Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

T. Zhao, R. Holmer, S.A. de Bruijn, G.C. Angenent, H.A. van den Burg, M.E. Schranz

Research output: Contribution to journalArticleAcademicpeer-review

18 Citations (Scopus)

Abstract

Conserved genomic context provides critical information for comparative evolutionary analysis. 29 With the increase in numbers of sequenced plant genomes, synteny analysis can provide new 30 insight into gene family evolution. Here, we exploit a network analysis approach to organize and
31 interpret massive pairwise syntenic relationships. Specifically, we analyzed synteny networks of 32 the MADS-box transcription factor gene family using fifty-one completed plant genomes. In 33 combination with phylogenetic profiling, several novel evolutionary patterns were inferred and 34 visualized from synteny network clusters. We found lineage-specific clusters that derive from 35 transposition events for the regulators of floral development (APETALA3 and PI) and flowering36 time (FLC) in the Brassicales and for the regulators of root-development (AGL17) in Poales. We 37 also identified two large gene clusters that jointly encompass many key phenotypic regulatory 38 Type II MADS-box gene clades (SEP1, SQUA, TM8, SEP3, FLC, AGL6 and TM3). Gene
39 clustering and gene trees support the idea that these genes are derived from an ancient tandem 40 gene duplication that likely predates the radiation of the seed plants and then expanded by 41 subsequent polyploidy events. We also identified angiosperm-wide conservation of synteny of 42 several other less studied clades. Combined, these findings provide new hypotheses for the
43 genomic origins, biological conservation and divergence of MADS-box gene family members.
Original languageEnglish
Pages (from-to)1278-1292
JournalThe Plant Cell
Volume29
Issue number6
Early online date5 Jun 2017
DOIs
Publication statusPublished - 7 Jul 2017

Fingerprint

Synteny
transposition (genetics)
Transcription Factors
transcription factors
Genes
Plant Genome
genes
Brassicales
Poales
genomics
Angiosperms
Polyploidy
Gene Duplication
genome
gene duplication
Multigene Family
Spermatophytina
Prednisolone
multigene family
polyploidy

Cite this

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title = "Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation",
abstract = "Conserved genomic context provides critical information for comparative evolutionary analysis. 29 With the increase in numbers of sequenced plant genomes, synteny analysis can provide new 30 insight into gene family evolution. Here, we exploit a network analysis approach to organize and31 interpret massive pairwise syntenic relationships. Specifically, we analyzed synteny networks of 32 the MADS-box transcription factor gene family using fifty-one completed plant genomes. In 33 combination with phylogenetic profiling, several novel evolutionary patterns were inferred and 34 visualized from synteny network clusters. We found lineage-specific clusters that derive from 35 transposition events for the regulators of floral development (APETALA3 and PI) and flowering36 time (FLC) in the Brassicales and for the regulators of root-development (AGL17) in Poales. We 37 also identified two large gene clusters that jointly encompass many key phenotypic regulatory 38 Type II MADS-box gene clades (SEP1, SQUA, TM8, SEP3, FLC, AGL6 and TM3). Gene39 clustering and gene trees support the idea that these genes are derived from an ancient tandem 40 gene duplication that likely predates the radiation of the seed plants and then expanded by 41 subsequent polyploidy events. We also identified angiosperm-wide conservation of synteny of 42 several other less studied clades. Combined, these findings provide new hypotheses for the43 genomic origins, biological conservation and divergence of MADS-box gene family members.",
author = "T. Zhao and R. Holmer and {de Bruijn}, S.A. and G.C. Angenent and {van den Burg}, H.A. and M.E. Schranz",
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Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation. / Zhao, T.; Holmer, R.; de Bruijn, S.A.; Angenent, G.C.; van den Burg, H.A.; Schranz, M.E.

In: The Plant Cell, Vol. 29, No. 6, 07.07.2017, p. 1278-1292.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

AU - Zhao, T.

AU - Holmer, R.

AU - de Bruijn, S.A.

AU - Angenent, G.C.

AU - van den Burg, H.A.

AU - Schranz, M.E.

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N2 - Conserved genomic context provides critical information for comparative evolutionary analysis. 29 With the increase in numbers of sequenced plant genomes, synteny analysis can provide new 30 insight into gene family evolution. Here, we exploit a network analysis approach to organize and31 interpret massive pairwise syntenic relationships. Specifically, we analyzed synteny networks of 32 the MADS-box transcription factor gene family using fifty-one completed plant genomes. In 33 combination with phylogenetic profiling, several novel evolutionary patterns were inferred and 34 visualized from synteny network clusters. We found lineage-specific clusters that derive from 35 transposition events for the regulators of floral development (APETALA3 and PI) and flowering36 time (FLC) in the Brassicales and for the regulators of root-development (AGL17) in Poales. We 37 also identified two large gene clusters that jointly encompass many key phenotypic regulatory 38 Type II MADS-box gene clades (SEP1, SQUA, TM8, SEP3, FLC, AGL6 and TM3). Gene39 clustering and gene trees support the idea that these genes are derived from an ancient tandem 40 gene duplication that likely predates the radiation of the seed plants and then expanded by 41 subsequent polyploidy events. We also identified angiosperm-wide conservation of synteny of 42 several other less studied clades. Combined, these findings provide new hypotheses for the43 genomic origins, biological conservation and divergence of MADS-box gene family members.

AB - Conserved genomic context provides critical information for comparative evolutionary analysis. 29 With the increase in numbers of sequenced plant genomes, synteny analysis can provide new 30 insight into gene family evolution. Here, we exploit a network analysis approach to organize and31 interpret massive pairwise syntenic relationships. Specifically, we analyzed synteny networks of 32 the MADS-box transcription factor gene family using fifty-one completed plant genomes. In 33 combination with phylogenetic profiling, several novel evolutionary patterns were inferred and 34 visualized from synteny network clusters. We found lineage-specific clusters that derive from 35 transposition events for the regulators of floral development (APETALA3 and PI) and flowering36 time (FLC) in the Brassicales and for the regulators of root-development (AGL17) in Poales. We 37 also identified two large gene clusters that jointly encompass many key phenotypic regulatory 38 Type II MADS-box gene clades (SEP1, SQUA, TM8, SEP3, FLC, AGL6 and TM3). Gene39 clustering and gene trees support the idea that these genes are derived from an ancient tandem 40 gene duplication that likely predates the radiation of the seed plants and then expanded by 41 subsequent polyploidy events. We also identified angiosperm-wide conservation of synteny of 42 several other less studied clades. Combined, these findings provide new hypotheses for the43 genomic origins, biological conservation and divergence of MADS-box gene family members.

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