Phylogenetic Analyses and Transcriptional Survey Reveal the Characteristics, Evolution, and Expression Profile of NBS-Type Resistance Genes in Papaya

Abstract

Carica papaya maintains an abnormally small but complete NLR family while showing weak disease resistance. To better understand their origin, evolution, and biological function, we identified 59 NLR genes via a customized RGAugury and investigated their characteristics, evolutionary history, and expression profiles based on the improved papaya genome and large-scale RNA-seq data. The results indicated that duplication is a major evolutionary force driving the formation of the papaya NLR family. Synteny analyses of papaya and other angiosperms showed that both insertion and inheritance-derived NLRs are present in papaya. Transcriptome-based expression and network analyses revealed that NLRs are actively involved in biotic stress responses. For example, a papaya-specific inserted TNL was up-regulated strongly by the fungal infection. Both transcriptome and qRT-PCR analyses confirmed the expression divergence of an RNL and an RCNL, a pair of tandem duplication genes involved in different co-expression modules. Furthermore, we observed an inserted gene cluster composed of five duplicated CNLs, showing dosage effects and functional differentiation of disease-resistance genes during evolution. This research will enhance our knowledge of the special NLR family in papaya, which may serve as a model plant for disease-resistance genetic studies.