Contrasting and conserved roles of NPR proteins in diverged land plant lineages

Abstract

SummaryThe NPR proteins AtNPR1 and AtNPR3/AtNPR4 function as salicylic acid (SA) receptors in the model eudicot Arabidopsis thaliana. AtNPR1 plays a central role in SA-induced transcriptional reprogramming and thus positively regulates disease resistance against a variety of pathogens. NPR homologs have been found in the genomes of nearly all land plant species sequenced to date, suggesting that the function of NPR in the SA-mediated response is conserved in land plants. However, we know relatively little about the molecular functions and physiological roles of NPR homologs in most plant species. Our phylogenetic analysis of 194 NPR proteins from 68 land plant species shows that NPR proteins can be classified into three significant clades: angiosperms NPR1/2, angiosperms NPR3/4, and non-seed plants NPR. Uniquely, in Brassicaceae species, NPR genes have been duplicated to form four Brassicaceae-specific subclades. Brassicaceae NPR1-like proteins have characteristically gained or lost functional amino acid residues or protein motifs identified in A. thaliana NPR proteins, pointing to the possibility of a unique evolutionary trajectory for the Brassicaceae NPR1-like proteins that has resulted in peculiar functions. We find that the only NPR in the model liverwort Marchantia polymorpha, MpNPR, is not the master regulator of SA-induced transcriptional reprogramming and rather negatively regulates resistance against bacterial pathogens in this species, although MpNPR expression could complement the mutant phenotypes of Atnpr1-1. The transcriptome of Mpnpr mutant plants suggested potential roles of MpNPR in heat and far-red (FR) light responses. Indeed, Mpnpr mutants displayed enhanced thermomorphogenesis and reduced FR-induced shade avoidance. Furthermore, we identify enhanced thermomorphogenesis in Atnpr1-1 seedlings, suggesting a conserved role of NPR in the heat response in land plants. Taken together, our results demonstrate that the SA-mediated disease resistance-related function of NPR is not evolutionarily well conserved among land plant lineages. We suggest that the common ancestor of land plants had acquired NPR to cope with highly fluctuating conditions, including temperature and light quality, in terrestrial environments.