Abstract
Nitric oxide (NO) is involved together with reactive oxygen species (ROS) in the activation of various stress responses in plants. However, the biochemical mechanisms by which ROS and NO participate, and the potential interaction between these molecules are still unclear. Ozone (O3) can be used as a tool to elicit ROS-activated stress responses and to activate cell death in plant leaves. We have recently shown that O3 induced a rapid accumulation of NO in Arabidopsis leaves and at late time points NO production coincided with the formation of hypersensitive response like lesions.1 Experiments using O3 and the NO-donor SNP alone or in combination indicated that both molecules are capable of activating a large set of stress related genes. In combined treatment, NO attenuated O3-induction of salicylic acid (SA) biosynthetic and signaling genes, and reduced SA accumulation. In addition, NO can elevate the levels of ethylene in several mutants. Thus, NO is a modifier of ROS signaling.
Key words: cell death, reactive oxygen species, ozone, nitric oxide, ethylene
Ozone (O3) is an air pollutant which in sensitive plants causes a reduction in photosynthesis and growth, ultimately leading to decreased growth and crop yields. induces the production of ROS by the O3 cells affected.2 These ROS include super-oxide anion (O2.-), hydrogen peroxide (H2O2) and hydroxyl radical (OH.-). The O3-induced quick burst of ROS resembles the oxidative burst in the hypersensitive response (HR) in incompatible plant pathogen interactions.3 The responses that follow the ROS burst include changes in the synthesis and accumulation of the plant stress hormones ethylene, salicylic acid (SA) and jasmonic acid and changes in gene expression.4,5 Eventually, the production of ROS can lead to HR-like cell death.2,5
In addition to ROS and hormones, nitric oxide (NO) has a prominent role in the defense against pathogens.6 Previous studies have shown that NO is quickly produced after pathogen attack and is involved in cell signaling during HR in plants.7,8 NO efficiently induces changes in gene expression9 suggesting that it has an active role in modifying plant stress responses. An important feature of NO is its lipophilic nature which enables its diffusion across plant membranes. NO can alter post-translational signaling by nitrosylation and/or direct binding to active centers of proteins, collectively making NO an effective signaling molecule.6
Recently we have shown that NO can modify cell death responses, signaling and gene expression in O3-exposed Arabidopsis plants.1 O3 induced NO production in a transient manner and production of NO occurred mainly in the area of O3-induced microlesions. Transcript profiling indicated a role for NO in attenuation of certain classes of O3 induced genes, many of which were related to SA biosynthesis or SA signaling. Furthermore, using mutants with altered levels of NO production we demonstrated that functional NO production is required for proper plant O3 responses. One of the earliest plant responses to O3 is ethylene production.2 A few studies indicate that NO and ethylene could interact in regulating stress responses, for example NO treatments induce production of ethylene in Arabidopsis and tobacco,10,11 and NO and ethylene are proposed to act together to regulate some O3 induced genes, exemplified by alternative oxidase AOX.11
To further dissect the interaction between NO and O3 we observed that both SNP (sodium nitroprusside) and O3 treatment of Col-0 increased expression of the ethylene biosynthesis related genes, ACS6 and ACC oxidase.1 O3 induced ACS6 expression correlates with ethylene formation.12 To confirm that SNP induce ethylene production we measured ethylene production in Col-0 and two mutants, rcd1 (NO overproducer) and Atnoa1/rif1 (reduced NO-production). SNP treatment increased ethylene production, particularly in the rcd1 mutant (Fig. 1). Interestingly, combined SNP + O3 treatment led to attenuation of ACS6 expression1 indicating that one role of NO during O3 could be to modulate ethylene responses.
Figure 1.
NO activates ethylene biosynthesis. 0.5 mM SnP treatment of Col-0, rcd1 and Atnoa1 lead to increase in ethylene formation.
Both SA and ethylene are regulators of ROS induced cell death.2,4 We propose that NO has a role in O3 induced signaling by modifying SA and ethylene levels and gene expression levels. Ethylene is known to be involved in lesion propagation and the elevated ethylene levels in all genotypes tested, especially in the O3 sensitive rcd1 (Fig. 1) suggests that NO indeed has a role in modifying hormone biosynthesis and accumulation.
Abbreviations
- NO
nitric oxide
- ROS
reactive oxygen species
- O3
ozone
- HR
hypersensitive response
- SA
salicylic acid
- SNP
sodium nitroprusside
Footnotes
Previously published online: www.landesbioscience.com/journals/psb/article/9428
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