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Protein subcellular relocalization of duplicated genes in Arabidopsis.

Liu SL, Pan AQ, Adams KL - Genome Biol Evol (2014)

Bottom Line: We identified potential sequence mutations through comparative analysis that likely result in relocalization of two duplicated gene products.We show that four cases of relocalization have new expression patterns, compared with orthologs in outgroup species, including two with novel expression in pollen.This study provides insights into subcellular relocalization of evolutionarily recent gene duplicates and features of genes whose products have been relocalized.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada Present address: Department of Life Science, Tunghai University, Taichung, Taiwan.

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Neolocalization, asymmetric sequence evolution, and gene expression divergence in a pair of VAMP proteins. (A) PAML analysis of VAMP genes. Numbers above the branches indicate the dN/dS ratios. dN analysis is shown in supplementary figure S5, Supplementary Material online. Subcellular localization for the proteins in A. thaliana is highlighted in red. VAMP722 is relocalized from PM/endosome to ER. Species include: At, A. thaliana; Al, Arabidopsis lyrata; Cr, Capsella rubella; Es, Eutrema salsugineum; Br, Brassica rapa; Cp, C. papaya; Gr, G. raimondii; Tc, T. cacao; Pt, P. trichocarpa; Me, M. esculenta; and Vv, V. vinifera. See supplementary figure S5, Supplementary Material online, for locus numbers of each gene. (B) Amino acid alignment showing the position of positively selected sites in the SNARE domain of VAMP723 inferred using the empirical Bayes approach.
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evu191-F4: Neolocalization, asymmetric sequence evolution, and gene expression divergence in a pair of VAMP proteins. (A) PAML analysis of VAMP genes. Numbers above the branches indicate the dN/dS ratios. dN analysis is shown in supplementary figure S5, Supplementary Material online. Subcellular localization for the proteins in A. thaliana is highlighted in red. VAMP722 is relocalized from PM/endosome to ER. Species include: At, A. thaliana; Al, Arabidopsis lyrata; Cr, Capsella rubella; Es, Eutrema salsugineum; Br, Brassica rapa; Cp, C. papaya; Gr, G. raimondii; Tc, T. cacao; Pt, P. trichocarpa; Me, M. esculenta; and Vv, V. vinifera. See supplementary figure S5, Supplementary Material online, for locus numbers of each gene. (B) Amino acid alignment showing the position of positively selected sites in the SNARE domain of VAMP723 inferred using the empirical Bayes approach.

Mentions: One gene pair showing accelerated sequence rate evolution of one copy is the tandemly duplicated gene pair for vesicle-associated membrane proteins VAMP723 (At2g33110) and VAMP722 (At2g33120) that contain SNARE (soluble N-ethylmaleimide sensitive factor receptors) domains (Uemura et al. 2004; Sanderfoot 2007). VAMP722 has two major functions: Involvement in secretory trafficking to the plasma membrane and cell plate formation (Zhang et al. 2011), and contributing to the plant immune response upon the infection with powdery mildew fungi by participating in the formation of an SDS-SNARE complex with the plasma membrane proteins PEN1 and SNAP33 (Kwon et al. 2008); in contrast the function of VAMP723 has not been characterized. We used a gene family approach and GFP subcellular localization data from a study of 54 genes with SNARE domains (Uemura et al. 2004) to infer the ancestral, preduplication, state of localization. We found that there have been multiple duplications of the VAMP72 genes to create five genes in A. thaliana (fig. 4 and supplementary fig. S5, Supplementary Material online). Only VAMP723 is localized to the endoplasmic reticulum (ER), whereas the other four gene products are localized to the plasma membrane and endosome. These results strongly suggest that the ancestral state of localization for the VAMP722/VAMP723 gene pair was to the plasma membrane and endosome, and that VAMP723 has been relocalized to the ER. The relocalization appears to be a relatively recent evolutionary event. Results from our phylogenetic analysis showed that VAMP723 and VAMP722 phylogenetically group together, to the exclusion of the VAMP722 genes from Brassica and Eutrema (fig. 4A), indicating that they are duplicates that formed during evolution of the Arabidopsis lineage after it diverged from the Eutrema lineage.Fig. 4.—


Protein subcellular relocalization of duplicated genes in Arabidopsis.

Liu SL, Pan AQ, Adams KL - Genome Biol Evol (2014)

Neolocalization, asymmetric sequence evolution, and gene expression divergence in a pair of VAMP proteins. (A) PAML analysis of VAMP genes. Numbers above the branches indicate the dN/dS ratios. dN analysis is shown in supplementary figure S5, Supplementary Material online. Subcellular localization for the proteins in A. thaliana is highlighted in red. VAMP722 is relocalized from PM/endosome to ER. Species include: At, A. thaliana; Al, Arabidopsis lyrata; Cr, Capsella rubella; Es, Eutrema salsugineum; Br, Brassica rapa; Cp, C. papaya; Gr, G. raimondii; Tc, T. cacao; Pt, P. trichocarpa; Me, M. esculenta; and Vv, V. vinifera. See supplementary figure S5, Supplementary Material online, for locus numbers of each gene. (B) Amino acid alignment showing the position of positively selected sites in the SNARE domain of VAMP723 inferred using the empirical Bayes approach.
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evu191-F4: Neolocalization, asymmetric sequence evolution, and gene expression divergence in a pair of VAMP proteins. (A) PAML analysis of VAMP genes. Numbers above the branches indicate the dN/dS ratios. dN analysis is shown in supplementary figure S5, Supplementary Material online. Subcellular localization for the proteins in A. thaliana is highlighted in red. VAMP722 is relocalized from PM/endosome to ER. Species include: At, A. thaliana; Al, Arabidopsis lyrata; Cr, Capsella rubella; Es, Eutrema salsugineum; Br, Brassica rapa; Cp, C. papaya; Gr, G. raimondii; Tc, T. cacao; Pt, P. trichocarpa; Me, M. esculenta; and Vv, V. vinifera. See supplementary figure S5, Supplementary Material online, for locus numbers of each gene. (B) Amino acid alignment showing the position of positively selected sites in the SNARE domain of VAMP723 inferred using the empirical Bayes approach.
Mentions: One gene pair showing accelerated sequence rate evolution of one copy is the tandemly duplicated gene pair for vesicle-associated membrane proteins VAMP723 (At2g33110) and VAMP722 (At2g33120) that contain SNARE (soluble N-ethylmaleimide sensitive factor receptors) domains (Uemura et al. 2004; Sanderfoot 2007). VAMP722 has two major functions: Involvement in secretory trafficking to the plasma membrane and cell plate formation (Zhang et al. 2011), and contributing to the plant immune response upon the infection with powdery mildew fungi by participating in the formation of an SDS-SNARE complex with the plasma membrane proteins PEN1 and SNAP33 (Kwon et al. 2008); in contrast the function of VAMP723 has not been characterized. We used a gene family approach and GFP subcellular localization data from a study of 54 genes with SNARE domains (Uemura et al. 2004) to infer the ancestral, preduplication, state of localization. We found that there have been multiple duplications of the VAMP72 genes to create five genes in A. thaliana (fig. 4 and supplementary fig. S5, Supplementary Material online). Only VAMP723 is localized to the endoplasmic reticulum (ER), whereas the other four gene products are localized to the plasma membrane and endosome. These results strongly suggest that the ancestral state of localization for the VAMP722/VAMP723 gene pair was to the plasma membrane and endosome, and that VAMP723 has been relocalized to the ER. The relocalization appears to be a relatively recent evolutionary event. Results from our phylogenetic analysis showed that VAMP723 and VAMP722 phylogenetically group together, to the exclusion of the VAMP722 genes from Brassica and Eutrema (fig. 4A), indicating that they are duplicates that formed during evolution of the Arabidopsis lineage after it diverged from the Eutrema lineage.Fig. 4.—

Bottom Line: We identified potential sequence mutations through comparative analysis that likely result in relocalization of two duplicated gene products.We show that four cases of relocalization have new expression patterns, compared with orthologs in outgroup species, including two with novel expression in pollen.This study provides insights into subcellular relocalization of evolutionarily recent gene duplicates and features of genes whose products have been relocalized.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada Present address: Department of Life Science, Tunghai University, Taichung, Taiwan.

Show MeSH
Related in: MedlinePlus