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Genome-Wide Comparative Analyses Reveal the Dynamic Evolution of Nucleotide-Binding Leucine-Rich Repeat Gene Family Among Solanaceae Plants

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Genome-Wide Comparative Analyses Reveal the Dynamic Evolution of Nucleotide-Binding Leucine-Rich Repeat Gene Family Among Solanaceae Plants

Eunyoung Seo et al. Front Plant Sci.

Abstract

Plants have evolved an elaborate innate immune system against invading pathogens. Within this system, intracellular nucleotide-binding leucine-rich repeat (NLR) immune receptors are known play critical roles in effector-triggered immunity (ETI) plant defense. We performed genome-wide identification and classification of NLR-coding sequences from the genomes of pepper, tomato, and potato using fixed criteria. We then compared genomic duplication and evolution features. We identified intact 267, 443, and 755 NLR-encoding genes in tomato, potato, and pepper genomes, respectively. Phylogenetic analysis and classification of Solanaceae NLRs revealed that the majority of NLR super family members fell into 14 subgroups, including a TIR-NLR (TNL) subgroup and 13 non-TNL subgroups. Specific subgroups have expanded in each genome, with the expansion in pepper showing subgroup-specific physical clusters. Comparative analysis of duplications showed distinct duplication patterns within pepper and among Solanaceae plants suggesting subgroup- or species-specific gene duplication events after speciation, resulting in divergent evolution. Taken together, genome-wide analysis of NLR family members provide insights into their evolutionary history in Solanaceae. These findings also provide important foundational knowledge for understanding NLR evolution and will empower broader characterization of disease resistance genes to be used for crop breeding.

Keywords: Solanaceae; effector-triggered immunity; genome-wide comparative analysis; nucleotide-binding leucine-rich repeat; plant innate immune system; resistance genes.

Figures

Figure 1
Figure 1
Phylogenetic relationships of Solanaceae NLRs. Intact NB domains of tomato (green), potato (blue), and pepper (red), including 31 cloned functional NLR genes (pink) from Arabidopsis and Solanaceae species, are used in the construction. The tree is constructed using the neighbor-joining method in MEGA5. Subgroups are classified into 13 CNL types and 1 TNL type. Each color indicates the subgroup and pepper-expanded branches are highlighted with red (CNL-G1) and green (CNL-G2) backgrounds.
Figure 2
Figure 2
Physical localization of pepper NLRs. White rectangular boxes symbolize the 12 pepper chromosomes. Line and letter colors indicate NLR subgroups. For ease of visualization, genes with intact NB domains are represented on the chromosomes. Numbers in parenthesis represent the total numbers of mapped NB-encoding genes on each chromosome.
Figure 3
Figure 3
Duplication history of NLR genes in Solanaceae crop. (A) Ks-values between paralogs of each subgroup are shown for pepper (red), tomato (green), and potato (blue). X and Y axes represent Ks-values and frequencies, respectively. Estimated speciation time (Ks value of ~0.3) is marked. Significant duplication after speciation is confirmed by chi-square test and is highlighted using colors (right). Intensified colors indicate a high portion of Ks-value after speciation. The distribution pattern of Ks-values for CNL-C1 (B) and CNL-C2 (C) are shown as examples.
Figure 4
Figure 4
Comparative analysis of the upper arm of chromosome 6 in Solanaceae. (A) The region compared in this study is highlighted by a red line on chromosome 6 (top). Flaking markers U218000 and SSR48 from tomato are represented. Dot plots between tomato and potato (left), pepper and tomato (middle), and potato and pepper (right) is presented. Red and blue lines indicate positive and negative alignments, respectively. NLR-rich regions are depicted by lines out of the dot plots. (B) The distribution of NLR genes on the upper arm of chromosome 6 is shown. Non-NLR genes were omitted.

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