Posttranslational regulation of photosynthetic activity via the TOR kinase in plants.

Chloroplasts are the powerhouse of the plant cell, and their activity must be matched to plant growth to avoid photooxidative damage. We have identified a posttranslational mechanism linking the eukaryotic target of rapamycin (TOR) kinase that promotes growth and the guanosine tetraphosphate (ppGpp) signaling pathway of prokaryotic origins that regulates chloroplast activity and photosynthesis in particular. We find that RelA SpoT homolog 3 (RSH3), a nuclear-encoded enzyme responsible for ppGpp biosynthesis, interacts directly with the TOR complex via a plant-specific amino-terminal region which is phosphorylated in a TOR-dependent manner. Down-regulating TOR activity causes a rapid increase in ppGpp synthesis in RSH3 overexpressors and reduces photosynthetic capacity in an RSH-dependent manner in wild-type plants. The TOR-RSH3 signaling axis therefore regulates the equilibrium between chloroplast activity and plant growth, setting a precedent for the regulation of organellar function by TOR.

CDC48 regulates immunity pathway in tobacco plants.

The CDC48 protein, highly conserved in the living kingdom, is a player of the ubiquitin proteasome system and contributes to various cellular processes. In plants, CDC48 is involved in cell division, plant growth and, as recently highlighted in several reports, in plant immunity. In the present study, to further extend our knowledge about CDC48 functions in plants, we analysed the incidence of its overexpression on tobacco development and immune responses. CDC48 overexpression disrupted plant development and morphology, induced changes in plastoglobule appearance and exacerbated ROS production. In addition, levels of salicylic acid (SA) and glycosylated SA were higher in transgenic plants, both in the basal state and in response to cryptogein, a protein produced by the oomycete Phytophthora cryptogea triggering defence responses. The expression of defence genes, notably those coding for some pathogenesis-related (PR) proteins, was also exacerbated in the basal state in transgenic plant lines. Finally, tobacco plants overexpressing CDC48 did not develop necrosis in response to tobacco mosaic virus (TMV) infection, suggesting a role for CDC48 in virus resistance.

Integrated multi-omics and genetic analyses reveal molecular determinants underlying Arabidopsis snap33 mutant phenotype.

The secretory pathway is essential for plant immunity, delivering diverse antimicrobial molecules into the extracellular space. Arabidopsis thaliana soluble N-ethylmaleimide-sensitive-factor attachment protein receptor SNAP33 is a key actor of this process. The snap33 mutant displays dwarfism and necrotic lesions, however the molecular determinants of its macroscopic phenotypes remain elusive. Here, we isolated several new snap33 mutants that exhibited constitutive cell death and H2O2 accumulation, further defining snap33 as an autoimmune mutant. We then carried out quantitative transcriptomic and proteomic analyses showing that numerous defense transcripts and proteins were up-regulated in the snap33 mutant, among which genes/proteins involved in defense hormone, pattern-triggered immunity, and nucleotide-binding domain leucine-rich-repeat receptor signaling. qRT-PCR analyses and hormone dosages supported these results. Furthermore, genetic analyses elucidated the diverse contributions of the main defense hormones and some nucleotide-binding domain leucine-rich-repeat receptor signaling actors in the establishment of the snap33 phenotype, emphasizing the preponderant role of salicylic acid over other defense phytohormones. Moreover, the accumulation of pattern-triggered immunity and nucleotide-binding domain leucine-rich-repeat receptor signaling proteins in the snap33 mutant was confirmed by immunoblotting analyses and further shown to be salicylic acid-dependent. Collectively, this study unveiled molecular determinants underlying the Arabidopsis snap33 mutant phenotype and brought new insights into autoimmunity signaling.

The improvement of the in vitro plant regeneration in barley with the epigenetic modifier of histone acetylation, trichostatin A.

Genotype-limited plant regeneration is one of the main obstacles to the broader use of genetic transformation in barley breeding. Thus, developing new approaches that might improve responses of in vitro recalcitrant genotypes remains at the center of barley biotechnology. Here, we analyzed different barley genotypes, including "Golden Promise," a genotype commonly used in the genetic transformation, and four malting barley cultivars of poor regenerative potential. The expression of hormone-related transcription factor (TF) genes with documented roles in plant regeneration was analyzed in genotypes with various plant-regenerating capacities. The results indicated differential expression of auxin-related TF genes between the barley genotypes in both the explants and the derived cultures. In support of the role of auxin in barley regeneration, distinct differences in the accumulation of free and oxidized auxin were observed in explants and explant-derived callus cultures of barley genotypes. Following the assumption that modifying gene expression might improve plant regeneration in barley, we treated the barley explants with trichostatin A (TSA), which affects histone acetylation. The effects of TSA were genotype-dependent as TSA treatment improved plant regeneration in two barley cultivars. TSA-induced changes in plant regeneration were associated with the increased expression of auxin biosynthesis-involved TFs. The study demonstrated that explant treatment with chromatin modifiers such as TSA might provide a new and effective epigenetic approach to improving plant regeneration in recalcitrant barley genotypes.

Biostimulation can prime elicitor induced resistance of grapevine leaves to downy mildew.

Using plant defense elicitors to protect crops against diseases is an attractive strategy to reduce chemical pesticide use. However, development of elicitors remains limited because of variable effectiveness in the field. In contrast to fungicides that directly target pathogens, elicitors activate plant immunity, which depends on plant physiological status. Other products, the biostimulants, can improve certain functions of plants. In this study, the objective was to determine whether a biostimulant via effects on grapevine physiology could increase effectiveness of a defense elicitor. A new methodology was developed to study biostimulant activity under controlled conditions using in vitro plantlets. Both biostimulant and defense elicitor used in the study were plant extracts. When added to the culture medium, the biostimulant accelerated the beginning of plantlet growth and affected the shoot and root development. It also modified metabolomes and phytohormone contents of leaves, stems, and roots. When applied on shoots, the defense elicitor changed metabolite and phytohormone contents, but effects were different depending on whether plantlets were biostimulated or controls. Defense responses and protection against Plasmopara viticola (downy mildew agent) were induced only for plantlets previously treated with the biostimulant, Therefore, the biostimulant may act by priming the defense elicitor action. In this study, a new method to screen biostimulants active on grapevine vegetative growth was used to demonstrate that a biostimulant can optimize the efficiency of a plant defense elicitor.

Involvement of sugar and abscisic acid in the genotype-specific response of rose to far-red light.

Plant architecture determines yield (fruit or flowers) and product quality in many horticultural species. It results from growth and branching processes and is dependent on genetic and environmental factors such as light quality. Highly significant genotype and light quality effects and their interaction have been demonstrated on the architecture of rose. Far-red (FR) light is known for its favourable effect on plant growth and development. We evaluated the effect of FR on rose growth and development and its interaction with the genotype through architectural, eco-physiological (net photosynthesis rate) and biochemical (sugar and hormone concentrations) approaches. Two cultivars ('The Fairy' - TF - and Knock Out® Radrazz - KO) with contrasting architectures were grown in a climate chamber under FR or in the absence of FR at an average photosynthetic photon flux density (400-700 nm) of 181.7 ± 12.8 µmol m-2 s-1 for 16 h. A significant effect of FR on the architecture of TF was demonstrated, marked by greater stem elongation, shoot branching and flowering, while KO remained insensitive to FR, supporting a genotype x FR interaction. The response of TF to FR was associated with improved photosynthetic capabilities, while KO exhibited an elevated level of abscisic acid (ABA) in its leaves. FR-dependent ABA accumulation might inhibit photosynthesis and prevent the increased plant carbon status required for growth. From a practical perspective, these findings argue in favour of a better reasoning of the choice of the cultivars grown in lighted production systems. Further investigations will be necessary to better understand these genotype-specific responses to FR and to unravel their molecular determinants.

Leafamine®, a Free Amino Acid-Rich Biostimulant, Promotes Growth Performance of Deficit-Irrigated Lettuce.

Water deficit causes substantial yield losses that climate change is going to make even more problematic. Sustainable agricultural practices are increasingly developed to improve plant tolerance to abiotic stresses. One innovative solution amongst others is the integration of plant biostimulants in agriculture. In this work, we investigate for the first time the effects of the biostimulant -Leafamine®-a protein hydrolysate on greenhouse lettuce (Lactuca sativa L.) grown under well-watered and water-deficit conditions. We examined the physiological and metabolomic water deficit responses of lettuce treated with Leafamine® (0.585 g/pot) or not. Root application of Leafamine® increased the shoot fresh biomass of both well-watered (+40%) and deficit-irrigated (+20%) lettuce plants because the projected leaf area increased. Our results also indicate that Leafamine® application could adjust the nitrogen metabolism by enhancing the total nitrogen content, amino acid (proline) contents and the total protein level in lettuce leaves, irrespective of the water condition. Osmolytes such as soluble sugars and polyols, also increased in Leafamine®-treated lettuce. Our findings suggest that the protective effect of Leafamine is a widespread change in plant metabolism and could involve ABA, putrescine and raffinose.

Guanosine tetraphosphate (ppGpp) accumulation inhibits chloroplast gene expression and promotes super grana formation in the moss Physcomitrium (Physcomitrella) patens.

The nucleotides guanosine tetraphosphate and pentaphosphate (or (p)ppGpp) are implicated in the regulation of chloroplast function in plants. (p)ppGpp signalling is best understood in the model vascular plant Arabidopsis thaliana in which it acts to regulate plastid gene expression to influence photosynthesis, plant development and immunity. However, little information is known about the conservation or diversity of (p)ppGpp signalling in other land plants. We studied the function of ppGpp in the moss Physcomitrium (previously Physcomitrella) patens using an inducible system for triggering ppGpp accumulation. We used this approach to investigate the effects of ppGpp on chloroplast function, photosynthesis and growth. We demonstrate that ppGpp accumulation causes a dramatic drop in photosynthetic capacity by inhibiting chloroplast gene expression. This was accompanied by the unexpected reorganisation of the thylakoid system into super grana. Surprisingly, these changes did not affect gametophore growth, suggesting that bryophytes and vascular plants may have different tolerances to defects in photosynthesis. Our findings point to the existence of both highly conserved and more specific targets of (p)ppGpp signalling in the land plants that may reflect different growth strategies.

A guanosine tetraphosphate (ppGpp) mediated brake on photosynthesis is required for acclimation to nitrogen limitation in Arabidopsis.

Guanosine pentaphosphate and tetraphosphate (together referred to as ppGpp) are hyperphosphorylated nucleotides found in bacteria and the chloroplasts of plants and algae. In plants and algae artificial ppGpp accumulation can inhibit chloroplast gene expression, and influence photosynthesis, nutrient remobilization, growth, and immunity. However, it is so far unknown whether ppGpp is required for abiotic stress acclimation in plants. Here, we demonstrate that ppGpp biosynthesis is necessary for acclimation to nitrogen starvation in Arabidopsis. We show that ppGpp is required for remodeling the photosynthetic electron transport chain to downregulate photosynthetic activity and for protection against oxidative stress. Furthermore, we demonstrate that ppGpp is required for coupling chloroplastic and nuclear gene expression during nitrogen starvation. Altogether, our work indicates that ppGpp is a pivotal regulator of chloroplast activity for stress acclimation in plants.

Plant nitrate supply regulates Erwinia amylovora virulence gene expression in Arabidopsis.

We showed previously that nitrogen (N) limitation decreases Arabidopsis resistance to Erwinia amylovora (Ea). We show that decreased resistance to bacteria in low N is correlated with lower apoplastic reactive oxygen species (ROS) accumulation and lower jasmonic acid (JA) pathway expression. Consistently, pretreatment with methyl jasmonate (Me-JA) increased the resistance of plants grown under low N. In parallel, we show that in planta titres of a nonvirulent type III secretion system (T3SS)-deficient Ea mutant were lower than those of wildtype Ea in low N, as expected, but surprisingly not in high N. This lack of difference in high N was consistent with the low expression of the T3SS-encoding hrp virulence genes by wildtype Ea in plants grown in high N compared to plants grown in low N. This suggests that expressing its virulence factors in planta could be a major limiting factor for Ea in the nonhost Arabidopsis. To test this hypothesis, we preincubated Ea in an inducing medium that triggers expression of hrp genes in vitro, prior to inoculation. This preincubation strongly enhanced Ea titres in planta, independently of the plant N status, and was correlated to a significant repression of JA-dependent genes. Finally, we identify two clusters of metabolites associated with resistance or with susceptibility to Ea. Altogether, our data showed that high susceptibility of Arabidopsis to Ea, under low N or following preincubation in hrp-inducing medium, is correlated with high expression of the Ea hrp genes in planta and low expression of the JA signalling pathway, and is correlated with the accumulation of specific metabolites.

Integration of the SMXL/D53 strigolactone signalling repressors in the model of shoot branching regulation in Pisum sativum.

DWARF53 (D53) in rice (Oryza sativa) and its homologs in Arabidopsis (Arabidopsis thaliana), SUPPRESSOR OF MAX2-LIKE 6 (SMXL6), SMXL7 and SMXL8, are well established negative regulators of strigolactone (SL) signalling in shoot branching regulation. Little is known of pea (Pisum sativum) homologs and whether D53 and related SMXLs are specific to SL signalling pathways. Here, we identify two allelic pea mutants, dormant3 (dor3), and demonstrate through gene mapping and sequencing that DOR3 corresponds to a homolog of D53 and SMXL6/SMXL7, designated PsSMXL7. Phenotype analysis, gene expression, protein and hormone quantification assays were performed to determine the role of PsSMXL7 in regulation of bud outgrowth and the role of PsSMXL7 and D53 in integrating SL and cytokinin (CK) responses. Like D53 and related SMXLs, we show that PsSMXL7 can be degraded by SL and induces feedback upregulation of PsSMXL7 transcript. Here we reveal a system conserved in pea and rice, whereby CK also upregulates PsSMXL7/D53 transcripts, providing a clear mechanism for SL and CK cross-talk in the regulation of branching. To further deepen our understanding of the branching network in pea, we provide evidence that SL acts via PsSMXL7 to modulate auxin content via PsAFB5, which itself regulates expression of SL biosynthesis genes. We therefore show that PsSMXL7 is key to a triple hormone network involving an auxin-SL feedback mechanism and SL-CK cross-talk.

RNAi suppression of DNA methylation affects the drought stress response and genome integrity in transgenic poplar.

Trees are long-lived organisms that continuously adapt to their environments, a process in which epigenetic mechanisms are likely to play a key role. Via downregulation of the chromatin remodeler DECREASED IN DNA METHYLATION 1 (DDM1) in poplar (Populus tremula × Populus alba) RNAi lines, we examined how DNA methylation coordinates genomic and physiological responses to moderate water deficit. We compared the growth and drought response of two RNAi-ddm1 lines to wild-type (WT) trees under well-watered and water deficit/rewatering conditions, and analyzed their methylomes, transcriptomes, mobilomes and phytohormone contents in the shoot apical meristem. The RNAi-ddm1 lines were more tolerant to drought-induced cavitation but did not differ in height or stem diameter growth. About 5000 differentially methylated regions were consistently detected in both RNAi-ddm1 lines, colocalizing with 910 genes and 89 active transposable elements. Under water deficit conditions, 136 differentially expressed genes were found, including many involved in phytohormone pathways; changes in phytohormone concentrations were also detected. Finally, the combination of hypomethylation and drought led to the mobility of two transposable elements. Our findings suggest major roles for DNA methylation in regulation of genes involved in hormone-related stress responses, and the maintenance of genome integrity through repression of transposable elements.

The miR166-SlHB15A regulatory module controls ovule development and parthenocarpic fruit set under adverse temperatures in tomato.

Fruit set is inhibited by adverse temperatures, with consequences on yield. We isolated a tomato mutant producing fruits under non-permissive hot temperatures and identified the causal gene as SlHB15A, belonging to class III homeodomain leucine-zipper transcription factors. SlHB15A loss-of-function mutants display aberrant ovule development that mimics transcriptional changes occurring in fertilized ovules and leads to parthenocarpic fruit set under optimal and non-permissive temperatures, in field and greenhouse conditions. Under cold growing conditions, SlHB15A is subjected to conditional haploinsufficiency and recessive dosage sensitivity controlled by microRNA 166 (miR166). Knockdown of SlHB15A alleles by miR166 leads to a continuum of aberrant ovules correlating with parthenocarpic fruit set. Consistent with this, plants harboring an Slhb15a-miRNA166-resistant allele developed normal ovules and were unable to set parthenocarpic fruit under cold conditions. DNA affinity purification sequencing and RNA-sequencing analyses revealed that SlHB15A is a bifunctional transcription factor expressed in the ovule integument. SlHB15A binds to the promoters of auxin-related genes to repress auxin signaling and to the promoters of ethylene-related genes to activate their expression. A survey of tomato genetic biodiversity identified pat and pat-1, two historical parthenocarpic mutants, as alleles of SlHB15A. Taken together, our findings demonstrate the role of SlHB15A as a sentinel to prevent fruit set in the absence of fertilization and provide a mean to enhance fruiting under extreme temperatures.

BdERECTA controls vasculature patterning and phloem-xylem organization in Brachypodium distachyon.

BACKGROUND: The vascular system of plants consists of two main tissue types, xylem and phloem. These tissues are organized into vascular bundles that are arranged into a complex network running through the plant that is essential for the viability of land plants. Despite their obvious importance, the genes involved in the organization of vascular tissues remain poorly understood in grasses. RESULTS: We studied in detail the vascular network in stems from the model grass Brachypodium distachyon (Brachypodium) and identified a large set of genes differentially expressed in vascular bundles versus parenchyma tissues. To decipher the underlying molecular mechanisms of vascularization in grasses, we conducted a forward genetic screen for abnormal vasculature. We identified a mutation that severely affected the organization of vascular tissues. This mutant displayed defects in anastomosis of the vascular network and uncommon amphivasal vascular bundles. The causal mutation is a premature stop codon in ERECTA, a LRR receptor-like serine/threonine-protein kinase. Mutations in this gene are pleiotropic indicating that it serves multiple roles during plant development. This mutant also displayed changes in cell wall composition, gene expression and hormone homeostasis. CONCLUSION: In summary, ERECTA has a pleiotropic role in Brachypodium. We propose a major role of ERECTA in vasculature anastomosis and vascular tissue organization in Brachypodium.

ppGpp influences protein protection, growth and photosynthesis in Phaeodactylum tricornutum.

Chloroplasts retain elements of a bacterial stress response pathway that is mediated by the signalling nucleotides guanosine penta- and tetraphosphate ((p)ppGpp). In the model flowering plant Arabidopsis, ppGpp acts as a potent regulator of plastid gene expression and influences photosynthesis, plant growth and development. However, little is known about ppGpp metabolism or its evolution in other photosynthetic eukaryotes. Here, we studied the function of ppGpp in the diatom Phaeodactylum tricornutum using transgenic lines containing an inducible system for ppGpp accumulation. We used these lines to investigate the effects of ppGpp on growth, photosynthesis, lipid metabolism and protein expression. We demonstrate that ppGpp accumulation reduces photosynthetic capacity and promotes a quiescent-like state with reduced proliferation and ageing. Strikingly, using nontargeted proteomics, we discovered that ppGpp accumulation also leads to the coordinated upregulation of a protein protection response in multiple cellular compartments. Our findings highlight the importance of ppGpp as a fundamental regulator of chloroplast function across different domains of life, and lead to new questions about the molecular mechanisms and roles of (p)ppGpp signalling in photosynthetic eukaryotes.

Salicylic acid is a key player of Arabidopsis autophagy mutant susceptibility to the necrotrophic bacterium Dickeya dadantii.

Autophagy is a ubiquitous vesicular process for protein and organelle recycling in eukaryotes. In plant, autophagy is reported to play pivotal roles in nutrient recycling, adaptation to biotic and abiotic stresses. The role of autophagy in plant immunity remains poorly understood. Several reports showed enhanced susceptibility of different Arabidopsis autophagy mutants (atg) to necrotrophic fungal pathogens. Interaction of necrotrophic bacterial pathogens with autophagy is overlooked. We then investigated such interaction by inoculating the necrotrophic enterobacterium Dickeya dadantii in leaves of the atg2 and atg5 mutants and an ATG8a overexpressing line. Overexpressing ATG8a enhances plant tolerance to D. dadantii. While atg5 mutant displayed similar susceptibility to the WT, the atg2 mutant exhibited accelerated leaf senescence and enhanced susceptibility upon infection. Both phenotypes were reversed when the sid2 mutation, abolishing SA signaling, was introduced in the atg2 mutant. High levels of SA signaling in atg2 mutant resulted in repression of the jasmonic acid (JA) defense pathway known to limit D. dadantii progression in A. thaliana. We provide evidence that in atg2 mutant, the disturbed hormonal balance leading to higher SA signaling is the main factor causing increased susceptibility to the D. dadantii necrotroph by repressing the JA pathway and accelerating developmental senescence.

Quantification of guanosine triphosphate and tetraphosphate in plants and algae using stable isotope-labelled internal standards.

Guanosine tetraphosphate (G4P) and guanosine pentaphosphate (G5P) are signalling nucleotides found in bacteria and photosynthetic eukaryotes that are implicated in a wide-range of processes including stress acclimation, developmental transitions and growth control. Measurements of G4P/G5P levels are essential for studying the diverse roles of these nucleotides. However, G4P/G5P quantification is particularly challenging in plants and algae due to lower cellular concentrations, compartmentalization and high metabolic complexity. Despite recent advances the speed and accuracy of G4P quantification in plants and algae can still be improved. Here, we report a new approach for rapid and accurate G4P quantification which relies on the use of synthesized stable isotope-labelled as internal standards. We anticipate that this approach will accelerate research into the function of G4P signaling in plants, algae and other organisms.

Involvement of Arabidopsis BIG protein in cell death mediated by Myo-inositol homeostasis.

Programmed cell death (PCD) is essential for several aspects of plant life. We previously identified the mips1 mutant of Arabidopsis thaliana, which is deficient for the enzyme catalysing myo-inositol synthesis, and that displays light-dependent formation of lesions on leaves due to Salicylic Acid (SA) over-accumulation. Rationale of this work was to identify novel regulators of plant PCD using a genetic approach. A screen for secondary mutations that abolish the mips1 PCD phenotype identified a mutation in the BIG gene, encoding a factor of unknown molecular function that was previously shown to play pleiotropic roles in plant development and defence. Physiological analyses showed that BIG is required for lesion formation in mips1 via SA-dependant signalling. big mutations partly rescued transcriptomic and metabolomics perturbations as stress-related phytohormones homeostasis. In addition, since loss of function of the ceramide synthase LOH2 was not able to abolish cell death induction in mips1, we show that PCD induction is not fully dependent of sphingolipid accumulation as previously suggested. Our results provide further insights into the role of the BIG protein in the control of MIPS1-dependent cell death and also into the impact of sphingolipid homeostasis in this pathway.

Hypomethylation of the aquatic invasive plant, Ludwigia grandiflora subsp. hexapetala mimics the adaptive transition into the terrestrial morphotype.

Ongoing global changes affect ecosystems and open up new opportunities for biological invasion. The ability of invasive species to rapidly adapt to new environments represents a relevant model for studying short-term adaptation mechanisms. The aquatic invasive plant, Ludwigia grandiflora subsp. hexapetala, is classified as harmful in European rivers. In French wet meadows, this species has shown a rapid transition from aquatic to terrestrial environments with emergence of two distinct morphotypes in 5 years. To understand the heritable mechanisms involved in adjustment to such a new environment, we investigate both genetic and epigenetic as possible sources of flexibility involved in this fast terrestrial transition. We found a low overall genetic differentiation between the two morphotypes arguing against the possibility that terrestrial morphotype emerged from a new adaptive genetic capacity. Artificial hypomethylation was induced on both morphotypes to assess the epigenetic hypothesis. We analyzed global DNA methylation, morphological changes, phytohormones and metabolite profiles of both morphotype responses in both aquatic and terrestrial conditions in shoot and root tissues. Hypomethylation significantly affected morphological variables, phytohormone levels and the amount of some metabolites. The effects of hypomethylation depended on morphotypes, conditions and plant tissues, which highlighted differences among the morphotypes and their plasticity. Using a correlative integrative approach, we showed that hypomethylation of the aquatic morphotype mimicked the characteristics of the terrestrial morphotype. Our data suggest that DNA methylation rather than a new adaptive genetic capacity is playing a key role in L. grandiflora subsp. hexapetala plasticity during its rapid aquatic to terrestrial transition.

GCN5 modulates salicylic acid homeostasis by regulating H3K14ac levels at the 5' and 3' ends of its target genes.

The modification of histones by acetyl groups has a key role in the regulation of chromatin structure and transcription. The Arabidopsis thaliana histone acetyltransferase GCN5 regulates histone modifications as part of the Spt-Ada-Gcn5 Acetyltransferase (SAGA) transcriptional coactivator complex. GCN5 was previously shown to acetylate lysine 14 of histone 3 (H3K14ac) in the promoter regions of its target genes even though GCN5 binding did not systematically correlate with gene activation. Here, we explored the mechanism through which GCN5 controls transcription. First, we fine-mapped its GCN5 binding sites genome-wide and then used several global methodologies (ATAC-seq, ChIP-seq and RNA-seq) to assess the effect of GCN5 loss-of-function on the expression and epigenetic regulation of its target genes. These analyses provided evidence that GCN5 has a dual role in the regulation of H3K14ac levels in their 5' and 3' ends of its target genes. While the gcn5 mutation led to a genome-wide decrease of H3K14ac in the 5' end of the GCN5 down-regulated targets, it also led to an increase of H3K14ac in the 3' ends of GCN5 up-regulated targets. Furthermore, genome-wide changes in H3K14ac levels in the gcn5 mutant correlated with changes in H3K9ac at both 5' and 3' ends, providing evidence for a molecular link between the depositions of these two histone modifications. To understand the biological relevance of these regulations, we showed that GCN5 participates in the responses to biotic stress by repressing salicylic acid (SA) accumulation and SA-mediated immunity, highlighting the role of this protein in the regulation of the crosstalk between diverse developmental and stress-responsive physiological programs. Hence, our results demonstrate that GCN5, through the modulation of H3K14ac levels on its targets, controls the balance between biotic and abiotic stress responses and is a master regulator of plant-environmental interactions.