Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana - PubMed (original) (raw)

Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana

Mariana Mondragón-Palomino et al. Genome Res. 2002 Sep.

Abstract

Plant disease resistance genes have been shown to be subject to positive selection, particularly in the leucine rich repeat (LRR) region that may determine resistance specificity. We performed a genome-wide analysis of positive selection in members of the nucleotide binding site (NBS)-LRR gene family of Arabidopsis thaliana. Analyses were possible for 103 of 163 NBS-LRR nucleotide sequences in the genome, and the analyses uncovered substantial evidence of positive selection. Sites under positive selection were detected and identified for 10 sequence groups representing 53 NBS-LRR sequences. Functionally characterized Arabidopsis resistance genes were in these 10 groups, but several groups with extensive evidence of positive selection contained no previously characterized resistance genes. Amino acid residues under positive selection were identified, and these residues were mapped onto protein secondary structure. Positively selected positions were disproportionately located in the LRR domain (P < 0.001), particularly a nine-amino acid beta-strand submotif that is likely to be solvent exposed. However, a substantial proportion (30%) of positively selected sites were located outside LRRs, suggesting that regions other than the LRR may function in determining resistance specificity. Because of the unusual sequence variability in the LRRs of this class of proteins, secondary-structure analysis identifies LRRs that are not identified by similarity analyses alone. LRRs also contain substantial indel variation, suggesting elasticity in LRR length could also influence resistance specificity.

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Figures

Figure 1

Figure 1

The posterior probability for sites in the positively selected class (ω > 1). Each graph represents 1 of the 10 sequence groups for which positive selection was detected by comparison of M7 and M8. The _X_-axis denotes position in the amino acid alignment. Sites with black bars had a posterior probability >0.9 under M8; sites with gray bars did not have posterior probabilities >0.9. Boxes under each graph denote domain structures of nucleotide sequences in the group, as identified either by Pfam (groups 2, 8, 9, 11, and 12) or by comparison to groups containing previously described R genes (groups 10, 14, 15, 18, and 20).

Figure 2

Figure 2

Secondary-structure predictions for LRRs from four groups with the highest number of positively selected sites. R# on left indicates the ordinal number for each LRR, and the sequence within each LRR represents the consensus from the alignment. Secondary-structure predictions are colored (yellow, coil; red, β-sheet; and blue, α-helix). The positions in which positive selection was detected are in bold and the sites that are part of the E4C5 motif are underlined. CON is the consensus sequence among LRRs for each group. Amino acids represented in uppercase are invariant among sequences. Notation for variable amino acid sites are as follows: X, any amino acid; 1, D,N; 2, E,Q; 3, S,T; 4, K,R; 5, F,Y,W; and 6, L,I,V,M. Dashes are gaps introduced to better align consensus LRRs and do not necessarily represent gaps in the original sequence alignments. In group 11, repeats 5, 6, 7, 8, 10, and 11 were defined by their predicted secondary structure. Similarly, repeats 1, 5, and 9 of group 18 were defined by predicted secondary structure. For other groups, LRRs were defined either by Pfam or by their similarity to characterized R genes.

Figure 3

Figure 3

A model of the evolutionary processes in LRRs that generate novel resistance specificities. (A) Indels in the backbone of the LRR domain. (B) Hypervariability in the E4C5 region. (C) Expansion/contraction in the overall number of LRR units. (D) Changes in secondary structure resulting from amino acid changes outside of the E4C5 region.

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