A meta-analysis of publicly available transcriptome data demonstrated that Kiwellins can be differentially regulated upon the interaction of plants with pathogens but also with symbionts. Furthermore, significant differences in Kiwellin expression levels dependent on tissues and cultivars were observed. In summary, our study sheds light on the evolution and regulation of a large protein family and provides a framework for a more detailed understanding of the molecular functions of Kiwellins.
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spelling doaj.art-ee8c795770de4a998dd540a18a7a6f6f2022-12-22T08:59:26ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-12-011310.3389/fpls.2022.10347081034708Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein familyPaul Klemm0Marvin Christ1Florian Altegoer2Johannes Freitag3Gert Bange4Gert Bange5Marcus Lechner6Center for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, Marburg, GermanyCenter for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, Marburg, GermanyInstitute of Microbiology, Heinrich Heine University Dusseldorf, Düsseldorf, GermanyDepartment of Biology, Philipps-University Marburg, Marburg, GermanyCenter for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, Marburg, GermanyMolecular Physiology of Microbes, Max-Planck Institute for Terrestrial Microbiology, Marburg, GermanyCenter for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, Marburg, GermanyCrop diseases caused by pathogens critically affect global food security and plant ecology. Pathogens are well adapted to their host plants and have developed sophisticated mechanisms allowing successful colonization. Plants in turn have taken measures to counteract pathogen attacks resulting in an evolutionary arms race. Recent studies provided mechanistic insights into how two plant Kiwellin proteins from Zea mays mitigate the activity of the chorismate mutase Cmu1, a virulence factor secreted by the fungal pathogen Ustilago maydis during maize infection. Formerly identified as human allergens in kiwifruit, the biological function of Kiwellins is apparently linked to plant defense. We combined the analysis of proteome data with structural predictions to obtain a holistic overview of the Kiwellin protein family, that is subdivided into proteins with and without a N-terminal kissper domain. We found that Kiwellins are evolutionarily conserved in various plant species. At median five Kiwellin paralogs are encoded in each plant genome. Structural predictions revealed that Barwin-like proteins and Kiwellins cannot be discriminated purely at the sequence level. Our data shows that Kiwellins emerged in land plants (embryophyta) and are not present in fungi as suggested earlier. They evolved via three major duplication events that lead to clearly distinguishable subfamilies. We introduce a systematic Kiwellin nomenclature based on a detailed evolutionary reconstruction of this protein family. A meta-analysis of publicly available transcriptome data demonstrated that Kiwellins can be differentially regulated upon the interaction of plants with pathogens but also with symbionts. Furthermore, significant differences in Kiwellin expression levels dependent on tissues and cultivars were observed. In summary, our study sheds light on the evolution and regulation of a large protein family and provides a framework for a more detailed understanding of the molecular functions of Kiwellins.https://www.frontiersin.org/articles/10.3389/fpls.2022.1034708/fullKiwellinsplantsinteractionpathogensymbiontsevolution
spellingShingle Paul Klemm
Marvin Christ
Florian Altegoer
Johannes Freitag
Gert Bange
Gert Bange
Marcus Lechner
Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein family
Frontiers in Plant Science
Kiwellins
plants
interaction
pathogen
symbionts
evolution
title Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein family
title_full Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein family
title_fullStr Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein family
title_full_unstemmed Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein family
title_short Evolutionary reconstruction, nomenclature and functional meta-analysis of the Kiwellin protein family
title_sort evolutionary reconstruction nomenclature and functional meta analysis of the kiwellin protein family
topic Kiwellins
plants
interaction
pathogen
symbionts
evolution
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1034708/full
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