BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000.

Takashi Yaeno,Koh Iba

doi:10.1104/pp.108.124529

Abstract

Salicylic acid (SA) is a primary factor responsible for exerting diverse immune responses in plants and is synthesized in response to attack by a wide range of pathogens. The Arabidopsis (Arabidopsis thaliana) sid2 mutant is defective in a SA biosynthetic pathway involving ISOCHORISMATE SYNTHASE1 (ICS1) and consequently contains reduced levels of SA. However, the sid2 mutant as well as ICS-suppressed tobacco (Nicotiana benthamiana) still accumulate a small but significant level of SA. These observations along with previous studies suggest that SA might also be synthesized by another pathway involving benzoic acid (BA). Here we isolated a benzoic acid hypersensitive1-Dominant (bah1-D) mutant that excessively accumulated SA after application of BA from activation-tagged lines. This mutant also accumulated higher levels of SA after inoculation with Pseudomonas syringae pv tomato DC3000. Analysis of the bah1-D sid2 double mutant suggested that the bah1-D mutation caused both ICS1-dependent and -independent accumulation. In addition, the bah1-D mutant showed SA-dependent localized cell death in response to P. syringae pv tomato DC3000. The T-DNA insertional mutation that caused the bah1-D phenotypes resulted in the suppression of expression of the NLA gene, which encodes a RING-type ubiquitin E3 ligase. These results suggest that BAH1/NLA plays crucial roles in the ubiquitination-mediated regulation of immune responses, including BA- and pathogen-induced SA accumulation, and control of cell death.

Highlights

Salicylic acid (SA) is a primary factor responsible for exerting diverse immune responses in plants and is synthesized in response to attack by a wide range of pathogens
SA is assumed to be synthesized through the Phe ammonia-lyase (PAL) pathway in which Phe is converted to benzoic acid (BA) by several enzymes including PAL and subsequently BA is converted to SA by a putative enzyme BA 2-hydroxylase (BA2H; Leon et al, 1993; Mauch-Mani and Slusarenko, 1996; Shirasu et al, 1997; Coquoz et al, 1998; Ferrari et al, 2003; Ogawa et al, 2005; Yaeno et al, 2006)
Detectable levels of total SA did accumulate in both sid2 and benzoic acid hypersensitive1-Dominant (bah1-D) sid2 plants, and the levels in the bah1-D sid2 plants were significantly higher than those in the sid2 plants (Fig. 3B). These results suggest that the majority of SA accumulation in the bah1-D plants is synthesized by the ISOCHORISMATE SYNTHASE1 (ICS1) pathway, but a residual amount of SA in both sid2 and bah1-D sid2 plants may be derived from an ICS1-independent pathway

Summary

Introduction

Salicylic acid (SA) is a primary factor responsible for exerting diverse immune responses in plants and is synthesized in response to attack by a wide range of pathogens. The sid mutant as well as ICS-suppressed tobacco (Nicotiana benthamiana) still accumulate a small but significant level of SA These observations along with previous studies suggest that SA might be synthesized by another pathway involving benzoic acid (BA). The T-DNA insertional mutation that caused the bah1-D phenotypes resulted in the suppression of expression of the NLA gene, which encodes a RING-type ubiquitin E3 ligase These results suggest that BAH1/NLA plays crucial roles in the ubiquitination-mediated regulation of immune responses, including BA- and pathogen-induced SA accumulation, and control of cell death. We isolated and characterized the benzoic acid hypersensitive1-Dominant (bah1-D) mutant, an activation-tagged line carrying a mutation in a RING-type ubiquitin E3 ligase, which accumulated excess amounts of SA. Our results suggest that the wild-type version of this gene may play a role as a negative regulator during both ICS1-independent and ICS1-mediated SA production in immune responses

Methods

Results

Conclusion