An integral part of global environment change is an increase in the atmospheric concentration of CO2 (CO2) 1. Increased CO2 reduces leaf stomatal apertures and density of stomata that plays out as ...reductions in evapotranspiration 2–4. Surprisingly, given the importance of transpiration to the control of terrestrial water fluxes 5 and plant nutrient acquisition 6, we know comparatively little about the molecular components involved in the intracellular signaling pathways by which CO2 controls stomatal development and function 7. Here, we report that elevated CO2-induced closure and reductions in stomatal density require the generation of reactive oxygen species (ROS), thereby adding a new common element to these signaling pathways. We also show that the PYR/RCAR family of ABA receptors 8, 9 and ABA itself are required in both responses. Using genetic approaches, we show that ABA in guard cells or their precursors is sufficient to mediate the CO2-induced stomatal density response. Taken together, our results suggest that stomatal responses to increased CO2 operate through the intermediacy of ABA. In the case of CO2-induced reductions in stomatal aperture, this occurs by accessing the guard cell ABA signaling pathway. In both CO2-mediated responses, our data are consistent with a mechanism in which ABA increases the sensitivity of the system to CO2 but could also be explained by requirement for a CO2-induced increase in ABA biosynthesis specifically in the guard cell lineage. Furthermore, the dependency of stomatal CO2 signaling on ABA suggests that the ABA pathway is, in evolutionary terms, likely to be ancestral.
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•CO2-induced stomatal closure and density reduction require reactive oxygen species•CO2-induced stomatal closure and density reduction require ABA and ABA receptors•Guard cell/precursor ABA is sufficient to mediate closure and density reduction•Stomatal CO2 responses operating via ABA explains overlap between these pathways
Chater et al. describe the requirement for ABA and ABA signaling in both elevated CO2-induced stomatal closure and elevated CO2-induced reductions in stomatal density, suggesting that ABA itself is downstream of stomatal CO2 perception and that ABA signaling is likely to predate the origin of CO2-induced stomatal responses.
Nitric oxide (NO) is an immensely important signaling molecule in animals and plants. It is involved in plant reproduction, development, key physiological responses such as stomatal closure, and cell ...death. One of the controversies of NO metabolism in plants is the identification of enzymatic sources. Although there is little doubt that nitrate reductase (NR) is involved, the identification of a nitric oxide synthase (NOS)-like enzyme remains elusive, and it is becoming increasingly clear that such a protein does not exist in higher plants, even though homologues have been found in algae. Downstream from its production, NO can have several potential actions, but none of these will be in isolation from other reactive signaling molecules which have similar chemistry to NO. Therefore, NO metabolism will take place in an environment containing reactive oxygen species (ROS), hydrogen sulfide (H₂S), glutathione, other antioxidants and within a reducing redox state. Direct reactions with NO are likely to produce new signaling molecules such as peroxynitrite and nitrosothiols, and it is probable that chemical competitions will exist which will determine the ultimate end result of signaling responses. How NO is generated in plants cells and how NO fits into this complex cellular environment needs to be understood.
As with all organisms, plants must respond to a plethora of external environmental cues. Individual plant cells must also perceive and respond to a wide range of internal signals. It is now ...well-accepted that nitric oxide (NO) is a component of the repertoire of signals that a plant uses to both thrive and survive. Recent experimental data have shown, or at least implicated, the involvement of NO in reproductive processes, control of development and in the regulation of physiological responses such as stomatal closure. However, although studies concerning NO synthesis and signalling in animals are well-advanced, in plants there are still fundamental questions concerning how NO is produced and used that need to be answered. For example, there is a range of potential NO-generating enzymes in plants, but no obvious plant nitric oxide synthase (NOS) homolog has yet been identified. Some studies have shown the importance of NOS-like enzymes in mediating NO responses in plants, while other studies suggest that the enzyme nitrate reductase (NR) is more important. Still, more published work suggests the involvement of completely different enzymes in plant NO synthesis. Similarly, it is not always clear how NO mediates its responses. Although it appears that in plants, as in animals, NO can lead to an increase in the signal cGMP which leads to altered ion channel activity and gene expression, it is not understood how this actually occurs. NO is a relatively reactive compound, and it is not always easy to study. Furthermore, its biological activity needs to be considered in conjunction with that of other compounds such as reactive oxygen species (ROS) which can have a profound effect on both its accumulation and function. In this paper, we will review the present understanding of how NO is produced in plants, how it is removed when its signal is no longer required and how it may be both perceived and acted upon.
Summary
Nitric oxide (NO) and hydrogen peroxide (H2O2) are key signalling molecules produced in response to various stimuli and involved in a diverse range of plant signal transduction processes. ...Nitric oxide and H2O2 have been identified as essential components of the complex signalling network inducing stomatal closure in response to the phytohormone abscisic acid (ABA). A close inter‐relationship exists between ABA and the spatial and temporal production and action of both NO and H2O2 in guard cells. This study shows that, in Arabidopsis thaliana guard cells, ABA‐mediated NO generation is in fact dependent on ABA‐induced H2O2 production. Stomatal closure induced by H2O2 is inhibited by the removal of NO with NO scavenger, and both ABA and H2O2 stimulate guard cell NO synthesis. Conversely, NO‐induced stomatal closure does not require H2O2 synthesis nor does NO treatment induce H2O2 production in guard cells. Tungstate inhibition of the NO‐generating enzyme nitrate reductase (NR) attenuates NO production in response to nitrite in vitro and in response to H2O2 and ABA in vivo. Genetic data demonstrate that NR is the major source of NO in guard cells in response to ABA‐mediated H2O2 synthesis. In the NR double mutant nia1, nia2 both ABA and H2O2 fail to induce NO production or stomatal closure, but in the nitric oxide synthase deficient Atnos1 mutant, responses to H2O2 are not impaired. Importantly, we show that in the NADPH oxidase deficient double mutant atrbohD/F, NO synthesis and stomatal closure to ABA are severely reduced, indicating that endogenous H2O2 production induced by ABA is required for NO synthesis. In summary, our physiological and genetic data demonstrate a strong inter‐relationship between ABA, endogenous H2O2 and NO‐induced stomatal closure.
Oxidative stress, resulting from an imbalance in the accumulation and removal of reactive oxygen species such as hydrogen peroxide (H2O2), is a challenge faced by all aerobic organisms. In plants, ...exposure to various abiotic and biotic stresses results in accumulation of H2O2 and oxidative stress. Increasing evidence indicates that H2O2 functions as a stress signal in plants, mediating adaptive responses to various stresses. To analyze cellular responses to H2O2, we have undertaken a large-scale analysis of the Arabidopsis transcriptome during oxidative stress. Using cDNA microarray technology, we identified 175 non-redundant expressed sequence tags that are regulated by H2O2. Of these, 113 are induced and 62 are repressed by H2O2. A substantial proportion of these expressed sequence tags have predicted functions in cell rescue and defense processes. RNA-blot analyses of selected genes were used to verify the microarray data and extend them to demonstrate that other stresses such as wilting, UV irradiation, and elicitor challenge also induce the expression of many of these genes, both independently of, and, in some cases, via H2O2.
Summary
The phytohormones abscisic acid (ABA) and gibberellic acid (GA) antagonistically control the shift between seed dormancy and its alleviation. DELAY OF GERMINATION1 (DOG1) is a critical ...regulator that determines the intensity of primary seed dormancy, but its underlying regulatory mechanism is unclear.
In this study, we combined physiological, biochemical, and genetic approaches to reveal that a bHLH transcriptional factor WRKY36 progressively silenced DOG1 expression to break seed dormancy through ABI5‐BINDING PROTEIN 2 (AFP2) as the negative regulator of ABA signal.
AFP2 interacted with WRKY36, which recognizes the W‐BOX in the DOG1 promoter to suppress its expression; Overexpressing WRKY36 broke primary seed dormancy, whereas wrky36 mutants showed strong primary seed dormancy. In addition, AFP2 recruited the transcriptional corepressor TOPLESS‐RELATED PROTEIN2 (TPR2) to reduce histone acetylation at the DOG1 locus, ultimately mediating WRKY36‐dependent inhibition of DOG1 expression to break primary seed dormancy.
Our result proposes that the WRKY36‐AFP2‐TPR2 module progressively silences DOG1 expression epigenetically, thereby fine‐tuning primary seed dormancy.
Nitric Oxide Signalling in Plants Neill, Steven J.; Desikan, Radhika; Hancock, John T.
The New phytologist,
July 2003, Letnik:
159, Številka:
1
Journal Article
Recenzirano
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Recently nitric oxide (NO) has emerged as a key signalling molecule in plants. Here we review the potential sources of endogenous NO, outline the biological processes likely to be mediated by NO, and ...discuss the downstream signalling processes by which NO exerts its cellular effects. It will be important to develop methods to quantify intracellular NO synthesis and release. Clasification of the biosynthetic origins of NO is also required. NO can be synthesised from nitrite via nitrate reductase (NR) and although biochemical and immunological data indicate the presence of enzyme(s) similar to mammalian nitric oxide synthase (NOS), no NOS genes have been identified. NO can induce various processes in plants, including the expression of defence-related genes and programmed cell death (PCD), stomatal closure, seed germination and root development. Intracellular signalling responses to NO involve generation of cGMP, cADPR and elevation of cytosolic calcium, but in many cases, the precise biochemical and cellular nature of these responses has not been detailed. Research priorities here must be the reliable quantification of downstream signalling molecules in NO-responsive cells, and cloning and manipulation of the enzymes responsible for synthesis and degradation of these molecules.
Ethylene is a plant hormone that regulates many aspects of growth and development. Despite the well-known association between ethylene and stress signalling, its effects on stomatal movements are ...largely unexplored. Here, genetic and physiological data are provided that position ethylene into the Arabidopsis guard cell signalling network, and demonstrate a functional link between ethylene and hydrogen peroxide (H₂O₂). In wild-type leaves, ethylene induces stomatal closure that is dependent on H₂O₂ production in guard cells, generated by the nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) oxidase AtrbohF. Ethylene-induced closure is inhibited by the ethylene antagonists 1-MCP and silver. The ethylene receptor mutants etr1-1 and etr1-3 are insensitive to ethylene in terms of stomatal closure and H₂O₂ production. Stomata of the ethylene signalling ein2-1 and arr2 mutants do not close in response to either ethylene or H₂O₂ but do generate H₂O₂ following ethylene challenge. Thus, the data indicate that ethylene and H₂O₂ signalling in guard cells are mediated by ETR1 via EIN2 and ARR2-dependent pathway(s), and identify AtrbohF as a key mediator of stomatal responses to ethylene.
Plant roots are gravitropic, detecting and responding to changes in orientation via differential growth that results in bending and reestablishment of downward growth. Recent data support the basics ...of the Cholodny-Went hypothesis, indicating that differential growth is due to redistribution of auxin to the lower sides of gravistimulated roots, but little is known regarding the molecular details of such effects. Here, we investigate auxin and gravity signal transduction by demonstrating that the endogenous signaling molecules nitric oxide (NO) and cGMP mediate responses to gravistimulation in primary roots of soybean (Glycine max). Horizontal orientation of soybean roots caused the accumulation of both NO and cGMP in the primary root tip. Fluorescence confocal microcopy revealed that the accumulation of NO was asymmetric, with NO concentrating in the lower side of the root. Removal of NO with an NO scavenger or inhibition of NO synthesis via NO synthase inhibitors or an inhibitor of nitrate reductase reduced both NO accumulation and gravitropic bending, indicating that NO synthesis was required for the gravitropic responses and that both NO synthase and nitrate reductase may contribute to the synthesis of the NO required. Auxin induced NO accumulation in root protoplasts and asymmetric NO accumulation in root tips. Gravistimulation, NO, and auxin also induced the accumulation of cGMP, a response inhibited by removal of NO or by inhibitors of guanylyl cyclase, compounds that also reduced gravitropic bending. Asymmetric NO accumulation and gravitropic bending were both inhibited by an auxin transport inhibitor, and the inhibition of bending was overcome by treatment with NO or 8-bromo-cGMP, a cell-permeable analog of cGMP. These data indicate that auxin-induced NO and cGMP mediate gravitropic curvature in soybean roots.
It is now clear that hydrogen peroxide (H2O2) and nitric oxide (NO) function as signalling molecules in plants. A wide range of abiotic and biotic stresses results in H2O2 generation, from a variety ...of sources. H2O2 is removed from cells via a number of antioxidant mechanisms, both enzymatic and non‐enzymatic. Both biotic and abiotic stresses can induce NO synthesis, but the biosynthetic origins of NO in plants have not yet been resolved. Cellular responses to H2O2 and NO are complex, with considerable cross‐talk between responses to several stimuli. In this review the potential roles of H2O2 and NO during various stresses and the signalling pathways they activate are discussed. Key signalling components that might provide targets for enhancing crop production are also identified.
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