Up-regulation of Arabidopsis thaliana NHL10 in the hypersensitive response to Cucumber mosaic virus infection and in senescing leaves is controlled by signalling pathways that differ in salicylate involvement

The Arabidopsis thaliana (L.) Heyhn. genome contains 45 genes that show substantial sequence similarity to the tobacco (Nicotiana tabacum L.) HIN1 (harpin-induced) gene and the Arabidopsis NDR1 (non-race-specific disease resistance) gene. Of these, the nine (NHL1 to NHL3, NHL8 to NHL12 and NHL22) that bear the highest identity to HIN1 were selected and their expression in various situations was examined. We found that NHL10 behaves like the tobacco HIN1 gene in that its transcripts are abundant in senescing leaves and they specifically accumulate during the hypersensitive response (HR) caused by exposure to an avirulent Cucumber mosaic virus (CMV) strain. Spermine, a novel inducer of tobacco PR (pathogenesis-related) genes, was found to up-regulate expression of NHL3, NHL10 and NDR1. Green fluorescent protein-fusion experiments indicated that NHL2 and NHL10, and possibly NDR1 are localized in the chloroplasts. Studies using Arabidopsis mutants defective in salicylic acid (SA), ethylene and jasmonic acid signalling revealed that the senescence-associated expression of NHL10 is mediated by a pathway that involves SA but that NHL10 expression during CMV-induced HR and spermine treatment is totally independent of SA.