Segmental and tandem chromosome duplications led to divergent evolution of the chalcone synthase gene family in phalaenopsis orchids

Yi Tzu Kuo, Ya Ting Chao, Wan Chieh Chen, Ming Che Shih, Song Bin Chang

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Abstract

• Background and Aims Orchidaceae is a large plant family, and its extraordinary adaptations may have guaranteed its evolutionary success. Flavonoids are a group of secondary metabolites that mediate plant acclimation to challenge environments. Chalcone synthase (CHS) catalyses the initial step in the flavonoid biosynthetic pathway. This is the first chromosome-level investigation of the CHS gene family in Phalaenopsis aphrodite and was conducted to elucidate if divergence of this gene family is associated with chromosome evolution. • Methods Complete CHS genes were identified from our whole-genome sequencing data sets and their gene expression profiles were obtained from our transcriptomic data sets. Fluorescence in situ hybridization (FISH) was conducted to position five CHS genes to high-resolution pachytene chromosomes. • Key Results The five Phalaenopsis CHS genes can be classified into three groups, PaCHS1, PaCHS2 and the tandemly arrayed three-gene cluster, which diverged earlier than those of the orchid genera and species. Additionally, pachytene chromosome-based FISH mapping showed that the three groups of CHS genes are localized on three distinct chromosomes. Moreover, an expression analysis of RNA sequencing revealed that the five CHS genes had highly differentiated expression patterns and its expression pattern-based clustering showed high correlations between sequence divergences and chromosomal localizations of the CHS gene family in P. aphrodite. • Conclusions Based on their phylogenetic relationships, expression clustering analysis and chromosomal distributions of the five paralogous PaCHS genes, we proposed that expansion of this gene family in P. aphrodite occurred through segmental duplications, followed by tandem duplications. These findings provide information for further studies of CHS functions and regulations, and shed light on the divergence of an important gene family in orchids.

Original languageEnglish
Pages (from-to)69-77
Number of pages9
JournalAnnals of Botany
Volume123
Issue number1
DOIs
Publication statusPublished - 2019 Jan 1

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Phalaenopsis
naringenin-chalcone synthase
divergent evolution
Orchidaceae
chromosomes
genes
pachytene stage
fluorescence in situ hybridization
flavonoids
transcriptomics
multigene family
secondary metabolites
biochemical pathways
acclimation
sequence analysis

All Science Journal Classification (ASJC) codes

  • Plant Science

Cite this

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title = "Segmental and tandem chromosome duplications led to divergent evolution of the chalcone synthase gene family in phalaenopsis orchids",
abstract = "• Background and Aims Orchidaceae is a large plant family, and its extraordinary adaptations may have guaranteed its evolutionary success. Flavonoids are a group of secondary metabolites that mediate plant acclimation to challenge environments. Chalcone synthase (CHS) catalyses the initial step in the flavonoid biosynthetic pathway. This is the first chromosome-level investigation of the CHS gene family in Phalaenopsis aphrodite and was conducted to elucidate if divergence of this gene family is associated with chromosome evolution. • Methods Complete CHS genes were identified from our whole-genome sequencing data sets and their gene expression profiles were obtained from our transcriptomic data sets. Fluorescence in situ hybridization (FISH) was conducted to position five CHS genes to high-resolution pachytene chromosomes. • Key Results The five Phalaenopsis CHS genes can be classified into three groups, PaCHS1, PaCHS2 and the tandemly arrayed three-gene cluster, which diverged earlier than those of the orchid genera and species. Additionally, pachytene chromosome-based FISH mapping showed that the three groups of CHS genes are localized on three distinct chromosomes. Moreover, an expression analysis of RNA sequencing revealed that the five CHS genes had highly differentiated expression patterns and its expression pattern-based clustering showed high correlations between sequence divergences and chromosomal localizations of the CHS gene family in P. aphrodite. • Conclusions Based on their phylogenetic relationships, expression clustering analysis and chromosomal distributions of the five paralogous PaCHS genes, we proposed that expansion of this gene family in P. aphrodite occurred through segmental duplications, followed by tandem duplications. These findings provide information for further studies of CHS functions and regulations, and shed light on the divergence of an important gene family in orchids.",
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Segmental and tandem chromosome duplications led to divergent evolution of the chalcone synthase gene family in phalaenopsis orchids. / Kuo, Yi Tzu; Chao, Ya Ting; Chen, Wan Chieh; Shih, Ming Che; Chang, Song Bin.

In: Annals of Botany, Vol. 123, No. 1, 01.01.2019, p. 69-77.

Research output: Contribution to journalArticle

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T1 - Segmental and tandem chromosome duplications led to divergent evolution of the chalcone synthase gene family in phalaenopsis orchids

AU - Kuo, Yi Tzu

AU - Chao, Ya Ting

AU - Chen, Wan Chieh

AU - Shih, Ming Che

AU - Chang, Song Bin

PY - 2019/1/1

Y1 - 2019/1/1

N2 - • Background and Aims Orchidaceae is a large plant family, and its extraordinary adaptations may have guaranteed its evolutionary success. Flavonoids are a group of secondary metabolites that mediate plant acclimation to challenge environments. Chalcone synthase (CHS) catalyses the initial step in the flavonoid biosynthetic pathway. This is the first chromosome-level investigation of the CHS gene family in Phalaenopsis aphrodite and was conducted to elucidate if divergence of this gene family is associated with chromosome evolution. • Methods Complete CHS genes were identified from our whole-genome sequencing data sets and their gene expression profiles were obtained from our transcriptomic data sets. Fluorescence in situ hybridization (FISH) was conducted to position five CHS genes to high-resolution pachytene chromosomes. • Key Results The five Phalaenopsis CHS genes can be classified into three groups, PaCHS1, PaCHS2 and the tandemly arrayed three-gene cluster, which diverged earlier than those of the orchid genera and species. Additionally, pachytene chromosome-based FISH mapping showed that the three groups of CHS genes are localized on three distinct chromosomes. Moreover, an expression analysis of RNA sequencing revealed that the five CHS genes had highly differentiated expression patterns and its expression pattern-based clustering showed high correlations between sequence divergences and chromosomal localizations of the CHS gene family in P. aphrodite. • Conclusions Based on their phylogenetic relationships, expression clustering analysis and chromosomal distributions of the five paralogous PaCHS genes, we proposed that expansion of this gene family in P. aphrodite occurred through segmental duplications, followed by tandem duplications. These findings provide information for further studies of CHS functions and regulations, and shed light on the divergence of an important gene family in orchids.

AB - • Background and Aims Orchidaceae is a large plant family, and its extraordinary adaptations may have guaranteed its evolutionary success. Flavonoids are a group of secondary metabolites that mediate plant acclimation to challenge environments. Chalcone synthase (CHS) catalyses the initial step in the flavonoid biosynthetic pathway. This is the first chromosome-level investigation of the CHS gene family in Phalaenopsis aphrodite and was conducted to elucidate if divergence of this gene family is associated with chromosome evolution. • Methods Complete CHS genes were identified from our whole-genome sequencing data sets and their gene expression profiles were obtained from our transcriptomic data sets. Fluorescence in situ hybridization (FISH) was conducted to position five CHS genes to high-resolution pachytene chromosomes. • Key Results The five Phalaenopsis CHS genes can be classified into three groups, PaCHS1, PaCHS2 and the tandemly arrayed three-gene cluster, which diverged earlier than those of the orchid genera and species. Additionally, pachytene chromosome-based FISH mapping showed that the three groups of CHS genes are localized on three distinct chromosomes. Moreover, an expression analysis of RNA sequencing revealed that the five CHS genes had highly differentiated expression patterns and its expression pattern-based clustering showed high correlations between sequence divergences and chromosomal localizations of the CHS gene family in P. aphrodite. • Conclusions Based on their phylogenetic relationships, expression clustering analysis and chromosomal distributions of the five paralogous PaCHS genes, we proposed that expansion of this gene family in P. aphrodite occurred through segmental duplications, followed by tandem duplications. These findings provide information for further studies of CHS functions and regulations, and shed light on the divergence of an important gene family in orchids.

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