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The WUS homeobox-containing (WOX) protein family.

van der Graaff E, Laux T, Rensing SA - Genome Biol. (2009)

Bottom Line: The prototypic WOX-family member WUS has recently been shown to act as a bifunctional transcription factor, functioning as repressor in stem-cell regulation and as activator in floral patterning.Past research has mainly focused on part of the WOX protein family in some model flowering plants, such as Arabidopsis thaliana (thale cress) or Oryza sativa (rice).Future research, including so-far neglected clades and non-flowering plants, is expected to reveal how these master switches of plant differentiation and embryonic patterning evolved and how they fulfill their function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biology III, Faculty of Biology, University of Freiburg, Schänzlestrasse 1, D-79104 Freiburg, Germany.

ABSTRACT
The WOX genes form a plant-specific subclade of the eukaryotic homeobox transcription factor superfamily, which is characterized by the presence of a conserved DNA-binding homeodomain. The analysis of WOX gene expression and function shows that WOX family members fulfill specialized functions in key developmental processes in plants, such as embryonic patterning, stem-cell maintenance and organ formation. These functions can be related to either promotion of cell division activity and/or prevention of premature cell differentiation. The phylogenetic tree of the plant WOX proteins can be divided into three clades, termed the WUS, intermediate and ancient clade. WOX proteins of the WUS clade appear to some extent able to functionally complement other members. The specific function of individual WOX-family proteins is most probably determined by their spatiotemporal expression pattern and probably also by their interaction with other proteins, which may repress their transcriptional activity. The prototypic WOX-family member WUS has recently been shown to act as a bifunctional transcription factor, functioning as repressor in stem-cell regulation and as activator in floral patterning. Past research has mainly focused on part of the WOX protein family in some model flowering plants, such as Arabidopsis thaliana (thale cress) or Oryza sativa (rice). Future research, including so-far neglected clades and non-flowering plants, is expected to reveal how these master switches of plant differentiation and embryonic patterning evolved and how they fulfill their function.

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Phylogenetic relationships of WOX family proteins. (a) Relationship of the WOX family to the other members of the HB transcription factor superfamily. Proteins matching the PFAM Homeodomain hidden Markov model (PF00046) [9] were retrieved from completely sequenced genomes of plants, animals, algae and non-photosynthetic protists and subjected to multiple sequence alignment using MAFFT [50]. After manual removal of nonconserved regions, essentially resulting in an alignment of homeodomains, phylogenetic inference was conducted using quicktree_sd [51,52]. Subsequent midpoint-rooting and visualization was performed using FigTree v1.2.2 [53]. Branch width corresponds to bootstrap support. The WOX family is in red. Other HB protein families consisting exclusively of proteins from one of the three kingdoms are colored in green (plants), blue (animals) and cyan (fungi), respectively. Families specific to opisthokonts (animals and fungi) are colored in brown (these clusters contain occasional protist sequences, for example, from Mycetozoa and Amoebozoa). Families indicated in black consist of members from both plants and opisthokonts or contain significant amounts of protist (algal, protozoan) sequences. (b) The WOX protein family. Proteins from genomes of completely sequenced plant and algal species were used to generate this phylogeny, which is essentially a representation of the red clade from (a). After manual removal of regions of low alignment quality, phylogenetic inference was conducted using MrBayes [54]. Branch width corresponds to support values; the A. thaliana proteins are shown in red. The three subclades are color-coded, WUS/WOX1-7 (WUS) in purple, WOX8, 9, 11, 12 (intermediate) in orange and WOX10, 13, 14 (ancient) in green.
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Figure 1: Phylogenetic relationships of WOX family proteins. (a) Relationship of the WOX family to the other members of the HB transcription factor superfamily. Proteins matching the PFAM Homeodomain hidden Markov model (PF00046) [9] were retrieved from completely sequenced genomes of plants, animals, algae and non-photosynthetic protists and subjected to multiple sequence alignment using MAFFT [50]. After manual removal of nonconserved regions, essentially resulting in an alignment of homeodomains, phylogenetic inference was conducted using quicktree_sd [51,52]. Subsequent midpoint-rooting and visualization was performed using FigTree v1.2.2 [53]. Branch width corresponds to bootstrap support. The WOX family is in red. Other HB protein families consisting exclusively of proteins from one of the three kingdoms are colored in green (plants), blue (animals) and cyan (fungi), respectively. Families specific to opisthokonts (animals and fungi) are colored in brown (these clusters contain occasional protist sequences, for example, from Mycetozoa and Amoebozoa). Families indicated in black consist of members from both plants and opisthokonts or contain significant amounts of protist (algal, protozoan) sequences. (b) The WOX protein family. Proteins from genomes of completely sequenced plant and algal species were used to generate this phylogeny, which is essentially a representation of the red clade from (a). After manual removal of regions of low alignment quality, phylogenetic inference was conducted using MrBayes [54]. Branch width corresponds to support values; the A. thaliana proteins are shown in red. The three subclades are color-coded, WUS/WOX1-7 (WUS) in purple, WOX8, 9, 11, 12 (intermediate) in orange and WOX10, 13, 14 (ancient) in green.

Mentions: Phylogenetic reconstruction of protein sequences that contain the homeodomain as defined by the PFAM database [8,9] (Figure 1a) reveals that this DNA-binding motif probably originated before the divergence of the eukaryotes [5]. (The PFAM-defined homeodomain is the one referred to throughout this article.) The last common ancestor of all extant eukaryotes probably already harbored several HB proteins (see Figure 1a). These were subsequently subject to loss as well as expansion among different lineages and diversified in function. However, because of the short length of the homeodomain, convergent evolution (evolution leading to similar sequences that lack a common ancestor) due to structural constraints imposed by a requirement for DNA binding, for example, cannot be excluded. This might explain some surprising appearances of HB proteins from different taxonomic groups within families that otherwise are apparently specific to a certain lineage (see Figure 1a).


The WUS homeobox-containing (WOX) protein family.

van der Graaff E, Laux T, Rensing SA - Genome Biol. (2009)

Phylogenetic relationships of WOX family proteins. (a) Relationship of the WOX family to the other members of the HB transcription factor superfamily. Proteins matching the PFAM Homeodomain hidden Markov model (PF00046) [9] were retrieved from completely sequenced genomes of plants, animals, algae and non-photosynthetic protists and subjected to multiple sequence alignment using MAFFT [50]. After manual removal of nonconserved regions, essentially resulting in an alignment of homeodomains, phylogenetic inference was conducted using quicktree_sd [51,52]. Subsequent midpoint-rooting and visualization was performed using FigTree v1.2.2 [53]. Branch width corresponds to bootstrap support. The WOX family is in red. Other HB protein families consisting exclusively of proteins from one of the three kingdoms are colored in green (plants), blue (animals) and cyan (fungi), respectively. Families specific to opisthokonts (animals and fungi) are colored in brown (these clusters contain occasional protist sequences, for example, from Mycetozoa and Amoebozoa). Families indicated in black consist of members from both plants and opisthokonts or contain significant amounts of protist (algal, protozoan) sequences. (b) The WOX protein family. Proteins from genomes of completely sequenced plant and algal species were used to generate this phylogeny, which is essentially a representation of the red clade from (a). After manual removal of regions of low alignment quality, phylogenetic inference was conducted using MrBayes [54]. Branch width corresponds to support values; the A. thaliana proteins are shown in red. The three subclades are color-coded, WUS/WOX1-7 (WUS) in purple, WOX8, 9, 11, 12 (intermediate) in orange and WOX10, 13, 14 (ancient) in green.
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Figure 1: Phylogenetic relationships of WOX family proteins. (a) Relationship of the WOX family to the other members of the HB transcription factor superfamily. Proteins matching the PFAM Homeodomain hidden Markov model (PF00046) [9] were retrieved from completely sequenced genomes of plants, animals, algae and non-photosynthetic protists and subjected to multiple sequence alignment using MAFFT [50]. After manual removal of nonconserved regions, essentially resulting in an alignment of homeodomains, phylogenetic inference was conducted using quicktree_sd [51,52]. Subsequent midpoint-rooting and visualization was performed using FigTree v1.2.2 [53]. Branch width corresponds to bootstrap support. The WOX family is in red. Other HB protein families consisting exclusively of proteins from one of the three kingdoms are colored in green (plants), blue (animals) and cyan (fungi), respectively. Families specific to opisthokonts (animals and fungi) are colored in brown (these clusters contain occasional protist sequences, for example, from Mycetozoa and Amoebozoa). Families indicated in black consist of members from both plants and opisthokonts or contain significant amounts of protist (algal, protozoan) sequences. (b) The WOX protein family. Proteins from genomes of completely sequenced plant and algal species were used to generate this phylogeny, which is essentially a representation of the red clade from (a). After manual removal of regions of low alignment quality, phylogenetic inference was conducted using MrBayes [54]. Branch width corresponds to support values; the A. thaliana proteins are shown in red. The three subclades are color-coded, WUS/WOX1-7 (WUS) in purple, WOX8, 9, 11, 12 (intermediate) in orange and WOX10, 13, 14 (ancient) in green.
Mentions: Phylogenetic reconstruction of protein sequences that contain the homeodomain as defined by the PFAM database [8,9] (Figure 1a) reveals that this DNA-binding motif probably originated before the divergence of the eukaryotes [5]. (The PFAM-defined homeodomain is the one referred to throughout this article.) The last common ancestor of all extant eukaryotes probably already harbored several HB proteins (see Figure 1a). These were subsequently subject to loss as well as expansion among different lineages and diversified in function. However, because of the short length of the homeodomain, convergent evolution (evolution leading to similar sequences that lack a common ancestor) due to structural constraints imposed by a requirement for DNA binding, for example, cannot be excluded. This might explain some surprising appearances of HB proteins from different taxonomic groups within families that otherwise are apparently specific to a certain lineage (see Figure 1a).

Bottom Line: The prototypic WOX-family member WUS has recently been shown to act as a bifunctional transcription factor, functioning as repressor in stem-cell regulation and as activator in floral patterning.Past research has mainly focused on part of the WOX protein family in some model flowering plants, such as Arabidopsis thaliana (thale cress) or Oryza sativa (rice).Future research, including so-far neglected clades and non-flowering plants, is expected to reveal how these master switches of plant differentiation and embryonic patterning evolved and how they fulfill their function.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biology III, Faculty of Biology, University of Freiburg, Schänzlestrasse 1, D-79104 Freiburg, Germany.

ABSTRACT
The WOX genes form a plant-specific subclade of the eukaryotic homeobox transcription factor superfamily, which is characterized by the presence of a conserved DNA-binding homeodomain. The analysis of WOX gene expression and function shows that WOX family members fulfill specialized functions in key developmental processes in plants, such as embryonic patterning, stem-cell maintenance and organ formation. These functions can be related to either promotion of cell division activity and/or prevention of premature cell differentiation. The phylogenetic tree of the plant WOX proteins can be divided into three clades, termed the WUS, intermediate and ancient clade. WOX proteins of the WUS clade appear to some extent able to functionally complement other members. The specific function of individual WOX-family proteins is most probably determined by their spatiotemporal expression pattern and probably also by their interaction with other proteins, which may repress their transcriptional activity. The prototypic WOX-family member WUS has recently been shown to act as a bifunctional transcription factor, functioning as repressor in stem-cell regulation and as activator in floral patterning. Past research has mainly focused on part of the WOX protein family in some model flowering plants, such as Arabidopsis thaliana (thale cress) or Oryza sativa (rice). Future research, including so-far neglected clades and non-flowering plants, is expected to reveal how these master switches of plant differentiation and embryonic patterning evolved and how they fulfill their function.

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