Nitric oxide regulation of temperature acclimation: a molecular genetic perspective

Heat stress (HS) is becoming an increasingly significant problem for food security as global warming progresses. Recent studies have elucidated the complex transcriptional regulatory networks involved in HS. Here, we provide an overview of current knowledge regarding the transcriptional regulatory network and post-translational regulation of the transcription factors involved in the HS response. Increasing evidence suggests that epigenetic regulation and small RNAs are important in heat-induced transcriptional responses and stress memory. It remains to be elucidated how plants sense and respond to HS. Several recent reports have discussed the heat sensing and signaling that activate transcriptional cascades; thus, we also highlight future directions of promoting crop tolerance to HS using these factors or other strategies for agricultural applications.

Nitric oxide (NO) is an important signaling molecule involved in many physiological processes in plants. We evaluated the role of NO in cold acclimation and freezing tolerance using Arabidopsis (Arabidopsis thaliana) wild type and mutants nia1nia2 (for nitrate reductase [NR]-defective double mutant) and Atnoa1/rif1 (for nitric oxide associated1/resistant to inhibition by fosmidomycin1) that exhibit defects in NR and reduced NO production, respectively. Cold acclimation induced an increase in endogenous NO production in wild-type and Atnoa1/rif1 leaves, while endogenous NO level in nia1nia2 leaves was lower than in wild-type ones and was little changed during cold acclimation. Cold acclimation stimulated NR activity and induced up-regulation of NIA1 gene expression. In contrast, cold acclimation reduced the quantity of NOA1/RIF1 protein and inhibited NO synthase (NOS) activity. These results indicate that up-regulation of NR-dependent NO synthesis underpins cold acclimation-induced NO production. Seedlings of nia1nia2 were less tolerant to freezing than wild-type plants. Pharmacological studies using NR inhibitor, NO scavenger, and NO donor showed that NR-dependent NO level was positively correlated with freezing tolerance. Furthermore, cold acclimation up- and down-regulated expression of P5CS1 and ProDH genes, respectively, resulting in enhanced accumulation of proline (Pro) in wild-type plants. The stimulation of Pro accumulation by cold acclimation was reduced by NR inhibitor and NO scavenger, while Pro accumulation by cold acclimation was not affected by the NOS inhibitor. In contrast to wild-type plants, cold acclimation up-regulated ProDH gene expression in nia1nia2 plants, leading to less accumulation in nia1nia2 plants than in wild-type plants. These findings demonstrate that NR-dependent NO production plays an important role in cold acclimation-induced increase in freezing tolerance by modulating Pro accumulation in Arabidopsis.

Nitric oxide (NO) is a key signaling molecule in plants. This analysis of Arabidopsis thaliana HOT5 (sensitive to hot temperatures), which is required for thermotolerance, uncovers a role of NO in thermotolerance and plant development. HOT5 encodes S-nitrosoglutathione reductase (GSNOR), which metabolizes the NO adduct S-nitrosoglutathione. Two hot5 missense alleles and two T-DNA insertion, protein null alleles were characterized. The missense alleles cannot acclimate to heat as dark-grown seedlings but grow normally and can heat-acclimate in the light. The null alleles cannot heat-acclimate as light-grown plants and have other phenotypes, including failure to grow on nutrient plates, increased reproductive shoots, and reduced fertility. The fertility defect of hot5 is due to both reduced stamen elongation and male and female fertilization defects. The hot5 null alleles show increased nitrate and nitroso species levels, and the heat sensitivity of both missense and null alleles is associated with increased NO species. Heat sensitivity is enhanced in wild-type and mutant plants by NO donors, and the heat sensitivity of hot5 mutants can be rescued by an NO scavenger. An NO-overproducing mutant is also defective in thermotolerance. Together, our results expand the importance of GSNOR-regulated NO homeostasis to abiotic stress and plant development.