PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity

Background: Floral organs are specified by MADS-domain transcription factors that act in a combinatorial manner, as summarized in the (A)BCE model. However, this evolutionarily conserved model is in contrast to a remarkable amount of morphological diversity in flowers. One of the mechanisms suggested to contribute to this diversity is duplication of floral MADS-domain transcription factors. Although gene duplication is often followed by loss of one of the copies, sometimes both copies are retained. If both copies are retained they will initially be redundant, providing freedom for one of the paralogs to change function. Here, we examine the evolutionary fate and functional consequences of a transposition event at the base of the Brassicales that resulted in the duplication of the floral regulator PISTILLATA (PI), using Tarenaya hassleriana (Cleomaceae) as a model system. Results: The transposition of a genomic region containing a PI gene led to two paralogs which are located at different positions in the genome. The original PI copy is syntenic in position with most angiosperms, whereas the transposed copy is syntenic with the PI genes in Brassicaceae. The two PI paralogs of T. hassleriana have very similar expression patterns. However, they may have diverged in function, as only one of these PI proteins was able to act heterologously in the first whorl of A. thaliana flowers. We also observed differences in protein complex formation between the two paralogs, and the two paralogs exhibit subtle differences in DNA-binding specificity. Sequence analysis indicates that most of the protein sequence divergence between the two T. hassleriana paralogs emerged in a common ancestor of the Cleomaceae and the Brassicaceae. Conclusions: We found that the PI paralogs in T. hassleriana have similar expression patterns, but may have diverged at the level of protein function. Data suggest that most protein sequence divergence occurred rapidly, prior to the origin of the Brassicaceae and Cleomaceae. It is tempting to speculate that the interaction specificities of the Brassicaceae-specific PI proteins are different compared to the PI found in other angiosperms. This could lead to PI regulating partly different genes in the Brassicaceae, and ultimately might result in change floral in morphology.

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Main Authors: de Bruijn, Suzanne, Zhao, Tao, Muiño, Jose M., Schranz, Eric M., Angenent, Gerco C., Kaufmann, Kerstin
Format: Article/Letter to editor biblioteca
Language:English
Subjects:Cleomaceae, Flower development, Gene duplications, MADS, PISTILLATA, Paralogs, Tarenaya,
Online Access:https://research.wur.nl/en/publications/pistillata-paralogs-in-tarenaya-hassleriana-have-diverged-in-inte
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spelling dig-wur-nl-wurpubs-5454342024-09-23 de Bruijn, Suzanne Zhao, Tao Muiño, Jose M. Schranz, Eric M. Angenent, Gerco C. Kaufmann, Kerstin Article/Letter to editor BMC Plant Biology 18 (2018) 1 ISSN: 1471-2229 PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity 2018 Background: Floral organs are specified by MADS-domain transcription factors that act in a combinatorial manner, as summarized in the (A)BCE model. However, this evolutionarily conserved model is in contrast to a remarkable amount of morphological diversity in flowers. One of the mechanisms suggested to contribute to this diversity is duplication of floral MADS-domain transcription factors. Although gene duplication is often followed by loss of one of the copies, sometimes both copies are retained. If both copies are retained they will initially be redundant, providing freedom for one of the paralogs to change function. Here, we examine the evolutionary fate and functional consequences of a transposition event at the base of the Brassicales that resulted in the duplication of the floral regulator PISTILLATA (PI), using Tarenaya hassleriana (Cleomaceae) as a model system. Results: The transposition of a genomic region containing a PI gene led to two paralogs which are located at different positions in the genome. The original PI copy is syntenic in position with most angiosperms, whereas the transposed copy is syntenic with the PI genes in Brassicaceae. The two PI paralogs of T. hassleriana have very similar expression patterns. However, they may have diverged in function, as only one of these PI proteins was able to act heterologously in the first whorl of A. thaliana flowers. We also observed differences in protein complex formation between the two paralogs, and the two paralogs exhibit subtle differences in DNA-binding specificity. Sequence analysis indicates that most of the protein sequence divergence between the two T. hassleriana paralogs emerged in a common ancestor of the Cleomaceae and the Brassicaceae. Conclusions: We found that the PI paralogs in T. hassleriana have similar expression patterns, but may have diverged at the level of protein function. Data suggest that most protein sequence divergence occurred rapidly, prior to the origin of the Brassicaceae and Cleomaceae. It is tempting to speculate that the interaction specificities of the Brassicaceae-specific PI proteins are different compared to the PI found in other angiosperms. This could lead to PI regulating partly different genes in the Brassicaceae, and ultimately might result in change floral in morphology. en application/pdf https://research.wur.nl/en/publications/pistillata-paralogs-in-tarenaya-hassleriana-have-diverged-in-inte 10.1186/s12870-018-1574-0 https://edepot.wur.nl/467928 Cleomaceae Flower development Gene duplications MADS PISTILLATA Paralogs Tarenaya https://creativecommons.org/licenses/by/4.0/ Wageningen University & Research
institution WUR NL
collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic Cleomaceae
Flower development
Gene duplications
MADS
PISTILLATA
Paralogs
Tarenaya
Cleomaceae
Flower development
Gene duplications
MADS
PISTILLATA
Paralogs
Tarenaya
spellingShingle Cleomaceae
Flower development
Gene duplications
MADS
PISTILLATA
Paralogs
Tarenaya
Cleomaceae
Flower development
Gene duplications
MADS
PISTILLATA
Paralogs
Tarenaya
de Bruijn, Suzanne
Zhao, Tao
Muiño, Jose M.
Schranz, Eric M.
Angenent, Gerco C.
Kaufmann, Kerstin
PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
description Background: Floral organs are specified by MADS-domain transcription factors that act in a combinatorial manner, as summarized in the (A)BCE model. However, this evolutionarily conserved model is in contrast to a remarkable amount of morphological diversity in flowers. One of the mechanisms suggested to contribute to this diversity is duplication of floral MADS-domain transcription factors. Although gene duplication is often followed by loss of one of the copies, sometimes both copies are retained. If both copies are retained they will initially be redundant, providing freedom for one of the paralogs to change function. Here, we examine the evolutionary fate and functional consequences of a transposition event at the base of the Brassicales that resulted in the duplication of the floral regulator PISTILLATA (PI), using Tarenaya hassleriana (Cleomaceae) as a model system. Results: The transposition of a genomic region containing a PI gene led to two paralogs which are located at different positions in the genome. The original PI copy is syntenic in position with most angiosperms, whereas the transposed copy is syntenic with the PI genes in Brassicaceae. The two PI paralogs of T. hassleriana have very similar expression patterns. However, they may have diverged in function, as only one of these PI proteins was able to act heterologously in the first whorl of A. thaliana flowers. We also observed differences in protein complex formation between the two paralogs, and the two paralogs exhibit subtle differences in DNA-binding specificity. Sequence analysis indicates that most of the protein sequence divergence between the two T. hassleriana paralogs emerged in a common ancestor of the Cleomaceae and the Brassicaceae. Conclusions: We found that the PI paralogs in T. hassleriana have similar expression patterns, but may have diverged at the level of protein function. Data suggest that most protein sequence divergence occurred rapidly, prior to the origin of the Brassicaceae and Cleomaceae. It is tempting to speculate that the interaction specificities of the Brassicaceae-specific PI proteins are different compared to the PI found in other angiosperms. This could lead to PI regulating partly different genes in the Brassicaceae, and ultimately might result in change floral in morphology.
format Article/Letter to editor
topic_facet Cleomaceae
Flower development
Gene duplications
MADS
PISTILLATA
Paralogs
Tarenaya
author de Bruijn, Suzanne
Zhao, Tao
Muiño, Jose M.
Schranz, Eric M.
Angenent, Gerco C.
Kaufmann, Kerstin
author_facet de Bruijn, Suzanne
Zhao, Tao
Muiño, Jose M.
Schranz, Eric M.
Angenent, Gerco C.
Kaufmann, Kerstin
author_sort de Bruijn, Suzanne
title PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_short PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_full PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_fullStr PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_full_unstemmed PISTILLATA paralogs in Tarenaya hassleriana have diverged in interaction specificity
title_sort pistillata paralogs in tarenaya hassleriana have diverged in interaction specificity
url https://research.wur.nl/en/publications/pistillata-paralogs-in-tarenaya-hassleriana-have-diverged-in-inte
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