Distinct Patterns of Gene Gain and Loss: Diverse Evolutionary Modes of NBS-Encoding Genes in Three Solanaceae Crop Species

Abstract

Plant resistance conferred by nucleotide binding site (NBS)-encoding resistance genes plays a key role in the defense against various pathogens throughout the entire plant life cycle. However, comparative analyses for the systematic evaluation and determination of the evolutionary modes of NBS-encoding genes among Solanaceae species are rare. In this study, 447, 255, and 306 NBS-encoding genes were identified from the genomes of potato, tomato, and pepper, respectively. These genes usually clustered as tandem arrays on chromosomes; few existed as singletons. Phylogenetic analysis indicated that three subclasses [TNLs (TIR-NBS-LRR), CNLs (CC-NBS-LRR), and RNLs (RPW8-NBS-LRR)] each formed a monophyletic clade and were distinguished by unique exon/intron structures and amino acid motif sequences. By comparing phylogenetic and systematic relationships, we inferred that the NBS-encoding genes in the present genomes of potato, tomato, and pepper were derived from 150 CNL, 22 TNL, and 4 RNL ancestral genes, and underwent independent gene loss and duplication events after speciation. The NBS-encoding genes therefore exhibit diverse and dynamic evolutionary patterns in the three Solanaceae species, giving rise to the discrepant gene numbers observed today. Potato shows a "consistent expansion" pattern, tomato exhibits a pattern of "first expansion and then contraction," and pepper presents a "shrinking" pattern. The earlier expansion of CNLs in the common ancestor led to the dominance of this subclass in gene numbers. However, RNLs remained at low copy numbers due to their specific functions. Along the evolutionary process of NBS-encoding genes in Solanaceae, species-specific tandem duplications contributed the most to gene expansions.

Keywords: NBS-encoding genes; Solanaceae; evolutionary pattern; phylogenetic relationship.

Figure 1

Phylogenetic relationship of tomato, potato, and pepper. Times of divergence (million years ago, MYA) are from Wu and Tanksley (2010), Tu et al. (2010), and Wang et al. (2008).

Figure 2

NBS loci in the tomato, potato, and pepper genomes. NBS, nucleotide binding site.

Figure 3

Six conserved motifs in NBS domains of the three Solanaceae species. The amino acids of the six motifs were extracted. Different conserved amino acids among TNL, CNL, and RNL subclass genes are labeled with a red star. The details of the amino acids of the whole NBS domain of NBS-encoding genes in the three Solanaceae species are shown in Figure S2. CNL, CC-NBS-LRR; NBS, nucleotide binding site; RNL, RPW8-NBS-LRR; TNL, TIR-NBS-LRR.

Figure 4

Exon/intron structures among the CNL, TNL, and RNL subclasses. CNL, CC-NBS-LRR; NBS, nucleotide binding site; RNL, RPW8-NBS-LRR; TNL, TIR-NBS-LRR.

Figure 5

Phylogenetic relationships of NBS-encoding genes in tomato, potato, and pepper based on conserved NBS domains. The red, blue, and green lines represent NBS-encoding genes in tomato, potato, and pepper, respectively. NBS-encoding gene subclasses (CNL, TNL, and RNL) and support values >0.75 (SH-aLRT values) for basal nodes are shown. The T-P-P ancestor lineage indicates the NBS-encoding genes from the common ancestor of tomato, potato, and pepper (a total of 176). Homologous genes with known-function disease resistance genes in the tomato, potato, and pepper genomes obtained by BLASTp homology comparison are labeled with red arrows and the names of functional genes (BS4, I2, Rpi-blb1, RPM1, RPP13, TM-2, BS2, Prf, R1, SW-5, Hero, CaMi, Rpi-blb2, and Mi-1). The detailed information on the phylogenetic tree of NBS-encoding genes identified from tomato, potato, and pepper, including gene names, evolutionary relationships among genes, and supporting values of all nodes, are shown in Figure S3. CNL, CC-NBS-LRR; NBS, nucleotide binding site; RNL, RPW8-NBS-LRR; TNL, TIR-NBS-LRR; T-P-P, tomato, potato, and pepper.

Figure 6

Dynamic patterns of NBS-encoding genes in the three Solanaceae genomes. (A) Loss/duplication events of NBS-encoding genes during the speciation of tomato, potato, and pepper. Gene losses and duplications are indicated by numbers with “–”or “+” on each branch. Dates of divergence of tomato, potato, and pepper are shown as MYA (Wang et al. 2008; Tu et al. 2010; Wu and Tanksley 2010). Detailed information for gain and loss of NBS-encoding genes is shown in Figure S5. In addition, the detailed information for gain and loss, and the loss/duplication events of NBS-encoding genes based on the phylogeny of NBS domains of all identified NBS-encoding genes are shown in Figure S6 and Figure S7, respectively. (B) Evolutionary modes of NBS-encoding genes in the three Solanaceae species. (I) The gene number variation from the T-P-P ancestor to potato. (II) The gene number variation from the T-P-P ancestor to tomato. (III) The gene number variation from the T-P-P ancestor to pepper. CNL, CC-NBS-LRR; MYA, millions of years ago; NBS, nucleotide binding site; RNL, RPW8-NBS-LRR; TNL, TIR-NBS-LRR; T-P-P, tomato, potato, and pepper.