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Evolutionary balance between LRR domain loss and young NBS-LRR genes production governs disease resistance in Arachis hypogaea cv. Tifrunner.

ABSTRACT: BACKGROUND:Cultivated peanut (Arachis hypogaea L.) is an important oil and protein crop, but it has low disease resistance; therefore, it is important to reveal the number, sequence features, function, and evolution of genes that confer resistance. Nucleotide-binding site-leucine-rich repeats (NBS-LRRs) are resistance genes that are involved in response to various pathogens. RESULTS:We identified 713 full-length NBS-LRRs in A. hypogaea cv. Tifrunner. Genetic exchange events occurred on NBS-LRRs in A. hypogaea cv. Tifrunner, which were detected in the same subgenomes and also found in different subgenomes. Relaxed selection acted on NBS-LRR proteins and LRR domains in A. hypogaea cv. Tifrunner. Using quantitative trait loci (QTL), we found that NBS-LRRs were involved in response to late leaf spot, tomato spotted wilt virus, and bacterial wilt in A. duranensis (2 NBS-LRRs), A. ipaensis (39 NBS-LRRs), and A. hypogaea cv. Tifrunner (113 NBS-LRRs). In A. hypogaea cv. Tifrunner, 113 NBS-LRRs were classified as 75 young and 38 old NBS-LRRs, indicating that young NBS-LRRs were involved in response to disease after tetraploidization. However, compared to A. duranensis and A. ipaensis, fewer LRR domains were found in A. hypogaea cv. Tifrunner NBS-LRR proteins, partly explaining the lower disease resistance of the cultivated peanut. CONCLUSIONS:Although relaxed selection acted on NBS-LRR proteins and LRR domains, LRR domains were preferentially lost in A. hypogaea cv. Tifrunner compared to A. duranensis and A. ipaensis. The QTL results suggested that young NBS-LRRs were important for resistance against diseases in A. hypogaea cv. Tifrunner. Our results provid insight into the greater susceptibility of A. hypogaea cv. Tifrunner to disease compared to A. duranensis and A. ipaensis.

SUBMITTER: Song H

PROVIDER: S-EPMC6852974 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Evolutionary balance between LRR domain loss and young NBS-LRR genes production governs disease resistance in Arachis hypogaea cv. Tifrunner.

Song Hui H Guo Zhonglong Z Hu Xiaohui X Qian Lang L Miao Fuhong F Zhang Xiaojun X Chen Jing J

BMC genomics 20191113 1

<h4>Background</h4>Cultivated peanut (Arachis hypogaea L.) is an important oil and protein crop, but it has low disease resistance; therefore, it is important to reveal the number, sequence features, function, and evolution of genes that confer resistance. Nucleotide-binding site-leucine-rich repeats (NBS-LRRs) are resistance genes that are involved in response to various pathogens.<h4>Results</h4>We identified 713 full-length NBS-LRRs in A. hypogaea cv. Tifrunner. Genetic exchange events occurr ...[more]

PMID: 31722670

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Project description:BackgroundCultivated peanut (Arachis hypogaea, AABB genome), an allotetraploid from a cross between A. duranensis (AA genome) and A. ipaensis (BB genome), is an important oil and protein crop with released genome and RNA-seq sequence datasets. These datasets provide the molecular foundation for studying gene expression and evolutionary patterns. However, there are no reports on the proteomic data of A. hypogaea cv. Tifrunner, which limits understanding of its gene function and protein level evolution.ResultsThis study sequenced the A. hypogaea cv. Tifrunner leaf and root proteome using the tandem mass tag technology. A total of 4803 abundant proteins were identified. The 364 differentially abundant proteins were estimated by comparing protein abundances between leaf and root proteomes. The differentially abundant proteins enriched the photosystem process. The number of biased abundant homeologs between the two sub-genomes A (87 homeologs in leaf and root) and B (69 and 68 homeologs in leaf and root, respectively) was not significantly different. However, homeologous proteins with biased abundances in different sub-genomes enriched different biological processes. In the leaf, homeologs biased to sub-genome A enriched biosynthetic and metabolic process, while homeologs biased to sub-genome B enriched iron ion homeostasis process. In the root, homeologs with biased abundance in sub-genome A enriched inorganic biosynthesis and metabolism process, while homeologs with biased abundance in sub-genome B enriched organic biosynthesis and metabolism process. Purifying selection mainly acted on paralogs and homeologs. The selective pressure values were negatively correlated with paralogous protein abundance. About 77.42% (24/31) homeologous and 80% (48/60) paralogous protein pairs had asymmetric abundance, and several protein pairs had conserved abundances in the leaf and root tissues.ConclusionsThis study sequenced the proteome of A. hypogaea cv. Tifrunner using the leaf and root tissues. Differentially abundant proteins were identified, and revealed functions. Paralog abundance divergence and homeolog bias abundance was elucidated. These results indicate that divergent abundance caused retention of homologs in A. hypogaea cv. Tifrunner.

Project description:BACKGROUND:The Root-Knot Nematode (RKN), Meloidogyne arenaria, significantly reduces peanut grain quality and yield worldwide. Whilst the cultivated species has low levels of resistance to RKN and other pests and diseases, peanut wild relatives (Arachis spp.) show rich genetic diversity and harbor high levels of resistance to many pathogens and environmental constraints. Comparative transcriptome analysis can be applied to identify candidate resistance genes. RESULTS:Transcriptome analysis during the early stages of RKN infection of two peanut wild relatives, the highly RKN resistant Arachis stenosperma and the moderately susceptible A. duranensis, revealed genes related to plant immunity with contrasting expression profiles. These included genes involved in hormone signaling and secondary metabolites production and also members of the NBS-LRR class of plant disease resistance (R) genes. From 345 NBS-LRRs identified in A.duranensis reference genome, 52 were differentially expressed between inoculated and control samples, with the majority occurring in physical clusters unevenly distributed on eight chromosomes with preferential tandem duplication. The majority of these NBS-LRR genes showed contrasting expression behaviour between A. duranensis and A. stenosperma, particularly at 6 days after nematode inoculation, coinciding with the onset of the Hypersensitive Response in the resistant species. The physical clustering of some of these NBS-LRR genes correlated with their expression patterns in the contrasting genotypes. Four NBS-LRR genes exclusively expressed in A. stenosperma are located within clusters on chromosome Aradu. A09, which harbors a QTL for RKN resistance, suggesting a functional role for their physical arrangement and their potential involvement in this defense response. CONCLUSION:The identification of functional novel R genes in wild Arachis species responsible for triggering effective defense cascades can contribute to the crop genetic improvement and enhance peanut resilience to RKN.

Project description:Dioscorea rotundata is an important food crop that is mainly cultivated in subtropical regions of the world. D. rotundata is frequently infected by various pathogens during its lifespan, which results in a substantial economic loss in terms of yield and quality. The disease resistance gene (R gene) profile of D. rotundata is largely unknown, which has greatly hampered molecular study of disease resistance in this species. Nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes are the largest group of plant R genes, and they play important roles in plant defense responses to various pathogens. In this study, 167 NBS-LRR genes were identified from the D. rotundata genome. Subsequently, one gene was assigned to the resistance to powdery mildew8 (RPW8)-NBS-LRR (RNL) subclass and the other 166 genes to the coiled coil (CC)-NBS-LRR (CNL) subclass. None of the Toll/interleukin-1 receptor (TIR)-NBS-LRR (TNL) genes were detected in the genome. Among them, 124 genes are located in 25 multigene clusters and 43 genes are singletons. Tandem duplication serves as the major force for the cluster arrangement of NBS-LRR genes. Segmental duplication was detected for 18 NBS-LRR genes, although no whole-genome duplication has been documented for the species. Phylogenetic analysis revealed that D. rotundata NBS-LRR genes share 15 ancestral lineages with Arabidopsis thaliana genes. The NBS-LRR gene number increased by more than a factor of 10 during D. rotundata evolution. A conservatively evolved ancestral lineage was identified from D. rotundata, which is orthologs to the Arabidopsis RPM1 gene. Transcriptome analysis for four different tissues of D. rotundata revealed a low expression of most NBS-LRR genes, with the tuber and leaf displaying a relatively high NBS-LRR gene expression than the stem and flower. Overall, this study provides a complete set of NBS-LRR genes for D. rotundata, which may serve as a fundamental resource for mining functional NBS-LRR genes against various pathogens.

Dataset Information

Evolutionary balance between LRR domain loss and young NBS-LRR genes production governs disease resistance in Arachis hypogaea cv. Tifrunner.

Publications

Evolutionary balance between LRR domain loss and young NBS-LRR genes production governs disease resistance in Arachis hypogaea cv. Tifrunner.

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