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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.


Related in: MedlinePlus

The gene expression of some pairs of LRR-RLP/SPUF genes is coordinated. (A,B) The average levels of gene expression measured in poplar leaves (non-wounded condition) and in excised leaf disks (wounded condition) with oligoarrays are compared for the considered LRR-RLP(A) and SPUF(B) genes. Error bar: SE, n = 6. The linear regression and associated values are indicated for each graph. Colored points are further discussed in the text and in the parts (C,D). The complete transcriptome dataset is available in Table S1C. (C) Cluster 11 (C11), a sub-part of Super-Cluster 5 (SC5), and Cluster 15 (C15) associated with a pair of LRR-RLP/SPUF genes from chromosome 12 (Chr.12) are depicted (for color code and gene model IDs, see Figure 2 and the legend of Figure 4). Green (C11), orange (SC5), and yellow (C15 + Chr.12) dots under gene models indicate a co-expression of LRR-RLP and SPUF genes in poplar leaves, as shown in (A,B). (D)RISP and LRR-RLP genes from scaffold 580 (Phytozome ID Poptr_0580s00210 and Poptr_0580s00200, respectively), are the closest paralogs of RISP-Like and LRR-RLP9 genes from chromosome 9 (Phytozome ID Poptr_0009s11500 and Poptr_0009s11510), respectively. Bars and associated numbers indicate the percentage of amino acid identity. Red and blue dots under RISP and LRR-RLP9 genes indicate their co-induction as shown in (A,B).
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Figure 5: The gene expression of some pairs of LRR-RLP/SPUF genes is coordinated. (A,B) The average levels of gene expression measured in poplar leaves (non-wounded condition) and in excised leaf disks (wounded condition) with oligoarrays are compared for the considered LRR-RLP(A) and SPUF(B) genes. Error bar: SE, n = 6. The linear regression and associated values are indicated for each graph. Colored points are further discussed in the text and in the parts (C,D). The complete transcriptome dataset is available in Table S1C. (C) Cluster 11 (C11), a sub-part of Super-Cluster 5 (SC5), and Cluster 15 (C15) associated with a pair of LRR-RLP/SPUF genes from chromosome 12 (Chr.12) are depicted (for color code and gene model IDs, see Figure 2 and the legend of Figure 4). Green (C11), orange (SC5), and yellow (C15 + Chr.12) dots under gene models indicate a co-expression of LRR-RLP and SPUF genes in poplar leaves, as shown in (A,B). (D)RISP and LRR-RLP genes from scaffold 580 (Phytozome ID Poptr_0580s00210 and Poptr_0580s00200, respectively), are the closest paralogs of RISP-Like and LRR-RLP9 genes from chromosome 9 (Phytozome ID Poptr_0009s11500 and Poptr_0009s11510), respectively. Bars and associated numbers indicate the percentage of amino acid identity. Red and blue dots under RISP and LRR-RLP9 genes indicate their co-induction as shown in (A,B).

Mentions: Some families of SPUFs are gathered into the same LRR-RLP clusters. The left-hand part of the figure presents a phylogenetic tree computed from poplar SPUF sequences. Sequence IDs of SPUFs are colored as their clustered LRR-RLPs in Figure 2. Vertical bars indicate close sequences for which gene models are physically associated within LRR-RLP clusters. Thick bars indicate examples presented in details in Figure 5D (black bar) or on the right-hand part of the figure (green and cyan bars). On the right-hand of the figure, the green rectangle presents a sub-part of Super-Cluster 5 (SC5), whereas the cyan rectangle presents the Cluster 15 (C15) as well as a SPUF/LRR-RLP pair from chromosome 12 (Chr. 12). The color code for arrows is as described in Figure 2. The last numbers of gene model IDs are indicated. Red bars and corresponding numbers indicate the percentage of amino acid identity between the protein products of the SPUF genes. The inserts in the black rectangles present SPUF alignments. Blue and red colors indicate a minimum of 50 and 90% of amino acid identity per position, respectively.


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)

The gene expression of some pairs of LRR-RLP/SPUF genes is coordinated. (A,B) The average levels of gene expression measured in poplar leaves (non-wounded condition) and in excised leaf disks (wounded condition) with oligoarrays are compared for the considered LRR-RLP(A) and SPUF(B) genes. Error bar: SE, n = 6. The linear regression and associated values are indicated for each graph. Colored points are further discussed in the text and in the parts (C,D). The complete transcriptome dataset is available in Table S1C. (C) Cluster 11 (C11), a sub-part of Super-Cluster 5 (SC5), and Cluster 15 (C15) associated with a pair of LRR-RLP/SPUF genes from chromosome 12 (Chr.12) are depicted (for color code and gene model IDs, see Figure 2 and the legend of Figure 4). Green (C11), orange (SC5), and yellow (C15 + Chr.12) dots under gene models indicate a co-expression of LRR-RLP and SPUF genes in poplar leaves, as shown in (A,B). (D)RISP and LRR-RLP genes from scaffold 580 (Phytozome ID Poptr_0580s00210 and Poptr_0580s00200, respectively), are the closest paralogs of RISP-Like and LRR-RLP9 genes from chromosome 9 (Phytozome ID Poptr_0009s11500 and Poptr_0009s11510), respectively. Bars and associated numbers indicate the percentage of amino acid identity. Red and blue dots under RISP and LRR-RLP9 genes indicate their co-induction as shown in (A,B).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3975113&req=5

Figure 5: The gene expression of some pairs of LRR-RLP/SPUF genes is coordinated. (A,B) The average levels of gene expression measured in poplar leaves (non-wounded condition) and in excised leaf disks (wounded condition) with oligoarrays are compared for the considered LRR-RLP(A) and SPUF(B) genes. Error bar: SE, n = 6. The linear regression and associated values are indicated for each graph. Colored points are further discussed in the text and in the parts (C,D). The complete transcriptome dataset is available in Table S1C. (C) Cluster 11 (C11), a sub-part of Super-Cluster 5 (SC5), and Cluster 15 (C15) associated with a pair of LRR-RLP/SPUF genes from chromosome 12 (Chr.12) are depicted (for color code and gene model IDs, see Figure 2 and the legend of Figure 4). Green (C11), orange (SC5), and yellow (C15 + Chr.12) dots under gene models indicate a co-expression of LRR-RLP and SPUF genes in poplar leaves, as shown in (A,B). (D)RISP and LRR-RLP genes from scaffold 580 (Phytozome ID Poptr_0580s00210 and Poptr_0580s00200, respectively), are the closest paralogs of RISP-Like and LRR-RLP9 genes from chromosome 9 (Phytozome ID Poptr_0009s11500 and Poptr_0009s11510), respectively. Bars and associated numbers indicate the percentage of amino acid identity. Red and blue dots under RISP and LRR-RLP9 genes indicate their co-induction as shown in (A,B).
Mentions: Some families of SPUFs are gathered into the same LRR-RLP clusters. The left-hand part of the figure presents a phylogenetic tree computed from poplar SPUF sequences. Sequence IDs of SPUFs are colored as their clustered LRR-RLPs in Figure 2. Vertical bars indicate close sequences for which gene models are physically associated within LRR-RLP clusters. Thick bars indicate examples presented in details in Figure 5D (black bar) or on the right-hand part of the figure (green and cyan bars). On the right-hand of the figure, the green rectangle presents a sub-part of Super-Cluster 5 (SC5), whereas the cyan rectangle presents the Cluster 15 (C15) as well as a SPUF/LRR-RLP pair from chromosome 12 (Chr. 12). The color code for arrows is as described in Figure 2. The last numbers of gene model IDs are indicated. Red bars and corresponding numbers indicate the percentage of amino acid identity between the protein products of the SPUF genes. The inserts in the black rectangles present SPUF alignments. Blue and red colors indicate a minimum of 50 and 90% of amino acid identity per position, respectively.

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.


Related in: MedlinePlus