NLR immune receptors can exhibit tissue-specific expression patterns across legume species

Abstract

Pathogen pressure threatens legume crop productivity worldwide. Nucleotide-binding leucine-rich repeat (NLR) immune receptors serve as crucial plant resistance genes, recognizing pathogens and triggering immunity. However, the extent and patterns of NLR expression in different tissues and organs, notably across evolutionary time, remain largely uncharacterized. To investigate tissue-specificity of NLR expression in the Fabaceae (legumes), we conducted comparative analyses integrating phylogenomics and transcriptomics in root and shoot tissues across different legume species. The NLR repertoires of 28 legumes were grouped into five monophyletic clades: coiled-coil NLR (CC-NLR), Toll/interleukin-1 receptor NLR (TIR-NLR), G10-subclade CC NLR (CCG10-NLR), RESISTANCE TO POWDERY MILDEW 8-like CC NLR (CCR-NLR), and TIR-NB-ARC-like {beta}-propeller WD40/tetratricopeptide repeats (TNPs). Most legume NLRs belonged to CC-NLR and TIR-NLR clades, followed by CCG10-NLR, CCR-NLR, and TNP clades. In seven of these species, comparative analysis of NLR expression in leaves versus roots revealed that over half ([~]57%) of expressed NLR genes showed predominant expression in one tissue: 34% in roots (451/1336), and 23% in leaves (311/1336). We identified 324 root-specific NLRs, 171 leaf-specific NLRs, and 841 non-specific NLRs, with an average tissue specificity per species of 32%. The closely related species grass pea (Lathyrus sativus) and pea (Pisum sativum) were an exception, showing higher levels of leaf-specific rather than root-specific NLR expression. We also identified conserved tissue expression patterns across legume species, resulting in a comprehensive resource describing tissue expression bias, enrichment, and specificity for 113 phylogenetic NLR subclasses. These legume NLR repertoires will support comparative studies between species and inform precision-breeding programs considering tissue expression patterns.