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Paleo-evolutionary plasticity of plant disease resistance genes.

Zhang R, Murat F, Pont C, Langin T, Salse J - BMC Genomics (2014)

Bottom Line: We unravel in the current article (i) a R-genes repertoire consisting in 7883 for monocots and 15758 for eudicots, (ii) a contrasted R-genes conservation with 23.8% for monocots and 6.6% for dicots, (iii) a minimal ancestral founder pool of 384 R-genes for the monocots and 150 R-genes for the eudicots, (iv) a general pattern of organization in clusters accounting for more than 60% of mapped R-genes, (v) a biased deletion of ancestral duplicated R-genes between paralogous blocks possibly compensated by clusterization, (vi) a bias in R-genes clusterization where Leucine-Rich Repeats act as a 'glue' for domain association, (vii) a R-genes/miRNAs interome enriched toward duplicated R-genes.Together, our data may suggest that R-genes family plasticity operated during plant evolution (i) at the structural level through massive duplicates loss counterbalanced by massive clusterization following polyploidization; as well as at (ii) the regulation level through microRNA/R-gene interactions acting as a possible source of functional diploidization of structurally retained R-genes duplicates.Such evolutionary shuffling events leaded to CNVs (i.e. Copy Number Variation) and PAVs (i.e. Presence Absence Variation) between related species operating in the decay of R-genes colinearity between plant species.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA/UBP UMR 1095 GDEC 'Génétique, Diversité et Ecophysiologie des Céréales', 5 chemin de Beaulieu, 63100 Clermont-Ferrand, France. jsalse@clermont.inra.fr.

ABSTRACT

Background: The recent access to a large set of genome sequences, combined with a robust evolutionary scenario of modern monocot (i.e. grasses) and eudicot (i.e. rosids) species from their founder ancestors, offered the opportunity to gain insights into disease resistance genes (R-genes) evolutionary plasticity.

Results: We unravel in the current article (i) a R-genes repertoire consisting in 7883 for monocots and 15758 for eudicots, (ii) a contrasted R-genes conservation with 23.8% for monocots and 6.6% for dicots, (iii) a minimal ancestral founder pool of 384 R-genes for the monocots and 150 R-genes for the eudicots, (iv) a general pattern of organization in clusters accounting for more than 60% of mapped R-genes, (v) a biased deletion of ancestral duplicated R-genes between paralogous blocks possibly compensated by clusterization, (vi) a bias in R-genes clusterization where Leucine-Rich Repeats act as a 'glue' for domain association, (vii) a R-genes/miRNAs interome enriched toward duplicated R-genes.

Conclusions: Together, our data may suggest that R-genes family plasticity operated during plant evolution (i) at the structural level through massive duplicates loss counterbalanced by massive clusterization following polyploidization; as well as at (ii) the regulation level through microRNA/R-gene interactions acting as a possible source of functional diploidization of structurally retained R-genes duplicates. Such evolutionary shuffling events leaded to CNVs (i.e. Copy Number Variation) and PAVs (i.e. Presence Absence Variation) between related species operating in the decay of R-genes colinearity between plant species.

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R-genes/miRNAs interactome in plants. (A) Illustration of the percentage of R-genes targeted by miRNA in dicots species classified according the number of experienced WGDs (x-axis). The regression curve, correlation and associated P-value are mentioned. (B) Illustration of a micro-synteny locus between cacao (one region) and soybean (four duplicated regions) harboring R-genes targeted by miRNA (according to the number of sequence mismatches between miRNA and R-genes from 4 to 7 identified as miRNA target score and highlighted with a color code at the bottom). Grey bars represent non R-genes. (C) Illustration of the percentage of R-genes targeted by miRNA (y-axis) in dicots (D) and monocots (M) species classified according to the investigated R-domains (LRR, NBS, TIR, WRKY, Pkinase; x-axis).
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Figure 4: R-genes/miRNAs interactome in plants. (A) Illustration of the percentage of R-genes targeted by miRNA in dicots species classified according the number of experienced WGDs (x-axis). The regression curve, correlation and associated P-value are mentioned. (B) Illustration of a micro-synteny locus between cacao (one region) and soybean (four duplicated regions) harboring R-genes targeted by miRNA (according to the number of sequence mismatches between miRNA and R-genes from 4 to 7 identified as miRNA target score and highlighted with a color code at the bottom). Grey bars represent non R-genes. (C) Illustration of the percentage of R-genes targeted by miRNA (y-axis) in dicots (D) and monocots (M) species classified according to the investigated R-domains (LRR, NBS, TIR, WRKY, Pkinase; x-axis).

Mentions: We considered resistance genes as in silico targets of miRNAs based on sequence mismatch scores using Targetfinder algorithm [84] (detailed in Methods section). On average, we characterized 33.31% and 35.60% R-genes predicted as in silico targets of miRNA in monocots and eudicots respectively, significantly higher than for non R-genes with 11.48% and 13.06% respectively (P-value = 9.013e-05 in paired student t-test, Additional file 1: Table S10). No highly significant differences where observed between non-conserved and conserved R-genes targeted in silico by miRNAs in monocot (Table 2). In eudicots, these differences (P-value = 3.48E-02 between conserved and non-conserved miRNA-targeted resistance genes) are likely to be associated with the numerous rounds of WGD. We observed a correlation (r = 0.7133 with P-value = 0.03) between the number of WGD rounds and the number of in silico miRNA/R-gene interactions that took place in the plant paleohistory (Figure 4A). This observation may suggest that successive WGDs may have increased or putatively shaped the R-gene/miRNA in silico interactome. After recent WGDs, for example, in soybean, ~50% of retained R-genes (Figure 4B) are potential targeted by miRNAs with mismatch score of < = 4. One explanation could be that additional species-specific R-genes copies (deriving from lineage-specific WGDs), then leading to R-gene functional redundancy, may be repressed at the expressional level through miRNAs. Such suggested impact of miRNA regulation on duplicated R-genes expression may need to be biologically and functionally validated.


Paleo-evolutionary plasticity of plant disease resistance genes.

Zhang R, Murat F, Pont C, Langin T, Salse J - BMC Genomics (2014)

R-genes/miRNAs interactome in plants. (A) Illustration of the percentage of R-genes targeted by miRNA in dicots species classified according the number of experienced WGDs (x-axis). The regression curve, correlation and associated P-value are mentioned. (B) Illustration of a micro-synteny locus between cacao (one region) and soybean (four duplicated regions) harboring R-genes targeted by miRNA (according to the number of sequence mismatches between miRNA and R-genes from 4 to 7 identified as miRNA target score and highlighted with a color code at the bottom). Grey bars represent non R-genes. (C) Illustration of the percentage of R-genes targeted by miRNA (y-axis) in dicots (D) and monocots (M) species classified according to the investigated R-domains (LRR, NBS, TIR, WRKY, Pkinase; x-axis).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4234491&req=5

Figure 4: R-genes/miRNAs interactome in plants. (A) Illustration of the percentage of R-genes targeted by miRNA in dicots species classified according the number of experienced WGDs (x-axis). The regression curve, correlation and associated P-value are mentioned. (B) Illustration of a micro-synteny locus between cacao (one region) and soybean (four duplicated regions) harboring R-genes targeted by miRNA (according to the number of sequence mismatches between miRNA and R-genes from 4 to 7 identified as miRNA target score and highlighted with a color code at the bottom). Grey bars represent non R-genes. (C) Illustration of the percentage of R-genes targeted by miRNA (y-axis) in dicots (D) and monocots (M) species classified according to the investigated R-domains (LRR, NBS, TIR, WRKY, Pkinase; x-axis).
Mentions: We considered resistance genes as in silico targets of miRNAs based on sequence mismatch scores using Targetfinder algorithm [84] (detailed in Methods section). On average, we characterized 33.31% and 35.60% R-genes predicted as in silico targets of miRNA in monocots and eudicots respectively, significantly higher than for non R-genes with 11.48% and 13.06% respectively (P-value = 9.013e-05 in paired student t-test, Additional file 1: Table S10). No highly significant differences where observed between non-conserved and conserved R-genes targeted in silico by miRNAs in monocot (Table 2). In eudicots, these differences (P-value = 3.48E-02 between conserved and non-conserved miRNA-targeted resistance genes) are likely to be associated with the numerous rounds of WGD. We observed a correlation (r = 0.7133 with P-value = 0.03) between the number of WGD rounds and the number of in silico miRNA/R-gene interactions that took place in the plant paleohistory (Figure 4A). This observation may suggest that successive WGDs may have increased or putatively shaped the R-gene/miRNA in silico interactome. After recent WGDs, for example, in soybean, ~50% of retained R-genes (Figure 4B) are potential targeted by miRNAs with mismatch score of < = 4. One explanation could be that additional species-specific R-genes copies (deriving from lineage-specific WGDs), then leading to R-gene functional redundancy, may be repressed at the expressional level through miRNAs. Such suggested impact of miRNA regulation on duplicated R-genes expression may need to be biologically and functionally validated.

Bottom Line: We unravel in the current article (i) a R-genes repertoire consisting in 7883 for monocots and 15758 for eudicots, (ii) a contrasted R-genes conservation with 23.8% for monocots and 6.6% for dicots, (iii) a minimal ancestral founder pool of 384 R-genes for the monocots and 150 R-genes for the eudicots, (iv) a general pattern of organization in clusters accounting for more than 60% of mapped R-genes, (v) a biased deletion of ancestral duplicated R-genes between paralogous blocks possibly compensated by clusterization, (vi) a bias in R-genes clusterization where Leucine-Rich Repeats act as a 'glue' for domain association, (vii) a R-genes/miRNAs interome enriched toward duplicated R-genes.Together, our data may suggest that R-genes family plasticity operated during plant evolution (i) at the structural level through massive duplicates loss counterbalanced by massive clusterization following polyploidization; as well as at (ii) the regulation level through microRNA/R-gene interactions acting as a possible source of functional diploidization of structurally retained R-genes duplicates.Such evolutionary shuffling events leaded to CNVs (i.e. Copy Number Variation) and PAVs (i.e. Presence Absence Variation) between related species operating in the decay of R-genes colinearity between plant species.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA/UBP UMR 1095 GDEC 'Génétique, Diversité et Ecophysiologie des Céréales', 5 chemin de Beaulieu, 63100 Clermont-Ferrand, France. jsalse@clermont.inra.fr.

ABSTRACT

Background: The recent access to a large set of genome sequences, combined with a robust evolutionary scenario of modern monocot (i.e. grasses) and eudicot (i.e. rosids) species from their founder ancestors, offered the opportunity to gain insights into disease resistance genes (R-genes) evolutionary plasticity.

Results: We unravel in the current article (i) a R-genes repertoire consisting in 7883 for monocots and 15758 for eudicots, (ii) a contrasted R-genes conservation with 23.8% for monocots and 6.6% for dicots, (iii) a minimal ancestral founder pool of 384 R-genes for the monocots and 150 R-genes for the eudicots, (iv) a general pattern of organization in clusters accounting for more than 60% of mapped R-genes, (v) a biased deletion of ancestral duplicated R-genes between paralogous blocks possibly compensated by clusterization, (vi) a bias in R-genes clusterization where Leucine-Rich Repeats act as a 'glue' for domain association, (vii) a R-genes/miRNAs interome enriched toward duplicated R-genes.

Conclusions: Together, our data may suggest that R-genes family plasticity operated during plant evolution (i) at the structural level through massive duplicates loss counterbalanced by massive clusterization following polyploidization; as well as at (ii) the regulation level through microRNA/R-gene interactions acting as a possible source of functional diploidization of structurally retained R-genes duplicates. Such evolutionary shuffling events leaded to CNVs (i.e. Copy Number Variation) and PAVs (i.e. Presence Absence Variation) between related species operating in the decay of R-genes colinearity between plant species.

Show MeSH
Related in: MedlinePlus