ABSTRACT
In plants, development of all above-ground tissues relies on the shoot apical meristem (SAM) which balances cell proliferation and differentiation to allow life-long growth. To maximize fitness and survival, meristem activity is adjusted to the prevailing conditions through a poorly understood integration of developmental signals with environmental and nutritional information. Here, we show that sugar signals influence SAM function by altering the protein levels of SHOOT MERISTEMLESS (STM), a key regulator of meristem maintenance. STM is less abundant in inflorescence meristems with lower sugar content, resulting from plants being grown or treated under limiting light conditions. Additionally, sucrose but not light is sufficient to sustain STM accumulation in excised inflorescences. Plants overexpressing the α1-subunit of SUCROSE-NON-FERMENTING1-RELATED KINASE 1 (SnRK1) accumulate less STM protein under optimal light conditions, despite higher sugar accumulation in the meristem. Furthermore, SnRK1α1 interacts physically with STM and inhibits its activity in reporter assays, suggesting that SnRK1 represses STM protein function. Contrasting the absence of growth defects in SnRK1α1 overexpressors, silencing SnRK1α in the SAM leads to meristem dysfunction and severe developmental phenotypes. This is accompanied by reduced STM transcript levels, suggesting indirect effects on STM. Altogether, we demonstrate that sugars promote STM accumulation and that the SnRK1 sugar sensor plays a dual role in the SAM, limiting STM function under unfavorable conditions but being required for overall meristem organization and integrity under favorable conditions. This highlights the importance of sugars and SnRK1 signaling for the proper coordination of meristem activities.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Gene Expression Regulation, Plant , Meristem , Protein Serine-Threonine Kinases , Signal Transduction , Arabidopsis/metabolism , Arabidopsis/genetics , Arabidopsis/growth & development , Meristem/metabolism , Meristem/growth & development , Meristem/genetics , Arabidopsis Proteins/metabolism , Arabidopsis Proteins/genetics , Protein Serine-Threonine Kinases/metabolism , Protein Serine-Threonine Kinases/genetics , Sucrose/metabolism , Sugars/metabolism , Light , Homeodomain ProteinsABSTRACT
Sugar signaling forms the basis of metabolic activities crucial for an organism to perform essential life activities. In plants, sugars like glucose, mediate a wide range of physiological responses ranging from seed germination to cell senescence. This has led to the elucidation of cell signaling pathways involving glucose and its counterparts and the mechanism of how these sugars take control over major hormonal pathways such as auxin, ethylene, abscisic acid and cytokinin in Arabidopsis. Plants use HXK1(Hexokinase) as a glucose sensor to modulate changes in photosynthetic gene expression in response to high glucose levels. Other proteins such as SIZ1, a major SUMO E3 ligase have recently been implicated in controlling sugar responses via transcriptional and translational regulation of a wide array of sugar metabolic genes. Here, we show that these two genes work antagonistically and are epistatic in controlling responsiveness toward high glucose conditions.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Abscisic Acid , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Glucose , Ligases/genetics , Plant Development , Ubiquitin-Protein Ligases/geneticsABSTRACT
Plants have evolved the adaptive capacity to mitigate the negative effect of external adversities at chemical, molecular, cellular, and physiological levels. This capacity is conferred by triggering the coordinated action of internal regulatory factors, in which sugars play an essential role in the regulating chloroplast degradation and leaf senescence under various stresses. In this review, we summarize the recent findings on the senescent-associated changes in carbohydrate metabolism and its relation to chlorophyl degradation, oxidative damage, photosynthesis inhibition, programmed cell death (PCD), and sink-source relation as affected by abiotic stresses. The action of sugar signaling in regulating the initiation and progression of leaf senescence under abiotic stresses involves interactions with various plant hormones, reactive oxygen species (ROS) burst, and protein kinases. This discussion aims to elucidate the complex regulatory network and molecular mechanisms that underline sugar-induced leaf senescence in response to various abiotic stresses. The imperative role of sugar signaling in regulating plant stress responses potentially enables the production of crop plants with modified sugar metabolism. This, in turn, may facilitate the engineering of plants with improved stress responses, optimal life span and higher yield achievement.
Subject(s)
Plant Leaves , Plant Senescence , Signal Transduction , Stress, Physiological , Sugars , Plant Leaves/metabolism , Plant Leaves/physiology , Sugars/metabolism , Carbohydrate Metabolism , Photosynthesis , Chloroplasts/metabolismABSTRACT
Heterotrimeric G-proteins are key modulators of multiple signaling and developmental pathways in plants, in which they act as molecular switches to engage in transmitting various stimuli signals from outside into the cells. Substantial studies have identiï¬ed G proteins as essential components of the organismal response to abiotic stress, leading to adaptation and survival in plants. Meanwhile, sugars are also well acknowledged key players in stress perception, signaling, and gene expression regulation. Connections between the two significant signaling pathways in stress response are of interest to a general audience in plant biology. In this article, advances unraveling a pivotal role of G proteins in the process of sugar signals outside the cells being translated into the operation of autophagy in cells during stress are reviewed. In addition, we have presented recent findings on G proteins regulating the response to drought, salt, alkali, cold, heat and other abiotic stresses. Perspectives on G-protein research are also provided in the end. Since G protein signaling regulates many agronomic traits, elucidation of detailed mechanism of the related pathways would provide useful insights for the breeding of abiotic stress resistant and high-yield crops.
Subject(s)
Heterotrimeric GTP-Binding Proteins , Plant Proteins , Signal Transduction , Stress, Physiological , Heterotrimeric GTP-Binding Proteins/metabolism , Heterotrimeric GTP-Binding Proteins/genetics , Plant Proteins/metabolism , Plant Proteins/genetics , Sugars/metabolism , Plants/metabolism , Gene Expression Regulation, Plant , Plant Physiological PhenomenaABSTRACT
Mosses hold a unique position in plant evolution and are crucial for protecting natural, long-term carbon storage systems such as permafrost and bogs. Due to small stature, mosses grow close to the soil surface and are exposed to high levels of CO2 , produced by soil respiration. However, the impact of elevated CO2 (eCO2 ) levels on mosses remains underexplored. We determined the growth responses of the moss Physcomitrium patens to eCO2 in combination with different nitrogen levels and characterized the underlying physiological and metabolic changes. Three distinct growth characteristics, an early transition to caulonema, the development of longer, highly pigmented rhizoids, and increased biomass, define the phenotypic responses of P. patens to eCO2 . Elevated CO2 impacts growth by enhancing the level of a sugar signaling metabolite, T6P. The quantity and form of nitrogen source influences these metabolic and phenotypic changes. Under eCO2 , P. patens exhibits a diffused growth pattern in the presence of nitrate, but ammonium supplementation results in dense growth with tall gametophores, demonstrating high phenotypic plasticity under different environments. These results provide a framework for comparing the eCO2 responses of P. patens with other plant groups and provide crucial insights into moss growth that may benefit climate change models.
Subject(s)
Carbon Dioxide , Nitrogen , Nitrogen/metabolism , Carbon Dioxide/pharmacology , Sugars , Biomass , SoilABSTRACT
BACKGROUND: Over the last decades, many strategies to procure and improve xylose consumption in Saccharomyces cerevisiae have been reported. This includes the introduction of efficient xylose-assimilating enzymes, the improvement of xylose transport, or the alteration of the sugar signaling response. However, different strain backgrounds are often used, making it difficult to determine if the findings are transferrable both to other xylose-consuming strains and to other xylose-assimilation pathways. For example, the influence of anomerization rates between α- and ß-xylopyranose in pathway optimization and sugar sensing is relatively unexplored. RESULTS: In this study, we tested the effect of expressing a xylose epimerase in S. cerevisiae strains carrying different xylose-consuming routes. First, XIs originating from three different species in isogenic S. cerevisiae strains were tested and the XI from Lachnoclostridium phytofermentans was found to give the best performance. The benefit of increasing the anomerization rate of xylose by adding a xylose epimerase to the XI strains was confirmed, as higher biomass formation and faster xylose consumption were obtained. However, the impact of xylose epimerase was XI-dependent, indicating that anomer preference may differ from enzyme to enzyme. The addition of the xylose epimerase in xylose reductase/xylitol dehydrogenase (XR/XDH)-carrying strains gave no improvement in xylose assimilation, suggesting that the XR from Spathaspora passalidarum had no anomer preference, in contrast to other reported XRs. The reduction in accumulated xylitol that was observed when the xylose epimerase was added may be associated with the upregulation of genes encoding endogenous aldose reductases which could be affected by the anomerization rate. Finally, xylose epimerase addition did not affect the sugar signaling, whereas the type of xylose pathway (XI vs. XR/XDH) did. CONCLUSIONS: Although xylose anomer specificity is often overlooked, the addition of xylose epimerase should be considered as a key engineering step, especially when using the best-performing XI enzyme from L. phytofermentans. Additional research into the binding mechanism of xylose is needed to elucidate the enzyme-specific effect and decrease in xylitol accumulation. Finally, the differences in sugar signaling responses between XI and XR/XDH strains indicate that either the redox balance or the growth rate impacts the SNF1/Mig1p sensing pathway.
ABSTRACT
Anthocyanin biosynthesis in plants is influenced by a wide range of environmental factors, such as light, temperature and nutrient availability. In this study, we revealed that the potassium-repressed anthocyanin accumulation in radish hypocotyls was associated with altered sugar distribution and sugar signaling pathways rather than changes in oxidative stress status. Sugar-feeding experiments suggested a hexokinase-independent glucose signal acted as a major contributor in regulating anthocyanin biosynthesis, transport and regulatory genes at the transcriptional level. Several R2R3-MYBs were identified as anthocyanin-related MYBs. Phylogenetic and protein sequence analyses suggested that RsMYB75 met the criteria of subgroup 6 MYB activator, while RsMYB39 and RsMYB82 seemed to be a non-canonical MYB anthocyanin activator and repressor, respectively. Through yeast-one-hybrid, dual-luciferase and transient expression assays, we confirmed that RsMYB39 strongly induced the promoter activity of anthocyanin transport-related gene RsGSTF12, while RsMYB82 significantly reduced anthocyanin biosynthesis gene RsANS1 expression. Molecular models are proposed in the discussion, allowing speculation on how these novel RsMYBs may regulate the expression levels of anthocyanin-related structural genes. Together, our data evidenced the strong impacts of potassium on sugar metabolism and signaling and its regulation of anthocyanin accumulation through different sugar signals and R2R3-MYBs in a hierarchical regulatory system.
Subject(s)
Anthocyanins , Raphanus , Transcription Factors/metabolism , Raphanus/genetics , Raphanus/metabolism , Sugars , Phylogeny , Plant Proteins/metabolism , Gene Expression Regulation, PlantABSTRACT
Salicylic acid (SA) is produced by plants in response to pathogen infection. SA binds the NONEXPRESSOR OF PATHOGENESIS-RELATED GENES (NPR) family of receptors to regulate both positive (NPR1) and negative (NPR3/4) plant immune responses by interacting with the clade II TGACG (TGA) motif-binding transcription factors (TGA2, TGA5, and TGA6). Here, we report that the principal metabolome-level response to SA treatment in Arabidopsis is a reduction in sucrose and other free sugars. We observed nearly identical effects in the tga256 triple mutant, which lacks all clade II TGA transcription factors. The tga256 mutant presents reduced leaf blade development and elongated hypocotyls, roots, and petioles consistent with sucrose starvation. No changes were detected in auxin levels, and mutant seedling growth could be restored to that of wild-type by sucrose supplementation. Although the retrograde signal 2-C-methyl-D-erythritol-2,4-cyclodiphosphate is known to stimulate SA biosynthesis and defense signaling, we detected no negative feedback by SA on this or any other intermediate of the 2-C-methyl-D-erythritol-4-phosphate pathway. Trehalose, a proxy for the sucrose regulator trehalose-6-phosphate (T6P), was highly reduced in tga256, suggesting that defense-related reductions in sugar availability may be controlled by changes in T6P levels. We conclude that the negative regulatory roles of TGA2/5/6 include maintaining sucrose levels in healthy plants. Disruption of TGA2/5/6-NPR3/4 inhibitory complexes by mutation or SA triggers sucrose reductions in Arabidopsis leaves, consistent with the 'pathogen starvation' hypothesis. These findings highlight sucrose availability as a mechanism by which TGA2/5/6 balance defense and development.
ABSTRACT
Nitrogen (N) is a basic building block that plays an essential role in the maintenance of normal plant growth and its metabolic functions through complex regulatory networks. Such the N metabolic network comprises a series of transcription factors (TFs), with the coordinated actions of phytohormone and sugar signaling to sustain cell homeostasis. The fluctuating N concentration in plant tissues alters the sensitivity of several signaling pathways to stressful environments and regulates the senescent-associated changes in cellular structure and metabolic process. Here, we review recent advances in the interaction between N assimilation and carbon metabolism in response to N deficiency and its regulation to the nutrient remobilization from source to sink during leaf senescence. The regulatory networks of N and sugar signaling for N deficiency-induced leaf senescence is further discussed to explain the effects of N deficiency on chloroplast disassembly, reactive oxygen species (ROS) burst, asparagine metabolism, sugar transport, autophagy process, Ca2+ signaling, circadian clock response, brassinazole-resistant 1 (BZRI), and other stress cell signaling. A comprehensive understanding for the metabolic mechanism and regulatory network underlying N deficiency-induced leaf senescence may provide a theoretical guide to optimize the source-sink relationship during grain filling for the achievement of high yield by a selection of crop cultivars with the properly prolonged lifespan of functional leaves and/or by appropriate agronomic managements.
ABSTRACT
Plants produce sugars by photosynthesis and use them for growth and development. Sugars are transported from source-to-sink organs via the phloem in the vasculature. It is well known that vascular development is precisely controlled by plant hormones and peptide hormones. However, the role of sugars in the regulation of vascular development is poorly understood. In this study, we examined the effects of sugars on vascular cell differentiation using a vascular cell induction system named 'Vascular Cell Induction Culture System Using Arabidopsis Leaves' (VISUAL). We found that sucrose has the strongest inhibitory effect on xylem differentiation, among several types of sugars. Transcriptome analysis revealed that sucrose suppresses xylem and phloem differentiation in cambial cells. Physiological and genetic analyses suggested that sucrose might function through the BRI1-EMS-SUPPRESSOR1 transcription factor, which is the central regulator of vascular cell differentiation. Conditional overexpression of cytosolic invertase led to a decrease in the number of cambium layers due to an imbalance between cell division and differentiation. Taken together, our results suggest that sucrose potentially acts as a signal that integrates environmental conditions with the developmental program.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Cambium/genetics , Cambium/metabolism , Cell Differentiation/genetics , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Phloem/metabolism , Xylem/metabolism , Sugars/metabolismABSTRACT
As an evolutionary strategy, plants overproduce ovaries as a safety net for survival, with those losing in the competition for resources being aborted. Grain abortion is, however, highly detrimental agronomically. The molecular basis of selective abortion of grain siblings remains unknown. In this opinion article we assess the current understanding of the molecular players controlling carbon resource import into ovaries and young grains, followed by an evaluation of the spatial hierarchy of sink capacity among grain siblings, focusing on the roles exerted by sugar transporters and enzymes. We argue that, upon sequential pollination and fertilization, robust activation of the carbon import and sugar signaling system plays a key role in establishing the capacity of grain siblings to acquire enough carbon resources to survive and thrive.
Subject(s)
Carbon , Edible Grain , Biological Transport , Biological Evolution , SugarsABSTRACT
Vacuolar Protein Sorting 8 (Vps8) protein is a specific subunit of the class C core vacuole/endosome tethering (CORVET) complex that plays a key role in endosomal trafficking in yeast (Saccharomyces cerevisiae). However, its functions remain largely unclear in plant vegetative growth. Here, we identified a soybean (Glycine max) T4219 mutant characterized with compact plant architecture. Map-based cloning targeted to a candidate gene GmVPS8a (Glyma.07g049700) and further found that two nucleotides deletion in the first exon of GmVPS8a causes a premature termination of the encoded protein in the T4219 mutant. Its functions were validated by CRISPR/Cas9-engineered mutation in the GmVPS8a gene that recapitulated the T4219 mutant phenotypes. Furthermore, NbVPS8a-silenced tobacco (Nicotiana benthamiana) plants exhibited similar phenotypes to the T4219 mutant, suggesting its conserved roles in plant growth. The GmVPS8a is widely expressed in multiple organs and its protein interacts with GmAra6a and GmRab5a. Combined analysis of transcriptomic and proteomic data revealed that dysfunction of GmVPS8a mainly affects pathways on auxin signal transduction, sugar transport and metabolism, and lipid metabolism. Collectively, our work reveals the function of GmVPS8a in plant architecture, which may extend a new way for genetic improvement of ideal plant-architecture breeding in soybean and other crops.
Subject(s)
Glycine max , Proteomics , Glycine max/genetics , Plant Breeding , Endosomes/metabolism , Vacuoles/metabolism , Saccharomyces cerevisiae/metabolismABSTRACT
Global climate change has altered, and will further alter, rainfall patterns and temperatures likely causing more frequent drought and heat waves, which will consequently exacerbate abiotic stresses of plants and significantly decrease the yield and quality of crops. On the one hand, the global demand for food is ever-increasing owing to the rapid increase of the human population. On the other hand, metabolic responses are one of the most important mechanisms by which plants adapt to and survive to abiotic stresses. Here we therefore summarize recent progresses including the plant primary and secondary metabolic responses to abiotic stresses and their function in plant resistance acting as antioxidants, osmoregulatory, and signaling factors, which enrich our knowledge concerning commonalities of plant metabolic responses to abiotic stresses, including their involvement in signaling processes. Finally, we discuss potential methods of metabolic fortification of crops in order to improve their abiotic stress tolerance.
Subject(s)
Adaptation, Physiological , Crops, Agricultural , Humans , Temperature , Signal Transduction , Stress, PhysiologicalABSTRACT
Lasiodiplodia theobromae is a causal agent of Botryosphaeria dieback, which seriously threatens grapevine production worldwide. Plant pathogens secrete diverse effectors to suppress host immune responses and promote the progression of infection, but the mechanisms underlying the manipulation of host immunity by L. theobromae effectors are poorly understood. In this study, we characterized LtCre1, which encodes a L. theobromae effector that suppresses BAX-triggered cell death in Nicotiana benthamiana. RNAi-silencing and overexpression of LtCre1 in L. theobromae showed impaired and increased virulence, respectively, and ectopic expression in N. benthamiana increased susceptibility. These results suggest that LtCre1 is as an essential virulence factor for L. theobromae. Protein-protein interaction studies revealed that LtCre1 interacts with grapevine RGS1-HXK1-interacting protein 1 (VvRHIP1). Ectopic overexpression of VvRHIP1 in N. benthamiana reduced infection, suggesting that VvRHIP1 enhances plant immunity against L. theobromae. LtCre1 was found to disrupt the formation of the VvRHIP1-VvRGS1 complex and to participate in regulating the plant sugar-signaling pathway. Thus, our results suggest that L. theobromae LtCre1 targets the grapevine VvRHIP1 protein to manipulate the sugar-signaling pathway by disrupting the association of the VvRHIP1-VvRGS1 complex.
Subject(s)
Ascomycota , Sugars , Sugars/metabolism , Ascomycota/physiology , Virulence , Virulence Factors/metabolism , Plant DiseasesABSTRACT
Plants have evolved multiple strategies to cope with rapid changes in the environment. During high light (HL) acclimation, the biosynthesis of photoprotective flavonoids, such as anthocyanins, is induced. However, the exact nature of the signal and downstream factors for HL induction of flavonoid biosynthesis (FB) is still under debate. Here, we show that carbon fixation in chloroplasts, subsequent export of photosynthates by triose phosphate/phosphate translocator (TPT), and rapid increase in cellular sugar content permit the transcriptional and metabolic activation of anthocyanin biosynthesis during HL acclimation. In combination with genetic and physiological analysis, targeted and whole-transcriptome gene expression studies suggest that reactive oxygen species and phytohormones play only a minor role in rapid HL induction of the anthocyanin branch of FB. In addition to transcripts of FB, sugar-responsive genes showed delayed repression or induction in tpt-2 during HL treatment, and a significant overlap with transcripts regulated by SNF1-related protein kinase 1 (SnRK1) was observed, including a central transcription factor of FB. Analysis of mutants with increased and repressed SnRK1 activity suggests that sugar-induced inactivation of SnRK1 is required for HL-mediated activation of anthocyanin biosynthesis. Our study emphasizes the central role of chloroplasts as sensors for environmental changes as well as the vital function of sugar signaling in plant acclimation.
Subject(s)
Anthocyanins , Sugars , Sugars/metabolism , Chloroplasts/metabolism , Plants/metabolism , Acclimatization , Phosphates/metabolism , Trioses/metabolismABSTRACT
In early developing tomato (Solanum lycopersicum L.) fruit, starch accumulates at high levels and is used by various primary metabolites in ripening fruits. ADP-glucose pyrophosphorylase is responsible for the first key step of starch biosynthesis. Although it has been reported that AgpL1 and AgpS1 isoforms are mainly expressed in early developing fruit, their regulatory mechanism has not been elucidated. The present study investigated the transcriptional response of AgpL1 and AgpS1 to various metabolizable sugars, nonmetabolizable sugar analogues, hexokinase inhibitors and proline by an experimental system using half-cut fruits. AgpL1 was upregulated in response to sucrose and constituted hexoses such glucose, whereas the AgpS1 gene almost did not exhibit a prominent sugar response. Further analyses revealed that other disaccharides such maltose and trehalose did not show a remarkable effect on both AgpL1 and AgpS1 expressions. These results indicate that there are two distinct regulatory mechanisms, namely, sugar metabolism-dependent and -independent, for the regulation of AGPase gene expression. Interestingly, the ADP treatment, a hexokinase inhibitors, cancelled the sugar response of AgpL1, indicating that hexokinase-mediated sugar signaling should be involved in the sugar response of AgpL1. These results suggest that sugar-dependent (AgpL1) and sugar-independent (AgpS1) pathways coordinatively regulate starch biosynthesis in immature tomato fruit.
ABSTRACT
Glucose-6-phosphate dehydrogenase (G6PDH) catalyzes a metabolic hub between glycolysis and the pentose phosphate pathway (PPP), which is the oxidation of glucose-6-phosphate (G6P) to 6-phosphogluconolactone concomitantly with the production of nicotinamide adenine dinucleotide phosphate (NADPH), a reducing power. It is considered to be the rate-limiting step that governs carbon flow through the oxidative pentose phosphate pathway (OPPP). The OPPP is the main supplier of reductant (NADPH) for several "reducing" biosynthetic reactions. Although it is involved in multiple physiological processes, current knowledge on its exact role and regulation is still piecemeal. The present review provides a concise and comprehensive picture of the diversity of plant G6PDHs and their role in seed germination, nitrogen assimilation, plant branching, and plant response to abiotic stress. This work will help define future research directions to improve our knowledge of G6PDHs in plant physiology and to integrate this hidden player in plant performance.
Subject(s)
Glucosephosphate Dehydrogenase , Plants , Glucosephosphate Dehydrogenase/metabolism , NADP/metabolism , Oxidation-Reduction , Plants/metabolism , Plant Physiological Phenomena , Pentose Phosphate PathwayABSTRACT
Plant receptors constitute a large protein family that regulates various aspects of development and responses to external cues. Functional characterization of this protein family and the identification of their ligands remain major challenges in plant biology. Previously, we identified plasma membrane-intrinsic sucrose-induced receptor kinase 1 (SIRK1) and Qian Shou kinase 1 (QSK1) as receptor/co-receptor pair involved in the regulation of aquaporins in response to osmotic conditions induced by sucrose. In this study, we identified a member of the elicitor peptide (PEP) family, namely PEP7, as the specific ligand of th receptor kinase SIRK1. PEP7 binds to the extracellular domain of SIRK1 with a binding constant of 1.44 ± 0.79 µM and is secreted to the apoplasm specifically in response to sucrose treatment. Stabilization of a signaling complex involving SIRK1, QSK1, and aquaporins as substrates is mediated by alterations in the external sucrose concentration or by PEP7 application. Moreover, the presence of PEP7 induces the phosphorylation of aquaporins in vivo and enhances water influx into protoplasts. Disturbed water influx, in turn, led to delayed lateral root development in the pep7 mutant. The loss-of-function mutant of SIRK1 is not responsive to external PEP7 treatment regarding kinase activity, aquaporin phosphorylation, water influx activity, and lateral root development. Taken together, our data indicate that the PEP7/SIRK1/QSK1 complex represents a crucial perception and response module that mediates sucrose-controlled water flux in plants and lateral root development.
Subject(s)
Aquaporins , Sucrose , Aquaporins/genetics , Aquaporins/metabolism , Gene Expression Regulation, Plant , Ligands , Peptides/metabolism , Plant Roots/metabolism , Sucrose/metabolism , Sucrose/pharmacology , Water/metabolismABSTRACT
Rapid callose accumulation has been shown to mediate defense in certain plant-virus interactions. Exposure to the green leaf volatile (Z)-3-hexenol (Z-3-HOL) can prime tomato (Solanum lycopersicum) for an enhanced defense against subsequent infection by whitefly-transmitted Tomato yellow leaf curl virus (TYLCV). However, the molecular mechanisms affecting Z-3-HOL-induced resistance are poorly understood. Here, we explored the mechanisms underlying Z-3-HOL-induced resistance against whitefly-transmitted TYLCV infection and the role of callose accumulation during this process. Tomato plants pre-treated with Z-3-HOL displayed callose priming upon whitefly infestation. The callose inhibitor 2-deoxy-d-glucose abolished Z-3-HOL-induced resistance, confirming the importance of callose in this induced resistance. We also found that Z-3-HOL pre-treatment enhanced salicylic acid levels and activated sugar signaling in tomato upon whitefly infestation, which increased the expression of the cell wall invertase gene Lin6 to trigger augmented callose deposition against TYLCV infection resulting from whitefly transmission. Using virus-induced gene silencing, we demonstrated the Lin6 expression is relevant for sugar accumulation mediated callose priming in restricting whitefly-transmitted TYLCV infection in plants that have been pre-treated with Z-3-HOL. Moreover, Lin6 induced the expression of the callose synthase gene Cals12, which is also required for Z-3-HOL-induced resistance of tomato against whitefly-transmitted TYLCV infection. These findings highlight the importance of sugar signaling in the priming of callose as a defense mechanism in Z-3-HOL-induced resistance of tomato against whitefly-transmitted TYLCV infection. The results will also increase our understanding of defense priming can be useful for the biological control of viral diseases.
Subject(s)
Begomovirus , Hemiptera , Solanum lycopersicum , Animals , Begomovirus/genetics , Solanum lycopersicum/genetics , Hemiptera/genetics , Plant Diseases/genetics , SugarsABSTRACT
Hexokinase (HXK) family proteins exert critical roles in catalyzing hexose phosphorylation, sugar sensing, and modulation of plant growth and stress adaptation. Nevertheless, a large amount remains unknown about the molecular profile of HXK enzymes in Populus trichocarpa, a woody model tree species. A genome-wide survey of HXK-encoding genes, including phylogenies, genomic structures, exon/intron organization, chromosomal distribution, and conserved features, was conducted, identifying six putative HXK isogenes (PtHXK1-6) in the Populus genome. The evolutionary tree demonstrated that 135 homologous HXKs between 17 plant species were categorized into four major subfamilies (type A, B, C, and D), clustering one plastidic (PtHXK3) and five mitochondrial PtHXKs grouped into type A and B, respectively. The in silico deduction prompted the presence of the conserved sugar-binding core (motif 4), phosphorylation sites (motif 2 and 3), and adenosine-binding domains (motif 7). The transcriptomic sequencing (RNA-seq) and the quantitative real-time PCR (qRT-PCR) assays revealed that three isogenes (PtHXK2, 3, and 6) were abundantly expressed in leaves, stems, and roots, while others appeared to be dominantly expressed in the reproductive tissues. Under the stress exposure, PtHXK2 and 6 displayed a significant induction upon the pathogenic fungi (Fusarium solani) infection and marked promotions by glucose feeding in roots. In contrast, the PtHXK3 and 6 are ABA-responsive genes, following a dose-dependent manner. The comprehensive analyses of the genomic patterns and expression profiling provide theoretical clues and lay a foundation for unraveling the physiological and signaling roles underlying the fine-tuned PtHXKs responding to diverse stressors.