Genome-wide characterization of the NLR gene family in tomato (Solanum lycopersicum) and their relatedness to disease resistance

Sehrish Bashir; Nazia Rehman; Fabia Fakhar Zaman; Muhammad Kashif Naeem; Atif Jamal; Aurélien Tellier; Muhammad Ilyas; Gustavo Adolfo Silva Arias; Muhammad Ramzan Khan

doi:10.3389/fgene.2022.931580

Genome-wide characterization of the NLR gene family in tomato (Solanum lycopersicum) and their relatedness to disease resistance

Front Genet. 2022 Dec 5:13:931580. doi: 10.3389/fgene.2022.931580. eCollection 2022.

Authors

Sehrish Bashir^{1

2}, Nazia Rehman^{1

2}, Fabia Fakhar Zaman^{1

2}, Muhammad Kashif Naeem¹, Atif Jamal³, Aurélien Tellier⁴, Muhammad Ilyas⁴, Gustavo Adolfo Silva Arias⁴, Muhammad Ramzan Khan^{1

2}

Affiliations

¹ National Institute for Genomics and Advanced Biotechnology, National Agricultural Research Centre, Islamabad, Pakistan.
² PARC Institute for Advanced Studies in Agriculture, NARC, Islamabad, Pakistan.
³ Crop Disease Research Institute, National Agricultural Research Center, Islamabad, Pakistan.
⁴ Population Genetics, Department of Life Science Systems, School of Life Sciences, Technical University of Munich, Freising, Germany.

Abstract

Nucleotide-binding leucine-rich-repeat receptors (NLR), the largest group of genes associated with plant disease resistance (R), have attracted attention due to their crucial role in protecting plants from pathogens. Genome-wide studies of NLRs have revealed conserved domains in the annotated tomato genome. The 321 NLR genes identified in the tomato genome have been randomly mapped to 12 chromosomes. Phylogenetic analysis and classification of NLRs have revealed that 211 genes share full-length domains categorized into three major clades (CNL, TNL, and RNL); the remaining 110 NLRs share partial domains and are classified in CN, TN, and N according to their motifs and gene structures. The cis-regulatory elements of NLRs exhibit the maximum number of these elements and are involved in response to biotic and abiotic stresses, pathogen recognition, and resistance. Analysis of the phylogenetic relationship between tomato NLRs and orthologs in other species has shown conservation among Solanaceae members and variation with A. thaliana. Synteny and Ka/Ks analyses of Solanum lycopersicum and Solanum tuberosum orthologs have underscored the importance of NLR conservation and diversification from ancestral species millions of years ago. RNA-seq data and qPCR analysis of early and late blight diseases in tomatoes revealed consistent NLR expression patterns, including upregulation in infected compared to control plants (with some exceptions), suggesting the role of NLRs as key regulators in early blight resistance. Moreover, the expression levels of NLRs associated with late blight resistance (Solyc04g007060 [NRC4] and Solyc10g008240 [RIB12]) suggested that they regulate S. lycopersicum resistance to P. infestans. These findings provide important fundamental knowledge for understanding NLR evolution and diversity and will empower the broader characterization of disease resistance genes for pyramiding through speed cloning to develop disease-tolerant varieties.

Keywords: Alternaria solani; NLR genes; Phytophthora infestans; phylogenetic relationship; synteny; tomato.