Abstract

BackgroundResistance genes composing the two-layer immune system of plants are thought as important markers for breeding pathogen-resistant crops. Many have been the attempts to establish relationships between the genomic content of Resistance Gene Analogs (RGAs) of modern sugarcane cultivars to its degrees of resistance to diseases such as smut. However, due to the highly polyploid and heterozygous nature of sugarcane genome, large scale RGA predictions is challenging.ResultsWe predicted, searched for orthologs, and investigated the genomic features of RGAs within a recently released sugarcane elite cultivar genome, alongside the genomes of sorghum, one sugarcane ancestor (Saccharum spontaneum), and a collection of de novo transcripts generated for six modern cultivars. In addition, transcriptomes from two sugarcane genotypes were obtained to investigate the roles of RGAs differentially expressed (RGADE) in their distinct degrees of resistance to smut. Sugarcane references lack RGAs from the TNL class (Toll-Interleukin receptor (TIR) domain associated to nucleotide-binding site (NBS) and leucine-rich repeat (LRR) domains) and harbor elevated content of membrane-associated RGAs. Up to 39% of RGAs were organized in clusters, and 40% of those clusters shared synteny. Basically, 79% of predicted NBS-encoding genes are located in a few chromosomes. S. spontaneum chromosome 5 harbors most RGADE orthologs responsive to smut in modern sugarcane. Resistant sugarcane had an increased number of RGAs differentially expressed from both classes of RLK (receptor-like kinase) and RLP (receptor-like protein) as compared to the smut-susceptible. Tandem duplications have largely contributed to the expansion of both RGA clusters and the predicted clades of RGADEs.ConclusionsMost of smut-responsive RGAs in modern sugarcane were potentially originated in chromosome 5 of the ancestral S. spontaneum genotype. Smut resistant and susceptible genotypes of sugarcane have a distinct pattern of RGADE. TM-LRR (transmembrane domains followed by LRR) family was the most responsive to the early moment of pathogen infection in the resistant genotype, suggesting the relevance of an innate immune system. This work can help to outline strategies for further understanding of allele and paralog expression of RGAs in sugarcane, and the results should help to develop a more applied procedure for the selection of resistant plants in sugarcane.

Highlights

  • Resistance genes composing the two-layer immune system of plants are thought as important markers for breeding pathogen-resistant crops

  • Resistance Gene Analog (RGA) have conserved domains/motifs and structural features, and can be classified into two major encoding families: 1) the classical R genes harboring a nucleotide-binding site followed by leucine-rich repeat (NBS-Leucine-rich Repeat (LRR) or NLRs); and 2) the pattern recognition receptors (PRR) characterized by transmembrane domain followed by leucine-rich repeat (TM-LRR) [2]

  • We addressed the following questions: 1) How many RGAs can be predicted within the genomes of sugarcane ancestors, and within the available genome of modern sugarcane cultivar? 2) How are they distributed and organized within those genomes? 3) Do transcriptomes from sugarcane genotypes having distinct degrees of resistance to smut can help to unravel the roles of PAMP-triggered immunity (PTI) and Effector-Triggered Immunity (ETI) immune systems during the early stages of sugarcane-smut interaction? 4) Do the orthologs of differentially expressed RGAs are biased towards chromosomes, clusters, or syntenic segments? 5) Do their expression profiles reflect their phylogenetic relationships?

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Summary

Introduction

Resistance genes composing the two-layer immune system of plants are thought as important markers for breeding pathogen-resistant crops. The genomic content of Resistance Gene Analogs (RGAs) is frequently associated with crop resistance and have been gathering the attention of many breeding programs [3,4,5]. Both the classical genetics [6] and analysis from large scale sequencing data [3] have shown RGAs biased to form clusters in the plant genomes. These clusters may contain RGAs related in function but not necessarily in sequence [7]. Ancient whole-genome duplications (WGDs), in addition to segmental duplications, both followed by gene deletions and genomic reorganizations have contributed to the expansion of RGA families [8, 9]

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