Hunting for Plant Nitric Oxide Synthase Provides New Evidence of a Central Role for Plastids in Nitric Oxide Metabolism

Gas, Elisabet; Flores-Pérez, Úrsula; Sauret-Güeto, Susanna; Rodríguez‐Concepción, Manuel

doi:10.1105/tpc.108.065243

Cited by 148 publications

(121 citation statements)

References 60 publications

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“…However, recent evidence shows that AtNOA1 localizes in chloroplast (Flores-Pérez et al, 2008;Gas et al, 2009). Organelle localization of AtNOA1 suggests that activation of this protein requires signal transduction from extracellular stimuli to intracellular organelle.…”

Section: No Plays An Important Role In Extcam Guard Cell Signalingmentioning

confidence: 99%

A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and Hydrogen Peroxide Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis

Liu

et al. 2009

Plant Physiology

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Extracellular calmodulin (ExtCaM) regulates stomatal movement by eliciting a cascade of intracellular signaling events including heterotrimeric G protein, hydrogen peroxide (H 2 O 2 ), and Ca 2+ . However, the ExtCaM-mediated guard cell signaling pathway remains poorly understood. In this report, we show that Arabidopsis (Arabidopsis thaliana) NITRIC OXIDE ASSOCIATED1 (AtNOA1)-dependent nitric oxide (NO) accumulation plays a crucial role in ExtCaM-induced stomatal closure. ExtCaM triggered a significant increase in NO levels associated with stomatal closure in the wild type, but both effects were abolished in the Atnoa1 mutant. Furthermore, we found that ExtCaM-mediated NO generation is regulated by GPA1, the Ga-subunit of heterotrimeric G protein. The ExtCaM-dependent NO accumulation was nullified in gpa1 knockout mutants but enhanced by overexpression of a constitutively active form of GPA1 (cGa). In addition, cGa Atnoa1 and gpa1-2 Atnoa1 double mutants exhibited a similar response as did Atnoa1. The defect in gpa1 was rescued by overexpression of AtNOA1. Finally, we demonstrated that G protein activation of NO production depends on H 2 O 2 . Reduced H 2 O 2 levels in guard cells blocked the stomatal response of cGa lines, whereas exogenously applied H 2 O 2 rescued the defect in ExtCaM-mediated stomatal closure in gpa1 mutants. Moreover, the atrbohD/F mutant, which lacks the NADPH oxidase activity in guard cells, had impaired NO generation in response to ExtCaM, and H 2 O 2 -induced stomatal closure and NO accumulation were greatly impaired in Atnoa1. These findings have established a signaling pathway leading to ExtCaM-induced stomatal closure, which involves GPA1-dependent activation of H 2 O 2 production and subsequent AtNOA1-dependent NO accumulation.Plant guard cells control opening and closure of the stomata in response to phytohormones (e.g. abscisic acid [ABA]) and various environmental signals such as light and temperature, thereby regulating gas exchange for photosynthesis and water status via transpiration . Cytosolic calcium ([Ca 2+ ] i ) has been shown to be a key second messenger that changes in response to multiple stimuli in guard cells (McAinsh et al., 1995;Grabov and Blatt, 1998;Wood et al., 2000). A large proportion of Ca 2+ is localized in extracellular space. It has been shown that external Ca 2+ concentration ([Ca 2+ ] o ) promotes stomatal closure and induces oscillation in [Ca 2+ ] i in guard cells (MacRobbie, 1992;McAinsh et al., 1995;Allen et al., 2001 Calmodulin is a well-known Ca 2+ sensor that is activated upon binding of Ca 2+ . It has been shown that calmodulin exists not only intracellularly but also extracellularly in many plant species

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Section: No Plays An Important Role In Extcam Guard Cell Signalingmentioning

confidence: 99%

A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and Hydrogen Peroxide Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis

Liu

et al. 2009

Plant Physiology

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“…Unlike animal systems, knowledge of NO generation and subcellular location in plants remains largely elusive, and the data are sometimes contradictory and ambiguous (Zemojtel et al, 2006;Jasid et al, 2006;Gas et al, 2009). In previous studies, we detected L-Arg-dependent nitric oxide synthase (NOS) activity in isolated pea (Pisum sativum) leaf peroxisomes .…”

mentioning

confidence: 99%

Peroxisomes Are Required for in Vivo Nitric Oxide Accumulation in the Cytosol following Salinity Stress of Arabidopsis Plants

et al. 2009

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Peroxisomes are unique organelles involved in multiple cellular metabolic pathways. Nitric oxide (NO) is a free radical active in many physiological functions under normal and stress conditions. Using Arabidopsis (Arabidopsis thaliana) wild type and mutants expressing green fluorescent protein through the addition of peroxisomal targeting signal 1 (PTS1), which enables peroxisomes to be visualized in vivo, this study analyzes the temporal and cell distribution of NO during the development of 3-, 5-, 8-, and 11-d-old Arabidopsis seedlings and shows that Arabidopsis peroxisomes accumulate NO in vivo. Pharmacological analyses using nitric oxide synthase (NOS) inhibitors detected the presence of putative calcium-dependent NOS activity. Furthermore, peroxins Pex12 and Pex13 appear to be involved in transporting the putative NOS protein to peroxisomes, since pex12 and pex13 mutants, which are defective in PTS1-and PTS2-dependent protein transport to peroxisomes, registered lower NO content. Additionally, we show that under salinity stress (100 mM NaCl), peroxisomes are required for NO accumulation in the cytosol, thereby participating in the generation of peroxynitrite (ONOO 2 ) and in increasing protein tyrosine nitration, which is a marker of nitrosative stress.

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“…The results suggest that there may be a common mechanism for NO production in time and space in tobacco. Recent studies suggest that plastids play a central role for NO metabolism by investigating NOS (Gas et al 2009), and in several plant tissues and purified organelles, including mitochondria, the nucleus, and peroxisome, NOS-like activities have been (Barroso et al 1999;Corpas et al 2006;Tian et al 2007). Why NO was produced in these places is still unclear.…”

Section: Discussionmentioning

confidence: 99%

“…NO can be synthesized in plant by different routes, both enzymatically and nonenzymatically (Arisan et al 2009). Most work focuses on NOS-like enzyme (Gas et al 2009) and NR (Yamasaki and Sakihama 2000). Recent studies found that polyamine induced rapid biosynthesis of NO in Arabidopsis thaliana (Tun et al 2006;Yamasaki and Cohen 2006), suggesting there maybe a possible linkage between polyamine and nitric oxide.…”

Section: Electronic Supplementary Materialsmentioning

confidence: 99%

Nitric oxide production and its functional link with OIPK in tobacco defense response elicited by chitooligosaccharide

et al. 2011

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Chitooligosaccharide (COS) or oligochitosan has been shown to induce tobacco defense responses which are connected with nitric oxide (NO) and OIPK (oligochitosan-induced Ser/Thr protein kinase). The aim of this study was to reveal the relationship between NO production and OIPK pathway in the defense response of tobacco elicited by COS. NO generation was investigated by epidermal strip bioassay and fluorophore microscope using fluorophore diaminofluorescein diacetate (DAF-2DA). Tobacco epidermal cells treated with COS resulted in production of NO, which was first present in chloroplast, then in nucleus, finally in the whole cell; this NO production was sensitive to NO scavenger cPTIO and the mammalian NO synthase (NOS) inhibitor L-NAME, suggesting that NOS-like enzyme maybe involved in NO generation in tobacco epidermal cells. However, NOS and nitrate reductase (NR, EC 1.6.6.1) inhibitors reduced NO content in tobacco leaves by using NO Assay Kit, suggesting both NOS and NR were involved in NO production in tobacco leaves. Using a pharmacological approach and western blotting, we provide evidence that NO acts upstream of OIPK expression. NO scavenger, NOS inhibitor partly blocked the activation of OIPK and the activities of several defense-related enzymes induced by COS; treatment with NO donor sodium nitroprusside (SNP) induced the activation of OIPK and enhanced the defense systems. The results suggest that COS is able to induce NO generation, which results in up-regulation the activities of some defense-related enzymes through an OIPK-dependent or independent pathway.

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Hunting for Plant Nitric Oxide Synthase Provides New Evidence of a Central Role for Plastids in Nitric Oxide Metabolism

Cited by 148 publications

References 60 publications

A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and Hydrogen Peroxide Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis

A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and Hydrogen Peroxide Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis

Peroxisomes Are Required for in Vivo Nitric Oxide Accumulation in the Cytosol following Salinity Stress of Arabidopsis Plants

Nitric oxide production and its functional link with OIPK in tobacco defense response elicited by chitooligosaccharide

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