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The evolution of WRKY transcription factors

BACKGROUND: The availability of increasing numbers of sequenced genomes has necessitated a re-evaluation of the evolution of the WRKY transcription factor family. Modern day plants descended from a charophyte green alga that colonized the land between 430 and 470 million years ago. The first charoph...

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Autores principales: Rinerson, Charles I, Rabara, Roel C, Tripathi, Prateek, Shen, Qingxi J, Rushton, Paul J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4350883/
https://www.ncbi.nlm.nih.gov/pubmed/25849216
http://dx.doi.org/10.1186/s12870-015-0456-y
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author Rinerson, Charles I
Rabara, Roel C
Tripathi, Prateek
Shen, Qingxi J
Rushton, Paul J
author_facet Rinerson, Charles I
Rabara, Roel C
Tripathi, Prateek
Shen, Qingxi J
Rushton, Paul J
author_sort Rinerson, Charles I
collection PubMed
description BACKGROUND: The availability of increasing numbers of sequenced genomes has necessitated a re-evaluation of the evolution of the WRKY transcription factor family. Modern day plants descended from a charophyte green alga that colonized the land between 430 and 470 million years ago. The first charophyte genome sequence from Klebsormidium flaccidum filled a gap in the available genome sequences in the plant kingdom between unicellular green algae that typically have 1-3 WRKY genes and mosses that contain 30-40. WRKY genes have been previously found in non-plant species but their occurrence has been difficult to explain. RESULTS: Only two WRKY genes are present in the Klebsormidium flaccidum genome and the presence of a Group IIb gene was unexpected because it had previously been thought that Group IIb WRKY genes first appeared in mosses. We found WRKY transcription factor genes outside of the plant lineage in some diplomonads, social amoebae, fungi incertae sedis, and amoebozoa. This patchy distribution suggests that lateral gene transfer is responsible. These lateral gene transfer events appear to pre-date the formation of the WRKY groups in flowering plants. Flowering plants contain proteins with domains typical for both resistance (R) proteins and WRKY transcription factors. R protein-WRKY genes have evolved numerous times in flowering plants, each type being restricted to specific flowering plant lineages. These chimeric proteins contain not only novel combinations of protein domains but also novel combinations and numbers of WRKY domains. Once formed, R protein WRKY genes may combine different components of signalling pathways that may either create new diversity in signalling or accelerate signalling by short circuiting signalling pathways. CONCLUSIONS: We propose that the evolution of WRKY transcription factors includes early lateral gene transfers to non-plant organisms and the occurrence of algal WRKY genes that have no counterparts in flowering plants. We propose two alternative hypotheses of WRKY gene evolution: The “Group I Hypothesis” sees all WRKY genes evolving from Group I C-terminal WRKY domains. The alternative “IIa + b Separate Hypothesis” sees Groups IIa and IIb evolving directly from a single domain algal gene separate from the Group I-derived lineage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0456-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-43508832015-03-06 The evolution of WRKY transcription factors Rinerson, Charles I Rabara, Roel C Tripathi, Prateek Shen, Qingxi J Rushton, Paul J BMC Plant Biol Research Article BACKGROUND: The availability of increasing numbers of sequenced genomes has necessitated a re-evaluation of the evolution of the WRKY transcription factor family. Modern day plants descended from a charophyte green alga that colonized the land between 430 and 470 million years ago. The first charophyte genome sequence from Klebsormidium flaccidum filled a gap in the available genome sequences in the plant kingdom between unicellular green algae that typically have 1-3 WRKY genes and mosses that contain 30-40. WRKY genes have been previously found in non-plant species but their occurrence has been difficult to explain. RESULTS: Only two WRKY genes are present in the Klebsormidium flaccidum genome and the presence of a Group IIb gene was unexpected because it had previously been thought that Group IIb WRKY genes first appeared in mosses. We found WRKY transcription factor genes outside of the plant lineage in some diplomonads, social amoebae, fungi incertae sedis, and amoebozoa. This patchy distribution suggests that lateral gene transfer is responsible. These lateral gene transfer events appear to pre-date the formation of the WRKY groups in flowering plants. Flowering plants contain proteins with domains typical for both resistance (R) proteins and WRKY transcription factors. R protein-WRKY genes have evolved numerous times in flowering plants, each type being restricted to specific flowering plant lineages. These chimeric proteins contain not only novel combinations of protein domains but also novel combinations and numbers of WRKY domains. Once formed, R protein WRKY genes may combine different components of signalling pathways that may either create new diversity in signalling or accelerate signalling by short circuiting signalling pathways. CONCLUSIONS: We propose that the evolution of WRKY transcription factors includes early lateral gene transfers to non-plant organisms and the occurrence of algal WRKY genes that have no counterparts in flowering plants. We propose two alternative hypotheses of WRKY gene evolution: The “Group I Hypothesis” sees all WRKY genes evolving from Group I C-terminal WRKY domains. The alternative “IIa + b Separate Hypothesis” sees Groups IIa and IIb evolving directly from a single domain algal gene separate from the Group I-derived lineage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0456-y) contains supplementary material, which is available to authorized users. BioMed Central 2015-02-27 /pmc/articles/PMC4350883/ /pubmed/25849216 http://dx.doi.org/10.1186/s12870-015-0456-y Text en © Rinerson et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Rinerson, Charles I
Rabara, Roel C
Tripathi, Prateek
Shen, Qingxi J
Rushton, Paul J
The evolution of WRKY transcription factors
title The evolution of WRKY transcription factors
title_full The evolution of WRKY transcription factors
title_fullStr The evolution of WRKY transcription factors
title_full_unstemmed The evolution of WRKY transcription factors
title_short The evolution of WRKY transcription factors
title_sort evolution of wrky transcription factors
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4350883/
https://www.ncbi.nlm.nih.gov/pubmed/25849216
http://dx.doi.org/10.1186/s12870-015-0456-y
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