Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
Abstract Background Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known...
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| Format: | Article |
| Language: | English |
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BMC
2019-03-01
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| Series: | BMC Evolutionary Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12862-019-1398-z |
| _version_ | 1818677383860846592 |
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| author | Nicholas L. Panchy Christina B. Azodi Eamon F. Winship Ronan C. O’Malley Shin-Han Shiu |
| author_facet | Nicholas L. Panchy Christina B. Azodi Eamon F. Winship Ronan C. O’Malley Shin-Han Shiu |
| author_sort | Nicholas L. Panchy |
| collection | DOAJ |
| description | Abstract Background Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known about how TF duplicates have diverged in their expression and regulation, the answer to which may contribute to a better understanding of the elevated retention rate among TFs. Results Here we assessed what features may explain differences in the retention of TF duplicates and other genes using Arabidopsis thaliana as a model. We integrated 34 expression, sequence, and conservation features to build a linear model for predicting the extent of duplicate retention following WGD events among TFs and 19 groups of genes with other functions. We found that TFs was the least well predicted, demonstrating the features of TFs are substantially deviated from duplicate genes in other function groups. Consistent with this, the evolution of TF expression patterns and cis-regulatory cites favors the partitioning of ancestral states among the resulting duplicates: one “ancestral” TF duplicate retains most ancestral expression and cis-regulatory sites, while the “non-ancestral” duplicate is enriched for novel regulatory sites. By modeling the retention of ancestral expression and cis-regulatory states in duplicate pairs using a system of differential equations, we found that TF duplicate pairs in a partitioned state are preferentially maintained. Conclusions These TF duplicates with asymmetrically partitioned ancestral states are likely maintained because one copy retains ancestral functions while the other, at least in some cases, acquires novel cis-regulatory sites that may be important for novel, adaptive traits. |
| first_indexed | 2024-12-17T08:58:30Z |
| format | Article |
| id | doaj.art-8f3f8c5ce92b4b23a80db5df2f5e4d24 |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-17T08:58:30Z |
| publishDate | 2019-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-8f3f8c5ce92b4b23a80db5df2f5e4d242022-12-21T21:55:54ZengBMCBMC Evolutionary Biology1471-21482019-03-0119111710.1186/s12862-019-1398-zExpression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplicationNicholas L. Panchy0Christina B. Azodi1Eamon F. Winship2Ronan C. O’Malley3Shin-Han Shiu4Genetics Program, Michigan State UniversityDepartment of Plant Biology, Michigan State UniversityDepartment of Biochemistry and Molecular Biology, Michigan State UniversityDOE Joint Genome InstituteGenetics Program, Michigan State UniversityAbstract Background Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known about how TF duplicates have diverged in their expression and regulation, the answer to which may contribute to a better understanding of the elevated retention rate among TFs. Results Here we assessed what features may explain differences in the retention of TF duplicates and other genes using Arabidopsis thaliana as a model. We integrated 34 expression, sequence, and conservation features to build a linear model for predicting the extent of duplicate retention following WGD events among TFs and 19 groups of genes with other functions. We found that TFs was the least well predicted, demonstrating the features of TFs are substantially deviated from duplicate genes in other function groups. Consistent with this, the evolution of TF expression patterns and cis-regulatory cites favors the partitioning of ancestral states among the resulting duplicates: one “ancestral” TF duplicate retains most ancestral expression and cis-regulatory sites, while the “non-ancestral” duplicate is enriched for novel regulatory sites. By modeling the retention of ancestral expression and cis-regulatory states in duplicate pairs using a system of differential equations, we found that TF duplicate pairs in a partitioned state are preferentially maintained. Conclusions These TF duplicates with asymmetrically partitioned ancestral states are likely maintained because one copy retains ancestral functions while the other, at least in some cases, acquires novel cis-regulatory sites that may be important for novel, adaptive traits.http://link.springer.com/article/10.1186/s12862-019-1398-zExpression divergencecis-regulatory evolutionDuplicate retention |
| spellingShingle | Nicholas L. Panchy Christina B. Azodi Eamon F. Winship Ronan C. O’Malley Shin-Han Shiu Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication BMC Evolutionary Biology Expression divergence cis-regulatory evolution Duplicate retention |
| title | Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication |
| title_full | Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication |
| title_fullStr | Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication |
| title_full_unstemmed | Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication |
| title_short | Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication |
| title_sort | expression and regulatory asymmetry of retained arabidopsis thaliana transcription factor genes derived from whole genome duplication |
| topic | Expression divergence cis-regulatory evolution Duplicate retention |
| url | http://link.springer.com/article/10.1186/s12862-019-1398-z |
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