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Genome analysis of poplar LRR-RLP gene clusters reveals RISP, a defense-related gene coding a candidate endogenous peptide elicitor.

Petre B, Hacquard S, Duplessis S, Rouhier N - Front Plant Sci (2014)

Bottom Line: In these clusters, LRR-RLP genes are interspersed by orphan, poplar-specific genes encoding small proteins of unknown function (SPUFs).In particular, the nine largest clusters of LRR-RLP genes (47 LRR-RLPs) include 71 SPUF genes that account for 59% of the non-LRR-RLP gene content within these clusters.Both gene promoters share a highly conserved region of ~300 nucleotides.

View Article: PubMed Central - PubMed

Affiliation: INRA, Interactions Arbres/Microorganismes, UMR 1136 Champenoux, France ; Université de Lorraine, Interactions Arbres/Microorganismes, UMR 1136 Vandoeuvre-lès-Nancy, France.

ABSTRACT
In plants, cell-surface receptors control immunity and development through the recognition of extracellular ligands. Leucine-rich repeat receptor-like proteins (LRR-RLPs) constitute a large multigene family of cell-surface receptors. Although this family has been intensively studied, a limited number of ligands has been identified so far, mostly because methods used for their identification and characterization are complex and fastidious. In this study, we combined genome and transcriptome analyses to describe the LRR-RLP gene family in the model tree poplar (Populus trichocarpa). In total, 82 LRR-RLP genes have been identified in P. trichocarpa genome, among which 66 are organized in clusters of up to seven members. In these clusters, LRR-RLP genes are interspersed by orphan, poplar-specific genes encoding small proteins of unknown function (SPUFs). In particular, the nine largest clusters of LRR-RLP genes (47 LRR-RLPs) include 71 SPUF genes that account for 59% of the non-LRR-RLP gene content within these clusters. Forty-four LRR-RLP and 55 SPUF genes are expressed in poplar leaves, mostly at low levels, except for members of some clusters that show higher and sometimes coordinated expression levels. Notably, wounding of poplar leaves strongly induced the expression of a defense SPUF gene named Rust-Induced Secreted protein (RISP) that has been previously reported as a marker of poplar defense responses. Interestingly, we show that the RISP-associated LRR-RLP gene is highly expressed in poplar leaves and slightly induced by wounding. Both gene promoters share a highly conserved region of ~300 nucleotides. This led us to hypothesize that the corresponding pair of proteins could be involved in poplar immunity, possibly as a ligand/receptor couple. In conclusion, we speculate that some poplar SPUFs, such as RISP, represent candidate endogenous peptide ligands of the associated LRR-RLPs and we discuss how to investigate further this hypothesis.

No MeSH data available.


Poplar and arabidopsis LRR-RLP families evolved independently. (A) Alignment of the protein sequences of the 82 and 45 LRR-RLP from poplar and A. thaliana, respectively. Blue and red colors indicate a minimum of 50 and 90% of amino acid identity per position, respectively. The canonical domains of tomato Cf-9-like LRR-RLPs described by Fritz-Laylin et al. (2005) are indicated above the alignment. The asterisks mark the domains that are variable in size and position within the alignment; they have been arbitrarily adjusted to correspond to the sequence of poplar LRR-RLP9 (see text). The C3 and D domains, conserved in all sequences, are indicated in red and have been used for performing the phylogenetic analysis presented in (B). LRR, Leucine-Rich Repeat; Cys, Cysteine; TM, Trans-Membrane. (B) Phylogenetic tree of poplar and A. thaliana LRR-RLP families. The analysis was done with the C3-D domains presented in (A). Poplar sequences are highlighted in green, whereas arabidopsis sequences are in blue. Main nodes with Approximate Likelihood-Ratio Test (aLRT) values superior to 0.7 are marked with an asterisk.
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Figure 1: Poplar and arabidopsis LRR-RLP families evolved independently. (A) Alignment of the protein sequences of the 82 and 45 LRR-RLP from poplar and A. thaliana, respectively. Blue and red colors indicate a minimum of 50 and 90% of amino acid identity per position, respectively. The canonical domains of tomato Cf-9-like LRR-RLPs described by Fritz-Laylin et al. (2005) are indicated above the alignment. The asterisks mark the domains that are variable in size and position within the alignment; they have been arbitrarily adjusted to correspond to the sequence of poplar LRR-RLP9 (see text). The C3 and D domains, conserved in all sequences, are indicated in red and have been used for performing the phylogenetic analysis presented in (B). LRR, Leucine-Rich Repeat; Cys, Cysteine; TM, Trans-Membrane. (B) Phylogenetic tree of poplar and A. thaliana LRR-RLP families. The analysis was done with the C3-D domains presented in (A). Poplar sequences are highlighted in green, whereas arabidopsis sequences are in blue. Main nodes with Approximate Likelihood-Ratio Test (aLRT) values superior to 0.7 are marked with an asterisk.

Mentions: A total of 82 LRR-RLP genes were identified in the poplar genome (Table 1; Table S1A). This value is in the range of those reported in A. thaliana and rice, 57 and 90, respectively (Fritz-Laylin et al., 2005; Wang et al., 2008). LRR-RLPs are composed of several domains numbered from A to G (Fritz-Laylin et al., 2005). Domains such as the LRR domain C1 or the linker domain C2 have a variable number of repeats. In contrast, the LRR domain C3 and the linker domain D are conserved and are thus suitable for sequence comparison and phylogenetic analyses (Figure 1A). A phylogenetic tree was inferred with the C3 and D domains of poplar and A. thaliana LRR-RLPs (Figure 1B). Sequences from each species gather within a few well-separated clades, highlighting the strong divergence of the two families and their probable independent evolution in poplar and A. thaliana. A phylogenetic tree focusing only on poplar LRR-RLPs revealed that 81 of the 82 sequences group into four distinct clades termed a, b, c, and d (Figure 2A). LRR-RLP genomic organization correlates with phylogeny, since genes that cluster in the genome sequence gather in the same phylogenetic clade. For instance, the six LRR-RLPs from chromosome 15 are all grouped into the clade c, whereas the seven LRR-RLPs from chromosome 5 are found in the clade d. A more accurate analysis of gene positions revealed that 66 of the 82 LRR-RLPs are organized in 23 clusters or super-clusters (Table 1). A cluster is constituted by at least two genes within a 50 kb stretch, whereas a super-cluster refers to a group of at least two clusters separated by less than 2 Mb. The nine largest clusters or super-clusters gathering 47 LRR-RLPs (57% of the family) are depicted in Figure 2B.


Genome analysis of poplar LRR-RLP gene clusters reveals RISP, a defense-related gene coding a candidate endogenous peptide elicitor.

Petre B, Hacquard S, Duplessis S, Rouhier N - Front Plant Sci (2014)

Poplar and arabidopsis LRR-RLP families evolved independently. (A) Alignment of the protein sequences of the 82 and 45 LRR-RLP from poplar and A. thaliana, respectively. Blue and red colors indicate a minimum of 50 and 90% of amino acid identity per position, respectively. The canonical domains of tomato Cf-9-like LRR-RLPs described by Fritz-Laylin et al. (2005) are indicated above the alignment. The asterisks mark the domains that are variable in size and position within the alignment; they have been arbitrarily adjusted to correspond to the sequence of poplar LRR-RLP9 (see text). The C3 and D domains, conserved in all sequences, are indicated in red and have been used for performing the phylogenetic analysis presented in (B). LRR, Leucine-Rich Repeat; Cys, Cysteine; TM, Trans-Membrane. (B) Phylogenetic tree of poplar and A. thaliana LRR-RLP families. The analysis was done with the C3-D domains presented in (A). Poplar sequences are highlighted in green, whereas arabidopsis sequences are in blue. Main nodes with Approximate Likelihood-Ratio Test (aLRT) values superior to 0.7 are marked with an asterisk.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 1: Poplar and arabidopsis LRR-RLP families evolved independently. (A) Alignment of the protein sequences of the 82 and 45 LRR-RLP from poplar and A. thaliana, respectively. Blue and red colors indicate a minimum of 50 and 90% of amino acid identity per position, respectively. The canonical domains of tomato Cf-9-like LRR-RLPs described by Fritz-Laylin et al. (2005) are indicated above the alignment. The asterisks mark the domains that are variable in size and position within the alignment; they have been arbitrarily adjusted to correspond to the sequence of poplar LRR-RLP9 (see text). The C3 and D domains, conserved in all sequences, are indicated in red and have been used for performing the phylogenetic analysis presented in (B). LRR, Leucine-Rich Repeat; Cys, Cysteine; TM, Trans-Membrane. (B) Phylogenetic tree of poplar and A. thaliana LRR-RLP families. The analysis was done with the C3-D domains presented in (A). Poplar sequences are highlighted in green, whereas arabidopsis sequences are in blue. Main nodes with Approximate Likelihood-Ratio Test (aLRT) values superior to 0.7 are marked with an asterisk.
Mentions: A total of 82 LRR-RLP genes were identified in the poplar genome (Table 1; Table S1A). This value is in the range of those reported in A. thaliana and rice, 57 and 90, respectively (Fritz-Laylin et al., 2005; Wang et al., 2008). LRR-RLPs are composed of several domains numbered from A to G (Fritz-Laylin et al., 2005). Domains such as the LRR domain C1 or the linker domain C2 have a variable number of repeats. In contrast, the LRR domain C3 and the linker domain D are conserved and are thus suitable for sequence comparison and phylogenetic analyses (Figure 1A). A phylogenetic tree was inferred with the C3 and D domains of poplar and A. thaliana LRR-RLPs (Figure 1B). Sequences from each species gather within a few well-separated clades, highlighting the strong divergence of the two families and their probable independent evolution in poplar and A. thaliana. A phylogenetic tree focusing only on poplar LRR-RLPs revealed that 81 of the 82 sequences group into four distinct clades termed a, b, c, and d (Figure 2A). LRR-RLP genomic organization correlates with phylogeny, since genes that cluster in the genome sequence gather in the same phylogenetic clade. For instance, the six LRR-RLPs from chromosome 15 are all grouped into the clade c, whereas the seven LRR-RLPs from chromosome 5 are found in the clade d. A more accurate analysis of gene positions revealed that 66 of the 82 LRR-RLPs are organized in 23 clusters or super-clusters (Table 1). A cluster is constituted by at least two genes within a 50 kb stretch, whereas a super-cluster refers to a group of at least two clusters separated by less than 2 Mb. The nine largest clusters or super-clusters gathering 47 LRR-RLPs (57% of the family) are depicted in Figure 2B.

Bottom Line: In these clusters, LRR-RLP genes are interspersed by orphan, poplar-specific genes encoding small proteins of unknown function (SPUFs).In particular, the nine largest clusters of LRR-RLP genes (47 LRR-RLPs) include 71 SPUF genes that account for 59% of the non-LRR-RLP gene content within these clusters.Both gene promoters share a highly conserved region of ~300 nucleotides.

View Article: PubMed Central - PubMed

Affiliation: INRA, Interactions Arbres/Microorganismes, UMR 1136 Champenoux, France ; Université de Lorraine, Interactions Arbres/Microorganismes, UMR 1136 Vandoeuvre-lès-Nancy, France.

ABSTRACT
In plants, cell-surface receptors control immunity and development through the recognition of extracellular ligands. Leucine-rich repeat receptor-like proteins (LRR-RLPs) constitute a large multigene family of cell-surface receptors. Although this family has been intensively studied, a limited number of ligands has been identified so far, mostly because methods used for their identification and characterization are complex and fastidious. In this study, we combined genome and transcriptome analyses to describe the LRR-RLP gene family in the model tree poplar (Populus trichocarpa). In total, 82 LRR-RLP genes have been identified in P. trichocarpa genome, among which 66 are organized in clusters of up to seven members. In these clusters, LRR-RLP genes are interspersed by orphan, poplar-specific genes encoding small proteins of unknown function (SPUFs). In particular, the nine largest clusters of LRR-RLP genes (47 LRR-RLPs) include 71 SPUF genes that account for 59% of the non-LRR-RLP gene content within these clusters. Forty-four LRR-RLP and 55 SPUF genes are expressed in poplar leaves, mostly at low levels, except for members of some clusters that show higher and sometimes coordinated expression levels. Notably, wounding of poplar leaves strongly induced the expression of a defense SPUF gene named Rust-Induced Secreted protein (RISP) that has been previously reported as a marker of poplar defense responses. Interestingly, we show that the RISP-associated LRR-RLP gene is highly expressed in poplar leaves and slightly induced by wounding. Both gene promoters share a highly conserved region of ~300 nucleotides. This led us to hypothesize that the corresponding pair of proteins could be involved in poplar immunity, possibly as a ligand/receptor couple. In conclusion, we speculate that some poplar SPUFs, such as RISP, represent candidate endogenous peptide ligands of the associated LRR-RLPs and we discuss how to investigate further this hypothesis.

No MeSH data available.