Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism

Abstract

The plant hormone salicylic acid (SA) plays critical roles in plant defense, stress responses, and senescence. Although SA biosynthesis is well understood, the pathways by which SA is catabolized remain elusive. Here we report the identification and characterization of an SA 3-hydroxylase (S3H) involved in SA catabolism during leaf senescence. S3H is associated with senescence and is inducible by SA and is thus a key part of a negative feedback regulation system of SA levels during senescence. The enzyme converts SA (with a K m of 58.29 μM) to both 2,3-dihydroxybenzoic acid (2,3-DHBA) and 2,5-DHBA in vitro but only 2,3-DHBA in vivo. The s3h knockout mutants fail to produce 2,3-DHBA sugar conjugates, accumulate very high levels of SA and its sugar conjugates, and exhibit a precocious senescence phenotype. Conversely, the gain-of-function lines contain high levels of 2,3-DHBA sugar conjugates and extremely low levels of SA and its sugar conjugates and display a significantly extended leaf longevity. This research reveals an elegant SA catabolic mechanism by which plants regulate SA levels by converting it to 2,3-DHBA to prevent SA overaccumulation. The research also provides strong molecular genetic evidence for an important role of SA in regulating the onset and rate of leaf senescence.aging | benzoic acid | disease resistance | NahG | senescence-associated gene

Exploiting Natural Variation of Secondary Metabolism Identifies a Gene Controlling the Glycosylation Diversity of Dihydroxybenzoic Acids in Arabidopsis thaliana

“…Consistent with this observation, Arabidopsis isochorismate synthase mutant sid2, which is defective in SA biosynthesis, was found to be deficient in DHBA glycosides (Bartsch et al 2010). More recently, a SA 3-hydroxylase gene was identified from Arabidopsis, providing direct evidence for the involvement of SA in DHBA biosynthesis (Zhang et al 2013).…”

“…DHBA glycoside biosynthesis has been implicated in defense responses and leaf senescence regulation (Belles et al 1999;Fayos et al 2006;Bartsch et al 2010;Zhang et al 2013), but it is yet unclear whether these are due to modulation of SA activity or new activities conferred by DHBAs and/or their glycosides. Glycosylation is a common modification that contributes to the diversity of secondary metabolism.…”

PROHIBITIN3 Forms Complexes with ISOCHORISMATE SYNTHASE1 to Regulate Stress-Induced Salicylic Acid Biosynthesis in Arabidopsis

“…Interestingly, the Enhanced Disease 97 Susceptibility 5 (EDS5) SA transporter in the chloroplast envelope of Arabidopsis is 98 necessary for stress-induced SA accumulation, possibly due to a regulatory coupling of SA 99 transport and synthesis (Serrano et al, 2013;Yamasaki et al, 2013). Recently, a catabolic 100 enzyme that converts SA to 2,3 dihydroxybenzoic acid in Arabidopsis was described 101 (Zhang et al, 2013). Other enzymes that impact SA levels have been found or inferred from 102…”

“…Its developmental roles include 81 the regulation of flowering time (Martínez et al, 2004), leaf longevity (slow cell death; 82 Morris et al, 2000;Zhang et al, 2013), and biomass (Abreu et al, 2009) …”

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

“…SA levels increase during senescence [63]. Moreover, SA promotes senescence [64]. Transgenic barley plants with a reduced level of WHIRLY1 show a stay-green phenotype, despite having a higher level of SA than untransformed controls (C.H.F., B.K.…”