Plant Signaling Pathways Research Articles

Interactions Between Phosphorus, Zinc, and Iron Homeostasis in Nonmycorrhizal and Mycorrhizal Plants.

Phosphorus (P), zinc (Zn), and iron (Fe) are three essential elements for plant survival, and severe deficiencies in these nutrients lead to growth retardation and crop yield reduction. This review synthesizes recent progress on how plants coordinate the acquisition and signaling of Pi, Zn, and Fe from surrounding environments and which genes are involved in these Pi–Zn–Fe interactions with the aim of better understanding of the cross-talk between these macronutrient and micronutrient homeostasis in plants. In addition, identification of genes important for interactions between Pi, Zn, and/or Fe transport and signaling is a useful target for breeders for improvement in plant nutrient acquisition. Furthermore, to understand these processes in arbuscular mycorrhizal plants, the preliminary examination of interactions between Pi, Zn, and Fe homeostasis in some relevant crop species has been performed at the physiological level and is summarized in this article. In conclusion, the development of integrative study of cross-talks between Pi, Zn, and Fe signaling pathway in mycorrhizal plants will be essential for sustainable agriculture all around the world.

Comprehensive Understanding of the Interaction Among Stress Hormones Signalling Pathways by Gene Co-expression Network

Background: Plants respond to various stresses at the same time. Recent studies show that interactions of various phytohormones can play important roles in response to stresses. Objective: Although many studies have been done about the effects of the individual hormones, little information exists about the crosstalk among the hormone signalling pathways in plants. Methods: In this work, the weighted gene co-expression network analysis method was used to define modules containing genes with highly correlated expression patterns in response to abscisic acid, jasmonic acid, and salicylic acid in Arabidopsis. Results: Results indicate that plant hormones cause major changes the expression profile and control diverse cell functions, including response to environmental stresses and external factors, cell cycle, and antioxidant activity. In addition, AtbHLH15 and HY5 transcription factors can participate in phytochrome pathways in response to the phytohormones. It is probable that some Type III WRKY transcription factors control the response to bacterium separately from the other stresses. The E2Fa/DPa transcription factor also regulates the cell cycle. Conclusion: In general, many processes and pathways in plants may be regulated using a combination of abscisic acid, jasmonic acid, and salicylic acid.

Arabidopsis GCN2 kinase contributes to ABA homeostasis and stomatal immunity

General Control Non-derepressible 2 (GCN2) is an evolutionarily conserved serine/threonine kinase that modulates amino acid homeostasis in response to nutrient deprivation in yeast, human and other eukaryotes. However, the GCN2 signaling pathway in plants remains largely unknown. Here, we demonstrate that in Arabidopsis, bacterial infection activates AtGCN2-mediated phosphorylation of eIF2α and promotes TBF1 translational derepression. Consequently, TBF1 regulates a subset of abscisic acid signaling components to modulate pre-invasive immunity. We show that GCN2 fine-tunes abscisic acid accumulation and signaling during both pre-invasive and post-invasive stages of an infection event. Finally, we also demonstrate that AtGCN2 participates in signaling triggered by phytotoxin coronatine secreted by P. syringae. During the preinvasive phase, AtGCN2 regulates stomatal immunity by affecting pathogen-triggered stomatal closure and coronatine-mediated stomatal reopening. Our conclusions support a conserved role of GCN2 in various forms of immune responses across kingdoms, highlighting GCN2’s importance in studies on both plant and mammalian immunology.

A Transcriptomic Analysis Reveals Diverse Regulatory Networks That Respond to Cold Stress in Strawberry (Fragaria×ananassa)

Strawberry is often subjected to cold stress in temperate regions when insulation measures are not strictly applied in protected cultivation. Cold stress adversely influences plant growth and development by triggering a massive change to the transcriptome. To provide the potential strategies in improving strawberry cold tolerance and give a glimpse into the understanding of the complex cold signaling pathways in plants, this study identified attractive candidate genes and revealed diverse regulatory networks that responded to cold stress in strawberry (Fragaria×ananassa) by a transcriptomic analysis. Totally, there were 2397 differentially expressed genes (DEGs) under cold stress treatment (T1) vs. normal treatment (CK). Of these, 1180 DEGs were upregulated, while 1217 DEGs were downregulated. Functional enrichment analysis showed that DEGs were significantly (adjusted P value < 0.05) overrepresented in six pathways including plant hormone signal transduction, flavonoid biosynthesis, mitogen-activated protein kinase (MAPK) signaling, starch and sucrose metabolism, circadian rhythm, and alpha-linolenic acid metabolism. The cold signaling initiated expression of downstream cold-responsive (COR) genes with cis-acting element ABRE or CRT/DRE in the ABA-independent or ABA-dependent pathway to impel plant defense against the stress. Strikingly, GIGANTEA (gene id 101308922), two-component response regulator-like PRR95 (gene id 101295449), and ethylene-responsive transcription factor ERF105-like (gene id 101295082) were dramatically induced under low-temperature treatment, indicating that they played an important role in response to cold stress in strawberry.

Analysis of Protein Synthesis in Cucumber Leaves after Inoculation with Corynespora cassiicola: A Proteomic Approach.

Cucumber target leaf spot (TLS) disease caused by Corynespora cassiicola has become one of the most important fungal foliar diseases of cultivated cucumbers. However, the defense mechanisms of cucumber plants (Cucumis sativus) against C. cassiicola are still poorly understood. Here, proteins from resistant cucumber plants were analyzed using iTRAQ (isobaric tags for relative and absolute quantification) method. A total of 286 differentially expressed proteins were identified (p < 0.05, ratio > 1.2 or < 0.83) 6 and 24 h after pathogen inoculation in the resistant cultivar Jinyou 38 (the data are available via ProteomeXchange; identifier, PXD012903). Some of the early responses to C. cassiicola infection were revealed, and four factors related to the resistance of cucumber plants to TLS were discovered. First, the proteomic approach revealed modulation of signaling pathways in resistant cucumber plants in response to C. cassiicola infection. Second, the plant immune system recognizes the pathogen and initiates expression of immune response proteins, including those related to plant defense, stress response, signal transduction, cell metabolism, and redox regulation. Third, C. cassiicola activates common stress response pathways; in particular, mildew resistance locus O (MLO) proteins were found to play a crucial role in the TLS prevention. Fourth, rapid activation of the carbohydrate and secondary metabolic pathways, modification and reinforcement of cell walls, and adjustment of the apoplastic environment to the highly stressful conditions were crucial in the cucumber resistance to TLS. Overall, our data contribute to the understanding of interactions between plants and their pathogens and provide new insight into molecular processes involved in the resistance of cucumber plants to disease.

CYP707As are effectors of karrikin and strigolactone signalling pathways in Arabidopsis thaliana and parasitic plants.

Karrikins stimulate Arabidopsis thaliana germination, whereas parasitic weeds of the Orobanchaceae family have evolved to respond to host-exuded compounds such as strigolactones, dehydrocostus lactone, and 2-phenylethyl isothiocyanate. In Phelipanche ramosa, strigolactone-induced germination was shown to require one of the CYP707A proteins involved in abscisic acid catabolism. Here, germination and gene expression were analysed to investigate the role of CYP707As in germination of both parasitic plants and Arabidopsis upon perception of germination stimulants, after using pharmacological inhibitors and Arabidopsis mutants disrupting germination signals. CYP707A genes were up-regulated upon treatment with effective germination stimulants in both parasitic plants and Arabidopsis. Obligate parasitic plants exhibited both intensified up-regulation of CYP707A genes and increased sensitivity to the CYP707A inhibitor abscinazole-E2B, whereas Arabidopsis cyp707a mutants still positively responded to germination stimulation. In Arabidopsis, CYP707A regulation required the canonical karrikin signalling pathway KAI2/MAX2/SMAX1 and the transcription factor WRKY33. Finally, CYP707As and WRKY33 also modulated Arabidopsis root architecture in response to the synthetic strigolactone rac-GR24, and wrky33-1 exhibited a shoot hyperbranched phenotype. This study suggests that the lack of host-independent germination in obligate parasites is associated with an exacerbated CYP707A induction and that CYP707As and WRKY33 are new players involved in a variety of strigolactone/karrikin responses.

A calmodulin-gated calcium channel links pathogen patterns to plant immunity.

Pathogen-associated molecular patterns (PAMPs) activate innate immunity in both animals and plants. Although calcium has long been recognized as an essential signal for PAMP-triggered immunity in plants, the mechanism of PAMP-induced calcium signalling remains unknown1,2. Here we report that calcium nutrient status is critical for calcium-dependent PAMP-triggered immunity in plants. When calcium supply is sufficient, two genes that encode cyclic nucleotide-gated channel (CNGC) proteins, CNGC2 and CNGC4, are essential for PAMP-induced calcium signalling in Arabidopsis3-7. In a reconstitution system, we find that the CNGC2 and CNGC4 proteins together-but neither alone-assemble into a functional calcium channel that is blocked by calmodulin in the resting state. Upon pathogen attack, the channel is phosphorylated and activated by the effector kinase BOTRYTIS-INDUCED KINASE1 (BIK1) of the pattern-recognition receptor complex, and this triggers an increase in the concentration of cytosolic calcium8-10. The CNGC-mediated calcium entry thus provides a critical link between the pattern-recognition receptor complex and calcium-dependent immunity programs in the PAMP-triggered immunity signalling pathway in plants.

AraPPINet: An Updated Interactome for the Analysis of Hormone Signaling Crosstalk in Arabidopsis thaliana.

Protein-protein interactions (PPIs) play fundamental roles in various cellular processes. Here, we present a new version of computational interactome that contains more than 345,000 predicted PPIs involving about 51.2% of the Arabidopsis proteins. Compared to the earlier version, the updated AraPPINet displays a higher accuracy in predicting protein interactions through performance evaluation with independent datasets. In addition to the experimental verifications of the previous version, the new version has been subjected to further validation test that demonstrates its ability to discover novel PPIs involved in hormone signaling pathways. Moreover, network analysis shows that many overlapping proteins are significantly involved in the interactions which mediated the crosstalk among plant hormones. The new version of AraPPINet provides a more reliable interactome which would facilitate the understanding of crosstalk among hormone signaling pathways in plants.

Is There a Role for Glutaredoxins and BOLAs in the Perception of the Cellular Iron Status in Plants?

Glutaredoxins (GRXs) have at least three major identified functions. In apoforms, they exhibit oxidoreductase activity controlling notably protein glutathionylation/deglutathionylation. In holoforms, i.e., iron–sulfur (Fe–S) cluster-bridging forms, they act as maturation factors for the biogenesis of Fe–S proteins or as regulators of iron homeostasis contributing directly or indirectly to the sensing of cellular iron status and/or distribution. The latter functions seem intimately connected with the capacity of specific GRXs to form [2Fe–2S] cluster-bridging homodimeric or heterodimeric complexes with BOLA proteins. In yeast species, both proteins modulate the localization and/or activity of transcription factors regulating genes coding for proteins involved in iron uptake and intracellular sequestration in response notably to iron deficiency. Whereas vertebrate GRX and BOLA isoforms may display similar functions, the involved partner proteins are different. We perform here a critical evaluation of the results supporting the implication of both protein families in similar signaling pathways in plants and provide ideas and experimental strategies to delineate further their functions.

Mutations of the AtYAK1 Kinase Suppress TOR Deficiency in Arabidopsis

The target of rapamycin (TOR) kinase is a conserved energy sensor that regulates growth in response to environmental cues. However, little is known about the TOR signaling pathway in plants. We used Arabidopsis lines affected in the lethal with SEC13 protein 8 (LST8-1) gene, a core element of the TOR complex, to search for suppressor mutations. Two suppressor lines with improved growth were isolated that carried mutations in the Yet Another Kinase 1 (AtYAK1) gene encoding a member of the dual-specificity tyrosine phosphorylation-regulated kinase (DYRK) family. Atyak1 mutations partly rescued the developmental defects of lst8-1-1 mutants and conferred resistance to the TOR inhibitor AZD-8055. Moreover, atyak1 mutations suppressed the transcriptomic and metabolic perturbations as well as the abscisic acid (ABA)hypersensitivity of the lst8-1-1 mutants. AtYAK1 interacted with the regulatory-associated protein of TOR (RAPTOR), a component of the TOR complex, and was phosphorylated by TOR. Thus, our findings reveal that AtYAK1 is a TOR effector that probably needs to be switched off to activate plant growth.

A single residue change in the product of the chrysanthemum gene TPL1-2 leads to a failure in its repression of flowering

The TPL/TPR co-repressor is involved in many plant signaling pathways, including those regulating the switch from vegetative to reproductive growth. Here, a TPL homolog (TPL 1-2) was isolated from chrysanthemum. Its product was found to be deposited in the nucleus. The abundance of TPL1-2 transcript varied across the plant, with its highest level being recorded in the stem apex, and its lowest in the root and stem. In the leaf, the abundance of TPL1-2 transcript was highest at dusk in plants exposed to long days, and at dawn in those exposed to short days. Site-directed mutagenesis was used to induce an N176H mutation in TPL1-2. The constitutive expression in Arabidopsis thaliana of the wild type and the mutated alleles of TPL1-2 had a contrasting effect on flowering time, with the mutant transgene expressors flowering later than the wild type transgene expressors. The flowering-related genes FT, TSF, FUL and AP1 were all more strongly transcribed in the mutant transgene expressors than in the wild type transgene expressors.

Origin and Evolution of Core Components Responsible for Monitoring Light Environment Changes during Plant Terrestrialization

Light serves as the source of energy as well as an information signal for photosynthetic plants. During evolution, plants have acquired the ability to monitor environmental light radiation and adjust their developmental patterns to optimally utilize light energy for photosynthesis. The mechanisms of light perception and signal transduction have been comprehensively studied in past decades, mostly in a few model plants, including Arabidopsis thaliana. However, systematic analyses of the origin and evolution of core components involved in light perception and signaling are still lacking. In this study, we took advantage of the recently sequenced genomes and transcriptomes covering all the main Archaeplastida clades in the public domain to identify orthologous genes of core components involved in light perception and signaling and to reconstruct their evolutionary history. Our analyses suggested that acclimation to different distribution of light quality in new environments led to the origination of specific light signaling pathways in plants. The UVR8 (UV Resistance Locus 8) signaling pathway originated during the movement of plants from the deeper sea to shallow water and enabled plants to deal with ultraviolet B light (UV-B). After acquisition of UV-B adaptation, origination of the phytochrome signaling pathway helped plants to colonize water surface where red light became the prominent light energy source. The seedling emergence pathway, which is mediated by a combination of light and phytohormone signals that orchestrate plant growth pattern transitions, originated before the emergence of seed plants. Although cryptochromes and some key components of E3 ubiquitin ligase systems already existed before the divergence of the plant and animal kingdoms, the coevolution and optimization of light perception and downstream signal transduction components, including key transcription factors and E3 ubiquitin ligase systems, are evident during plant terrestrialization.

Cell cycle control by the target of rapamycin signalling pathway in plants.

Cells need to ensure a sufficient nutrient and energy supply before committing to proliferate. In response to positive mitogenic signals, such as light, sugar availability, and hormones, the target of rapamycin (TOR) signalling pathway promotes cell growth that connects to the entry and passage through the cell division cycle via multiple signalling mechanisms. Here, we summarize current understanding of cell cycle regulation by the RBR-E2F regulatory hub and the DREAM-like complexes, and highlight possible functional relationships between these regulators and TOR signalling. A genetic screen recently uncovered a downstream signalling component to TOR that regulates cell proliferation, YAK1, a member of the dual specificity tyrosine phosphorylation-regulated kinase (DYRK) family. YAK1 activates the plant-specific SIAMESE-RELATED (SMR) cyclin-dependent kinase inhibitors and therefore could be important to regulate both the CDKA-RBR-E2F pathway to control the G1/S transition and the mitotic CDKB1;1 to control the G2/M transition. TOR, as a master regulator of both protein synthesis-driven cell growth and cell proliferation is also central for cell size homeostasis. We conclude the review by briefly highlighting the potential applications of combining TOR and cell cycle knowledge in the context of ensuring future food security.

Identification of Molecular Integrators Shows that Nitrogen Actively Controls the Phosphate Starvation Response in Plants.

Nitrogen (N) and phosphorus (P) are key macronutrients sustaining plant growth and crop yield and ensuring food security worldwide. Understanding how plants perceive and interpret the combinatorial nature of these signals thus has important agricultural implications within the context of (1) increased food demand, (2) limited P supply, and (3) environmental pollution due to N fertilizer usage. Here, we report the discovery of an active control of P starvation response (PSR) by a combination of local and long-distance N signaling pathways in plants. We show that, in Arabidopsis (Arabidopsis thaliana), the nitrate transceptor CHLORINA1/NITRATE TRANSPORTER1.1 (CHL1/NRT1.1) is a component of this signaling crosstalk. We also demonstrate that this crosstalk is dependent on the control of the accumulation and turnover by N of the transcription factor PHOSPHATE STARVATION RESPONSE1 (PHR1), a master regulator of P sensing and signaling. We further show an important role of PHOSPHATE2 (PHO2) as an integrator of the N availability into the PSR since the effect of N on PSR is strongly affected in pho2 mutants. We finally show that PHO2 and NRT1.1 influence each other's transcript levels. These observations are summarized in a model representing a framework with several entry points where N signal influence PSR. Finally, we demonstrate that this phenomenon is conserved in rice (Oryza sativa) and wheat (Triticum aestivum), opening biotechnological perspectives in crop plants.

Exploring the nine realms of TOR.

The target of rapamycin (TOR) kinase regulates crucial cellular processes. Characterization of its signalling pathway in plants has lagged behind animals and yeast. A large-scale phosphoproteome and interactome analysis in Arabidopsis has now uncovered plant-specific and conserved TOR targets and interactors.

Lotus SHAGGY-like kinase1 is required to suppress nodulation in Lotus japonicus.

Glycogen synthase kinase/SHAGGY-like kinases (SKs) are a highly conserved family of signaling proteins that participate in many developmental, cell-differentiation, and metabolic signaling pathways in plants and animals. Here, we investigate the involvement of SKs in legume nodulation, a process requiring the integration of multiple signaling pathways. We describe a group of SKs in the model legume Lotus japonicus (LSKs), two of which respond to inoculation with the symbiotic nitrogen-fixing bacterium Mesorhizobium loti. RNAi knock-down plants and an insertion mutant for one of these genes, LSK1, display increased nodulation. Ηairy-root lines overexpressing LSK1 form only marginally fewer mature nodules compared with controls. The expression levels of genes involved in the autoregulation of nodulation (AON) mechanism are affected in LSK1 knock-down plants at low nitrate levels, both at early and late stages of nodulation. At higher levels of nitrate, these same plants show the opposite expression pattern of AON-related genes and lose the hypernodulation phenotype. Our findings reveal an additional role for the versatile SK gene family in integrating the signaling pathways governing legume nodulation, and pave the way for further study of their functions in legumes.

OsbZIP42 is a positive regulator of ABA signaling and confers drought tolerance to rice.

OsbZIP42 is a positive regulator of ABA signaling and drought stress tolerance. The activation of OsbZIP42 depends on stress-/ABA-activated protein kinase 4 (SAPK4) and an additional ABA-dependent modification of OsbZIP42. Basic leucine zipper transcription factors (bZIP TFs) play important roles in the ABA signaling pathway in plants. Rice OsbZIP42 is a member of the group E bZIP, which is an ortholog of Arabidopsis group A bZIP. This latter group includes abscisic acid-responsive element (ABRE)-binding factors (ABFs) involved in abiotic stress tolerance. The expression of OsbZIP42 was induced by ABA treatment, although it was not induced by drought and salt stresses. Unlike other bZIP TFs, OsbZIP42 contained two transcriptional activation domains. Although the full-length OsbZIP42 protein did not, the N-terminus of the protein interacted with SAPK4. Our results suggest that the activation of OsbZIP42 by SAPK4 requires another ABA-dependent modification of OsbZIP42. Transgenic rice overexpressing OsbZIP42 (OsbZIP42-OX) exhibited a rapidly elevated expression of the ABA-responsive LEA3 and Rab16 genes and was hypersensitive to ABA. Analyses of the OsbZIP42-OX plants revealed enhanced tolerance to drought stress. These results suggest that OsbZIP42 is a positive regulator of ABA signaling and drought stress tolerance depending on its activation, which is followed by an additional ABA-dependent modification. We propose that OsbZIP42 is an important player in rice for conferring ABA-dependent drought tolerance.

Biocontrol potential of a Bacillus subtilis strain BJ-1 against the rice blast fungus Magnaporthe oryzae

The biocontrol strain BJ-1 was isolated from a contaminated Magnaporthe oryzae culture plate and identified as Bacillus subtilis based on morphological characteristics, Biolog Microlog identification and 16S rDNA sequence analysis. The dual culture test showed that BJ-1 has a wide antimicrobial spectrum, and is especially potent against M. oryzae. The culture filtrates of BJ-1 significantly inhibited mycelial growth of M. oryzae P131, caused mycelial disintegration and induced swollen germ tubes. RT-PCR revealed the expressions of seven lipopeptide synthesis genes, encoding surfactin (srfAA and SPAB-ERIB), fengycin (fenB and FENCEA), subtilin (spa and spaS) and bacilysin (BACD) in BJ-1. Application of 1 × 108 CFU mL−1 bacterial cells or 5% culture filtrates of BJ-1 completely suppressed rice blast on detached leaves. In pot experiments, both spray and seed treatments using culture broth provided more than 50% disease suppression on rice blast. Interestingly, rice seeds soaked in culture broth of BJ-1 before planting induced host systemic resistance to inhibit rice blast development and promote plant growth, with disease reduction of over 70%, at a similar level as the fungicide tricyclazole. Expressions of two PR genes (OsPR1a and OsPR10) and three genes (OsPAL, OsICS1 and OsAOS2) known to function in salicylate- and jasmonate-dependent defence signalling pathways in rice plants after seed treatment by culture broth of BJ-1 were significantly induced. This is the first description of the use of B. subtilis as a seed treatment for control of rice blast and these results indicate that B. subtilis BJ-1 is a highly promising biocontrol agent for suppression of rice blast disease.

TOR сигнальная система в растениях

The mammalian target of rapamycin (TOR), is a protein Ser-Thr kinase that functions as a central element in a signaling pathway responsible for a cellular reaction towards stresss and nutrient/energy availability and promote appropriate changes in cell growth and proliferation, cell survival, and protein synthesis. Until now, study of the molecular mechanisms of TOR signaling pathway have been mainly focused on yeast and animal cells. As sessile organisms plants are limited to one habitat are obliged to constantly adjust the growth rates (expressed in increasing the size of organs) and development (consisting in the formation of new organs and structures) to the availability of nutrients. Furthermore, plants also overcome adverse external factors without being able to physically avoid them. Therefore, the disclosure of molecular mechanisms of the TOR signaling pathways in plants is the key to controlling stress resistance and plant productivity. Recent advances in the study of TOR signaling pathway in plants suggest a significant overlap in the cellular and developmental processes that are regulated by TOR in plants, animals and humans. The purpose of this review is to reveal the latest advances in studies of the TOR signaling pathway in plants Key words: TOR, mammals, plants, algae, Saccharomyces cerevisiae, rapamycin, autophagy, raptor.

The phytochrome-interacting family of transcription factors in maize (Zea mays L.): identification, evolution, and expression analysis

The phytochrome-interacting factor (PIF) subfamily of transcription factors is among the most important families of plant transcriptional regulators. PIFs regulate multiple biological processes, especially the photomorphogenic development. However, studies on PIF are mostly concentrated in Arabidopsis, little information on PIFs in maize (Zea mays L.) is currently available. The release of assembled genome sequences of maize enables the genome-wide investigation of maize PIF proteins. In this study, six PIF genes in maize were identified and named ZmPIF1–6. Among them, ZmPIF1 and ZmPIF3 were previously cloned in our laboratory. According to the structural features of their proteins, maize PIF genes (ZmPIFs) were classified into two main groups. Group I have an active phytochrome B (APB) domain and interacts with ZmphyB1. Group II has APA and APB domains and interacts with ZmphyA1 and ZmphyB1. The global expression patterns of ZmPIF genes in various tissues, as well as response of ZmPIF genes to diurnal rhythm, environmental stresses, and plant hormones were analyzed. The expression patterns of the ZmPIF genes suggested that ZmPIF1 and ZmPIF3 play an important role in the diurnal rhythm, while ZmPIF4 and ZmPIF6 are possibly the genes that respond to stimulation during plant growth and development. Meanwhile, the functions of ZmPIF2 and ZmPIF5 requires further investigation. These results can facilitate the exploration of the role of maize PIF-mediated plant signaling pathways and contribute to the development of molecular breeding for maize.