Plant Signaling Systems Research Articles

L-histidine makes Ni2+ ‘visible’ for plant signalling systems: Shading the light on Ni2+-induced Ca2+ and redox signalling in plants.

Nickel is both an important nutrient and an ecotoxicant for plants. Organic ligands, such as L-histidine (His), play a key role in Ni2+ detoxification. Here, we show that His (added together with 0.01-10 mM Ni2+) decreases Ni2+ toxicity to Arabidopsis thaliana roots not only as a result of a decrease in Ni2+ activity, but also via the induction of signalling phenomena important for adaptation such as the generation of reactive oxygen species (ROS) and cytosolic Ca2+ transients. With the use of EPR spectroscopy, we demonstrate that Ni-His complexes generate hydroxyl radicals that is not detected by the addition of Ni2+ or His separately. Similarly, Ni-His complexes, but not Ni2+, activate Ca2+ influx and K+ efflux currents in patch-clamped root protoplasts resulting in distinct cytosolic Ca2+ signals and a transient K+ release. His prevented programmed cell death symptoms (cytoplasm shrinkage, protease and endonuclease activation) induced by Ni2+ and inhibited Ni2+ accumulation at [Ni2+]>0.3 mM. Intriguingly, priming of roots with Ni-His stimulated plant resistance to Ni2+. Overall, these data show that His triggers ROS-Ca2+-mediated reactions making Ni2+ ‘visible’ for plant signalling machinery and facilitating adaptation to the excess Ni2+.

Novel Approach for EcoPhysiological and Biogeographic Understanding of Signaling Systems in Plants

Novel Approach for EcoPhysiological and Biogeographic Understanding of Signaling Systems in Plants

The Key Roles of ROS and RNS as a Signaling Molecule in Plant-Microbe Interactions.

Reactive oxygen species (ROS) and reactive nitrogen species (RNS) play a pivotal role in the dynamic cell signaling systems in plants, even under biotic and abiotic stress conditions. Over the past two decades, various studies have endorsed the notion that these molecules can act as intracellular and intercellular signaling molecules at a very low concentration to control plant growth and development, symbiotic association, and defense mechanisms in response to biotic and abiotic stress conditions. However, the upsurge of ROS and RNS under stressful conditions can lead to cell damage, retarded growth, and delayed development of plants. As signaling molecules, ROS and RNS have gained great attention from plant scientists and have been studied under different developmental stages of plants. However, the role of RNS and RNS signaling in plant-microbe interactions is still unknown. Different organelles of plant cells contain the enzymes necessary for the formation of ROS and RNS as well as their scavengers, and the spatial and temporal positions of these enzymes determine the signaling pathways. In the present review, we aimed to report the production of ROS and RNS, their role as signaling molecules during plant-microbe interactions, and the antioxidant system as a balancing system in the synthesis and elimination of these species.

Broadening the definition of a nervous system to better understand the evolution of plants and animals

ABSTRACT Most textbook definitions recognize only animals as having nervous systems. However, for the past couple decades, botanists have been meticulously studying long-distance signaling systems in plants, and some researchers have stated that plants have a simple nervous system. Thus, an academic conflict has emerged between those who defend and those who deny the existence of a nervous system in plants. This article analyses that debate, and we propose an alternative to answering yes or no: broadening the definition of a nervous system to include plants. We claim that a definition broader than the current one, which is based only on a phylogenetic viewpoint, would be helpful in obtaining a deeper understanding of how evolution has driven the features of signal generation, transmission and processing in multicellular beings. Also, we propose two possible definitions and exemplify how broader a definition allows for new viewpoints on the evolution of plants, animals and the nervous system.

Regulation of the activity of adenylate cyclases by hydrogen peroxide in pea root cells Infected with pathogens and a mutualist

This study examines the effect of a range of exogenous concentrations of hydrogen peroxide on the activity of transmembrane and soluble adenylate cyclases (EC 4.6.1.1) contained in root cells of pea seedlings infected with one of the following: Rhizobium leguminosarum bv. Viciae, Pseudomonas syringae pv. Pisi, and Clavibacter michiganensis ssp. sepedonicus. The results showed that the pool of intracellular H2O2 increased when pea roots were infected with bacteria regardless of type. The study analysed the concentration of intracellular cyclic adenosine monophosphate, a product of the adenosine triphosphate cyclization reaction catalyzed by transmembrane and soluble adenylate cyclases. The concentration of intracellular cyclic adenosine monophosphate increased when infected with either Rhizobium leguminosarum bv. viciae or Clavibacter michiganensis ssp. Sepedonicus; however, the concentration decreased by 20% when infected with Pseudomonas syringae pv. Pisi. The in vitro activity of soluble and transmembrane adenylate cyclases from pea root cells inoculated with Rhizobium leguminosarum bv. viciae was H2O2 dose-dependent: 100 nM of H2O2 reduced the activity of soluble and transmembrane adenylate cyclases slightly, while 26 µM inhibited their activity by 50–60%. When infected with Pseudomonas syringae pv. pisi, the reduction in the activity of soluble and transmembrane adenylate cyclases was independent of the concentrations of H2O2 in the range investigated. When infected with Clavibacter michiganensis ssp. sepedonicus, 100 nM of H2O2 inhibited the activity of transmembrane adenylate cyclases, although enhancing the activity of soluble adenylate cyclases. On the contrary, concentrations of H2O2 of 2.6 and 26 µM increased the activity of transmembrane adenylate cyclases and inhibited the activity of soluble adenylate cyclases. It can be concluded that the specific concentration of second messengers in plant cells depends on the specificity of the biotic stressor and forms, inter alia, by their mutual influence on the components of other plant signaling systems.

Effect of nodule and pathogenic bacteria on levels of nitric oxide and cyclic adenosine monophosphate in pea roots at initial stages of interaction

A significant role in the initial stages of rhizobial symbiosis formation in pea plants is performed by innate immunity. In this connection, the present study is focused on the concentration dynamics of two signalling molecules – nitric oxide (NO) and cyclic adenosine monophosphate (cAMP) – in the roots of etiolated seedlings of the Pisum sativum L. pea interacting with pathogenic (Pseudomonas syringae pv. Pisi) and nodule (Rhizobium leguminosarum bv. Viceae) bacteria. In time dynamics experiments, an endogenous rhythm of nitric oxide content changes in the root tissues of pea seedlings was characterised by an increase followed by a decrease in the level of nitric oxide and depending on exogenous biotic factors (symbiotic and pathogenic bacteria). Similar fluctuations were also observed when studying the dynamics of cyclic adenosine monophosphate concentration under the influence of the same biotic factors. The observed effects are assumed to be associated with certain exometabolites of Rhizobium leguminosarum bv. viceae (Nod-factors) and Pseudomonas syringae pv. pisi (cell wall exopolysaccharides) influencing the legume plant and activeting its innate immunity. Moreover, it is feasible that the different dynamics of changes in the studied components of the host plant signalling systems at the initial stages of interaction with symbiotic and pathogenic microorganisms have a variegated function: regulatory or protective in cases of symbiosis and pathogenesis, respectively. The observed change in the dynamics of the NO-synthase and adenylate cyclase signalling systems (NO and cAMP) components is assumed to be applied by the host plant as a “code” for transmitting a signal concerning the nature of the operating factor and the generation of corresponding reactions at the molecular level.

Implication of cAMP in Regulation of Hydrogen Peroxide Level in Pea Seedling Roots under Biotic Stress

Relationships between changes in the levels of intracellular cAMP and H2O2 were studied in various growth zones of pea (Pisumsativum L.) seedling roots upon infection with Rhizobium leguminosarum bv. viceae (Rlv), Pseudomonas syringae pv. pisi (Psp), or Clavibacter michiganensis ssp. sepedonicus (Cms). Previous studies have shown that these root zones are differentially sensitive to Rlv. In the present work, the highest level of H2O2 in growth zones of pea roots was observed after a short-term (5 min) inoculation with Rlv. In roots treated with Psp and Cms, the H2O2 contents were lower and showed little variation between Psp and Rlv treatments as well as between various growth zones. In all three treatments, the H2O2 content in seedling epicotyls decreased by approximately 20% with respect to the control level. Under these conditions, the level of intracellular cAMP increased substantially in almost all growth zones of pea seedling roots. The largest increase was observed upon the inoculation with Cms. The intracellular cAMP level was artificially increased by applying various concentrations of exogenous n-butyryl-cAMP known to readily permeate into the cells. At concentrations of 5 and 10 nM, n-butyryl-cAMP induced equal increases of H2O2 content in all analyzed zones, whereas the treatment with 50 nM n-butyryl-cAMP diminished H2O2 content in root zones and epicotyls. A 30-min incubation of samples in the presence of 10 or 50 nM n-butyryl-cAMP followed by a 5‑min infection with Rlv, Psp, and Cms significantly modified the H2O2 level in root growth zones. In order to decrease the intracellular content of cAMP, an inhibitor of transmembrane adenylate cyclase, suramin was applied. Under the action of suramin, the cAMP concentration in the root growth zones decreased by approximately 40%; in addition, the intracellular H2O2 content increased in the same root zones and in epicotyls. The treatment of seedlings with suramin followed by a 5-min incubation of plants in the presence of Rlv and Psp microorganisms led to insignificant lowering in the content of a signaling molecule H2O2, whereas the “suramin + Cms” treatment induced a larger decrease in H2O2 content, thus shifting it to the control level. It is concluded that, in plant cells exposed to biotic stressors, a certain concentration status of secondary messengers is established by virtue of their mutual influence on the components of other plant signaling systems.

A Lotus japonicus E3 ligase interacts with the Nod Factor Receptor 5 and positively regulates nodulation

BackgroundPost-translational modification of receptor proteins is involved in activation and de-activation of signalling systems in plants. Both ubiquitination and deubiquitination have been implicated in plant interactions with pathogens and symbionts.ResultsHere we present LjPUB13, a PUB-ARMADILLO repeat E3 ligase that specifically ubiquitinates the kinase domain of the Nod Factor receptor NFR5 and has a direct role in nodule organogenesis events in Lotus japonicus. Phenotypic analyses of three LORE1 retroelement insertion plant lines revealed that pub13 plants display delayed and reduced nodulation capacity and retarded growth. LjPUB13 expression is spatially regulated during symbiosis with Mesorhizobium loti, with increased levels in young developing nodules.ConclusionLjPUB13 is an E3 ligase with a positive regulatory role during the initial stages of nodulation in L. japonicus.

The Arabidopsis Calcium-Dependent Protein Kinases (CDPKs) and Their Roles in Plant Growth Regulation and Abiotic Stress Responses.

As a ubiquitous secondary messenger in plant signaling systems, calcium ions (Ca2+) play essential roles in plant growth and development. Within the cellular signaling network, the accurate decoding of diverse Ca2+ signal is a fundamental molecular event. Calcium-dependent protein kinases (CDPKs), identified commonly in plants, are a kind of vital regulatory protein deciphering calcium signals triggered by various developmental and environmental stimuli. This review chiefly introduces Ca2+ distribution in plant cells, the classification of Arabidopsis thaliana CDPKs (AtCDPKs), the identification of the Ca2+-AtCDPK signal transduction mechanism and AtCDPKs’ functions involved in plant growth regulation and abiotic stress responses. The review presents a comprehensive overview of AtCDPKs and may contribute to the research of CDPKs in other plants.

Protoplasts in plant signaling analysis: moving forward in the omics era

Genomic and functional analysis of plant signaling systems has reached a new level and an integrated understanding of the signaling system becomes unprecedentedly critical. Versatile cell-based ass...

Conservation of ethylene as a plant hormone over 450 million years of evolution.

Land plants evolved more than 450 million years ago from a lineage of freshwater charophyte green algae(1). The extent to which plant signalling systems existed before the evolutionary transition to land is unknown. Although charophytes occupy a key phylogenetic position for elucidating the origins of such signalling systems(2-4), there is a paucity of sequence data for these organisms(5,6). Here we carry out de novo transcriptomics of five representative charophyte species, and find putative homologues for the biosynthesis, transport, perception and signalling of major plant hormones. Focusing on the plant hormone ethylene, we provide evidence that the filamentous charophyte Spirogyra pratensis possesses an ethylene hormone system homologous to that in plants. Spirogyra produces ethylene and exhibits a cell elongation response to ethylene. Spirogyra ethylene-signalling homologues partially rescue mutants of the angiosperm Arabidopsis thaliana and respond post-translationally to ethylene when expressed in plant cells, indicative of unambiguously homologous ethylene-signalling pathways in Spirogyra and Arabidopsis. These findings imply that the common aquatic ancestor possessed this pathway prior to the colonization of land and that cell elongation was possibly an ancestral ethylene response. This highlights the importance of charophytes for investigating the origins of fundamental plant processes.

Towards Understanding Extracellular ROS Sensory and Signaling Systems in Plants

Reactive Oxygen Species (ROS) are ubiquitous metabolites in all aerobic organisms. Traditionally ROS have been considered as harmful, accidental byproducts of cellular functions involving electron transport chains or electron transfer. However, it is now recognized that controlled production of ROS has significant signaling functions, for example, in pathogen defense, in the regulation of stomatal closure, or in cell-to-cell signaling. ROS formation in subcellular compartments is critical to act as “alarm” signal in the response to stress, and the concept of ROS as primarily signaling substances has emerged. The involvement of ROS in several developmental and inducible processes implies that there must be coordinated function of signaling network(s) that govern ROS responses and subsequent processes. The air pollutant ozone can be used as a useful tool to elucidate the function of apoplastic ROS: O3degrades in cell wall into various ROS which are interpreted as ROS with signaling function inducing downstream responses. We have used ozone as a tool in mutant screens and transcript profiling-reverse genetics to identify genes involved in processes related to the signaling function of ROS. We review here our recent findings in the elucidation of apoplastic ROS sensing, signaling, and interaction with various symplastic components.

Do plant–plant signals mediate herbivory consistently in multiple taxa and ecological contexts?

It is becoming increasingly accepted that plant–plant signals can affect plant defense against herbivores. In a few taxa, both the mechanisms of plant–plant signaling and the ecological consequences are well described. However, the current adaptive explanations for plant–plant signaling rely heavily on many ecological contingencies, such as the behavior of herbivores and genetic structure of plant neighborhoods, making it unclear how frequently plant–plant signaling is important across the plant kingdom. Moreover, these same ecological contingencies mean that it may be beneficial for a plant to release a publicly available cue to coordinate its (or its neighbor's) defenses following herbivory in some cases, but it may be disadvantageous in others. In this paper, we focus on recent studies that expand the taxonomic breadth of plant–plant signaling about herbivores that bring classic plant–plant signaling systems into a broader ecological context, and those that find either no consequence or counterintuitive consequences of plant–plant signaling. There is currently a need to explore plant–plant signaling in taxonomically diverse plants and in various ecological settings.

AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction?

Since we are living in the 'age of transcription', awareness of aspects other than transcription in auxin signal transduction seems to have faded. One purpose of this review is to recall these other aspects. The focus will also be on the time scales of auxin responses and their potential or known dependence on either AUXIN BINDING PROTEIN 1 (ABP1) or on TRANSPORT-INHIBITOR-RESISTANT1 (TIR1) as a receptor. Furthermore, both direct and indirect evidence for the function of ABP1 as a receptor will be reviewed. Finally, the potential functions of a two-receptor system for auxin and similarities to other two-receptor signalling systems in plants will be discussed. It is suggested that such a functional arrangement is a property of plants which strengthens tissue autonomy and overcomes the lack of nerves or blood circulation which are responsible for rapid signal transport in animals.

Comprehensive Analysis ofCLEPolypeptide Signaling Gene Expression and Overexpression Activity in Arabidopsis

Intercellular signaling is essential for the coordination of growth and development in higher plants. Although hundreds of putative receptors have been identified in Arabidopsis (Arabidopsis thaliana), only a few families of extracellular signaling molecules have been discovered, and their biological roles are largely unknown. To expand our insight into the developmental processes potentially regulated by ligand-mediated signal transduction pathways, we undertook a systematic expression analysis of the members of the Arabidopsis CLAVATA3/ESR-RELATED (CLE) small signaling polypeptide family. Using reporter constructs, we show that the CLE genes have distinct and specific patterns of promoter activity. We find that each Arabidopsis tissue expresses at least one CLE gene, indicating that CLE-mediated signaling pathways are likely to play roles in many biological processes during the plant life cycle. Some CLE genes that are closely related in sequence have dissimilar expression profiles, yet in many tissues multiple CLE genes have overlapping patterns of promoter-driven reporter activity. This observation, plus the general absence of detectable morphological phenotypes in cle null mutants, suggest that a high degree of functional redundancy exists among CLE gene family members. Our work establishes a community resource of CLE-related biological materials and provides a platform for understanding and ultimately manipulating many different plant signaling systems.

Do plants dynamically regulate nectar features through sugar sensing?

Nectar properties (volume, concentration, viscosity) change dynamically in time. As stated by Pedersen some decades ago (1958), “Nectar is not a static product remaining outside the plant once produced but is in close contact with the plant system.”1 It is now evident that secretion may occur concomitantly with resorption and that the latter process sometimes continues after secretion has ended. The rate of the two processes may be modified dynamically by the plant in response to ecological and physiological constraints, maintaining a relatively constant nectar concentration to ensure pollinator visits (nectar homeostasis) and reallocating resources, especially during development of the ovules and pericarp after fertilization. We suspect that nectar resorption is under-estimated as a phenomenon, because it requires detailed information on the dynamics of nectar production throughout the life of the flower that is seldom available or taken into consideration. The cytological and molecular mechanisms involved in nectar resorption are almost completely unknown. Sugar sensing may have a fundamental role in nectar resorption and homeostasis. Due to direct contact with sugar solutions, nectaries may offer wide scope for insights into this phenomenon which has attracted interest as part of plant signalling systems. Addendum to: Nepi M, Stpiczyńska M. The complexity of nectar: Secretion and resorption dynamically regulate nectar features. Naturwissenschaften 2008 95:177-84.

Involvement of sphingosine kinase in plant cell signalling

In mammalian cells sphingosine-1-phosphate (S1P) is a well-established messenger molecule that participates in a wide range of signalling pathways. The objective of the work reported here was to investigate the extent to which phosphorylated long-chain sphingoid bases, such as sphingosine-1-phosphate and phytosphingosine-1-phosphate (phytoS1P) are used in plant cell signalling. To do this, we manipulated Arabidopsis genes capable of metabolizing these messenger molecules. We show that Sphingosine kinase1 (SPHK1) encodes an enzyme that phosphorylates sphingosine, phytosphingosine and other sphingoid long-chain bases. The stomata of SPHK1-KD Arabidopsis plants were less sensitive, whereas the stomata of SPHK1-OE plants were more sensitive, than wild type to ABA. The rate of germination of SPHK1-KD was enhanced, whereas the converse was true for SPHK1-OE seed. Reducing expression of either the putative Arabidopsis S1P phosphatase (SPPASE) or the DPL1 gene, which encodes an enzyme with S1P lyase activity, individually, had no effect on guard-cell ABA signalling; however, stomatal responses to ABA in SPPASEDPL1 RNAi plants were compromised. Reducing the expression of DPL1 had no effect on germination; however, germination of SPPASE RNAi seeds was more sensitive to applied ABA. We also found evidence that expression of SPHK1 and SPPASE were coordinately regulated, and discuss how this might contribute to robustness in guard-cell signalling. In summary, our data establish SPHK1 as a component in two separate plant signalling systems, opening the possibility that phosphorylated long-chain sphingoid bases such as S1P and phytoS1P are ubiquitous messengers in plants.

Plant signaling systems. Plastid-generated signals and their role in nuclear gene expression

Current concepts are outlined regarding the chloroplast effects on expression of the nuclear genes encoding plastid proteins. The major types of plastid-generated signals are considered. The signal molecules are shown to include the reactive oxygen species, the redox state of the components of photosynthetic electron transport, in particular plastoquinones, the redox-active molecules of plastid stroma, such as thioredoxin and glutathione, and also the intermediates of tetrapyrrole biosynthesis (Mg-protoporphyrin IX and its monomethyl ester). The sophisticated regulatory network is emphasized as a channel matching up the expression of nuclear and plastid genes. The plastid-generated signals help plants adapt to the changing and frequently adverse environmental conditions.

Protein sensors and transducers of cold and osmotic stress in cyanobacteria and plants

Genome-wide analysis of gene expression at the transcriptional level with DNA microarrays identified almost all genes induced by particular stress in cyanobacteria and plants. Adaptation to stress conditions starts with the perception and transduction of the stress signal. A combination of systematic mutagenesis of potential sensors and transducers with genome transcription profiling allowed significant progress in understanding the mechanisms responsible for the perception of stress signals in photosynthesizing cells. The review considers the recent data on the cyanobacterial and plant signaling systems perceiving and transmitting the cold, hyperosmotic, and salt stress signals.

Receptor kinase signaling in plant development.

The Arabidopsis genome sequence has revealed that plants contain a much larger complement of receptor kinase genes than other organisms. Early analysis of these genes revealed involvement in a diverse array of developmental and defense functions that included gametophyte development, pollen-pistil interactions, shoot apical meristem equilibrium, hormone perception, and cell morphogenesis. Amino acid sequence motifs and binding studies indicate that the ectodomains are capable of binding, either directly or indirectly, various classes of molecules including proteins, carbohydrates, and steroids. Genetic and biochemical approaches have begun to identify other components of several signal transduction pathways. Some receptor-like kinases (RLKs) appear to function with coreceptors lacking kinase domains, and genome analysis suggests this might be true for many RLKs. The KAPP protein phosphatase functions as a negative regulator of at least two RLK systems, and in vitro studies suggest it could be a common component of more. Whether plant signaling systems display a modularity similar to animal systems remains to be determined. Future efforts will reveal unknown functions of other RLKs and elucidate the relationships among their signaling networks.