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The large repertoire of conifer NLR resistance genes includes drought responsive and highly diversified RNLs - PubMed

  • ️Tue Jan 01 2019

The large repertoire of conifer NLR resistance genes includes drought responsive and highly diversified RNLs

Cyril Van Ghelder et al. Sci Rep. 2019.

Abstract

The NLRs or NBS-LRRs (nucleotide-binding, leucine-rich-repeat) form the largest resistance gene family in plants, with lineage-specific contingents of TNL, CNL and RNL subfamilies and a central role in resilience to stress. The origin, evolution and distribution of NLR sequences has been unclear owing in part to the variable size and diversity of the RNL subfamily and a lack of data in Gymnosperms. We developed, searched and annotated transcriptomes assemblies of seven conifers and identified a resource of 3816 expressed NLR sequences. Our analyses encompassed sequences data spanning the major groups of land plants and determinations of NLR transcripts levels in response to drought in white spruce. We showed that conifers have among the most diverse and numerous RNLs in tested land plants. We report an evolutionary swap in the formation of RNLs, which emerged from the fusion of an RPW8 domain to a NB-ARC domain of CNL. We uncovered a quantitative relationship between RNLs and TNLs across all land plants investigated, with an average ratio of 1:10. The conifer RNL repertoire harbours four distinct groups, with two that differ from Angiosperms, one of which contained several upregulated sequences in response to drought while the majority of responsive NLRs are downregulated.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1

Schematic representation of the four subfamilies of NLRs in conifers. The detailed motifs of the NB-ARC domain are split into conserved motifs through NLR subfamilies (green) and discriminative motifs (grey). Pfam and Superfamilies entry identifiers are indicated above the green bar. Discriminant amino acids are highlighted in red, ‘h’ indicates various hydrophobic residue.

Figure 2
Figure 2

Distribution of the RNL and TNL genes in 49 land plants. (a) RNL- and TNL-related sequence numbers are mapped to the species tree created from the NCBI Common Taxonomy Tree (

https://www.ncbi.nlm.nih.gov/Taxonomy/CommonTree/wwwcmt.cgi

). Abscissa axis represents the protein numbers situated above the diagram. (b) RNL versus TNL numbers. (c) RNL versus CNL numbers. Light red dots represent the conifer species used in this study. The linear regression equation and the R2 coefficient are indicated.

Figure 3
Figure 3

Unrooted ML phylogenetic tree and motif analysis for the RPW8 domain. (a) 185 RPW8 domains identified in conifers in this study together with RPW8 domains of ADR1 (blue dot), RPW8.1, RPW8.2 and NRG1 (red dots) were selected to build the ML phylogenetic tree. The number of conifer sequences contained in each of the groups are indicated below group numbers. For clarity, only main support values >0.70 are displayed (full data available in Supplementary Fig. S6). (b) Motif pattern diversification within the RPW8 domain associated with each group. The details of the motifs are available in Supplementary Table S3.

Figure 4
Figure 4

Unrooted ML phylogenetic tree of the RPW8 domain in land plants. 197 representative RPW8 domains retrieved from 50 land plants (49 species used in the Fig. 3 and Picea abies) were used for the phylogenetic analysis. The size of the circles reflects the number of sequences that are clustered (sequence identity cut-off of 0.60) with the representative sequence. For clarity, only main support values >0.70 are displayed (full data available in Supplementary Fig. S7). Colours are used to reveal taxonomic groups and reference sequences.

Figure 5
Figure 5

Expression patterns and distribution of drought responsive NLR genes in Picea glauca. (a) Heatmap illustrating the 14 expression groups formed of the 119 NLR sequences with drought responsive transcript levels for each genotype, treatment and sampling day. Red asterisks indicate expression groups with a single subfamily of NLR. (b) Number of drought responsive NLR genes and Log2 Fold Change observed in the four subfamilies and undetermined (U). (c) Measurement of water potential in needles for control and water-stressed plants at five sampling times. Each point is the average of 12 biological replicates (3 P. glauca genotypes with 4 replicates each) with standard deviation (adapted from Stival Sena et al.).

Figure 6
Figure 6

Expression of the 13 drought responsive RNLs and their RNL group assignation. The main figure shows transcript levels (Log2 fold change) after 22 days without water. Adjusted p-values are the result of the statistical tests for differential expression between drought-treated and control groups. Time course of expression profiles (Log2 fold change) are shown for the five most upregulated RNLs (top).

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