Salicylate Accumulation Inhibits Growth at Chilling Temperature in Arabidopsis

Abstract

The growth of Arabidopsis plants in chilling conditions could be related to their levels of salicylic acid (SA). Plants with the SA hydroxylase NahG transgene grew at similar rates to Col-0 wild types at 23°C, and growth of both genotypes was slowed by transfer to 5°C. However, at 5°C, NahG plants displayed relative growth rates about one-third greater than Col-0, so that by 2 months NahG plants were typically 2.7-fold larger. This resulted primarily from greater cell expansion in NahG rosette leaves. Specific leaf areas and leaf area ratios remained similar in both genotypes. Net assimilation rates were similar in both genotypes at 23°C, but higher in NahG at 5°C. Chlorophyll fluorescence measurements revealed no PSII photodamage in chilled leaves of either genotype. Col-0 shoots at 5°C accumulated SA, particularly in glucosylated form. SA in NahG shoots showed similar tendencies at 5°C, but at greatly depleted levels. Catechol was not detected as a metabolite of the NahG transgene product. We also examined growth and SA levels in SA signaling and metabolism mutants at 5°C. The partially SAinsensitive npr1 mutant displayed growth intermediate between NahG and Col-0, while the SA-deficient eds5 mutant behaved like NahG. In contrast, the cpr1 mutant at 5°C accumulated very high levels of SA and its growth was much more inhibited than wild type. At both temperatures, cpr1 was the only SA-responsive genotype in which oxidative damage (measured as thiobarbituric acid-reactive substances) was significantly different from wild type.Salicylic acid (SA) has received much attention due to its association with economically important plant responses to disease and other stresses. Detailed evidence implicates SA in PR gene expression, systemic acquired resistance, and the hypersensitive response (Kunkel and Brooks, 2002). SA also seems to be involved in responses to abiotic stresses, such as ozone (Sharma et al., 1996;Rao and Davis, 1999;Koch et al., 2000), salt and osmotic stress (Borsani et al., 2001;Molina et al., 2002;Shim et al., 2003), UV-B (Surplus et al., 1998), drought (Senaratna et al., 2000Nemeth et al., 2002), paraquat (Kim et al., 2003, and heat (Dat et al., 1998a(Dat et al., , 1998b(Dat et al., , 2000Lopez-Delgado et al., 1998a;Senaratna et al., 2000;Larkindale and Knight, 2002; Clarke et al., 2004). Stress-influenced developmental transitions, including flowering (Hatayama and Takeno, 2003;Martinez et al., 2004), tuberization (Lopez-Delgado and Scott, 1997), and senescence (Morris et al., 2000), may also involve SA.Cold is one of the most important limitations to crop productivity and species distribution. Freezing (subzero) or chilling (low positive) temperatures can cause injury or reduced growth depending on the cold tolerance of the species (Schneider et al., 1995;Pearce, 1999;Humphreys et al., 2003). Recent studies describe potentially valuable effects of salicylate treatment on cold tolerance in maize, rice, and wheat (Janda et al., 1999;Szalai et al., 2000;Kang and Saltveit, 2002;Tasgin et al., 200...

Arabidopsis Isochorismate Synthase Functional in Pathogen-induced Salicylate Biosynthesis Exhibits Properties Consistent with a Role in Diverse Stress Responses

“…We found non-enzymatic conversion of IC to SA under physiological conditions to be negligible. Furthermore, total SA accumulates to levels similar to those induced by pathogen in Arabidopsis grown at 5°C (32), a temperature at which non-enzymatic conversion of IC to SA should be insignificant. In P. aeruginosa, a direct comparison of the enzymatic (k cat Pae PchB (50)) and non-enzymatic (64) rates of SA formation from IC indicates that the enzyme accelerates SA formation ϳ4 ϫ 10 5 -fold (64).…”

“…Over the past few years, a more general role for SA as a mediator of diverse stress responses has been emerging. For example, in Arabidopsis SA is synthesized in response to abiotic stresses such as UV-C (30), ozone (31), cold (32), and heat (33,34) and has been shown to play a role in stress-induced developmental transitions, including flowering (35) and senescence (36). Although AtICS1 has been confirmed to be involved in many of these processes, it has only been implicated in others, such as cold-tolerant growth.…”

Root-Secreted Malic Acid Recruits Beneficial Soil Bacteria

“…S2). Similarly, when free SA levels were analyzed (Scott et al, 2004), the Col-0 plant roots colonized with FB17 showed increased free SA titers compared to plants without FB17 colonization (data not shown).…”

Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

“…Although we cannot exclude potential effects of the catechol by-product of NahG-mediated SA degradation, the phenotypic effects seen in the NahG transgenic plants of increased rosette biomass through greater cell expansion and increased seed yields are known to be directly associated with reduced SA levels in Arabidopsis (39)(40)(41)(42). NahG-generated catechol may not accumulate to high levels (43), which in any case would cause growth inhibition (44) and not the growth enhancement observed.…”