Corrigendum: Essential Oils prime epigenetic and metabolomic changes in tomato defense against Fusarium oxysporum.

[This corrects the article DOI: 10.3389/fpls.2022.804104.].

Recent advances in research on phosphate starvation signaling in plants.

Phosphorus is indispensable for plant growth and development, with its status crucial for determining crop productivity. Plants have evolved various biochemical, morphological, and developmental responses to thrive under conditions of low P availability, as inorganic phosphate (Pi), the primary form of P uptake, is often insoluble in soils. Over the past 25 years, extensive research has focused on understanding these responses, collectively forming the Pi starvation response system. This effort has not only expanded our knowledge of strategies to cope with Pi starvation (PS) but also confirmed their adaptive significance. Moreover, it has identified and characterized numerous components of the intricate regulatory network governing P homeostasis. This review emphasizes recent advances in PS signaling, particularly highlighting the physiological importance of local PS signaling in inhibiting primary root growth and uncovering the role of TORC1 signaling in this process. Additionally, advancements in understanding shoot-root Pi allocation and a novel technique for studying Pi distribution in plants are discussed. Furthermore, emerging data on the regulation of plant-microorganism interactions by the PS regulatory system, crosstalk between the signaling pathways of phosphate starvation, phytohormones and immunity, and recent studies on natural variation in Pi homeostasis are addressed.

Iron Homeostasis in Azotobacter vinelandii.

Iron is an essential nutrient for all life forms. Specialized mechanisms exist in bacteria to ensure iron uptake and its delivery to key enzymes within the cell, while preventing toxicity. Iron uptake and exchange networks must adapt to the different environmental conditions, particularly those that require the biosynthesis of multiple iron proteins, such as nitrogen fixation. In this review, we outline the mechanisms that the model diazotrophic bacterium Azotobacter vinelandii uses to ensure iron nutrition and how it adapts Fe metabolism to diazotrophic growth.

Essential Oils Prime Epigenetic and Metabolomic Changes in Tomato Defense Against Fusarium oxysporum.

In this work, we studied the direct and indirect plant protection effects of an Artemisia absinthium essential oil (AEO) on tomato seedlings against Fusarium oxysporum sp. oxysporum radicis lycopersici (Fol). AEO exhibited a toxic effect in vitro against Fol. Additionally, tomato seedlings germinated from seeds pretreated with AEO and grown hydroponically were protected against Fol. Plant disease symptoms, including, water and fresh weight loss, tissue necrosis, and chlorosis were less pronounced in AEO-treated seedlings. AEO also contributed to plant defenses by increasing callose deposition and the production of reactive oxygen species (ROS) on seed surfaces without affecting seed germination or plant development. The essential oil seed coating also primed a durable tomato seedling defense against the fungus at later stages of plant development. RNA-seq and metabolomic analysis performed on seedlings after 12 days showed that the AEO treatment on seeds induced transcriptomic and metabolic changes. The metabolomic analysis showed an induction of vanillic acid, coumarin, lycopene, oleamide, and an unknown metabolite of m/z 529 in the presence of Fol. The StNRPD2 gene, the second largest component of RNA polymerases IV and V directly involved in de novo cytosine methylation by RNA-directed DNA methylation (RdDM), was highly induced in the presence of AEO. The host methionine cycle (MTC) controlling trans-methylation reactions, was also altered by AEO through the high induction of S-adenosyl methionine transferases (SAMts). Our results suggest that AEO treatment could induce de novo epigenetic changes in tomato, modulating the speed and extent of its immune response to Fol. The EO-seed coating could be a new strategy to prime durable tomato resistance, compatible with other environmentally friendly biopesticides.

Plant adaptation to low phosphorus availability: Core signaling, crosstalks, and applied implications.

Phosphorus (P) is an essential nutrient for plant growth and reproduction. Plants preferentially absorb P as orthophosphate (Pi), an ion that displays low solubility and that is readily fixed in the soil, making P limitation a condition common to many soils and Pi fertilization an inefficient practice. To cope with Pi limitation, plants have evolved a series of developmental and physiological responses, collectively known as the Pi starvation rescue system (PSR), aimed to improve Pi acquisition and use efficiency (PUE) and protect from Pi-starvation-induced stress. Intensive research has been carried out during the last 20 years to unravel the mechanisms underlying the control of the PSR in plants. Here we review the results of this research effort that have led to the identification and characterization of several core Pi starvation signaling components, including sensors, transcription factors, microRNAs (miRNAs) and miRNA inhibitors, kinases, phosphatases, and components of the proteostasis machinery. We also refer to recent results revealing the existence of intricate signaling interplays between Pi and other nutrients and antagonists, N, Fe, Zn, and As, that have changed the initial single-nutrient-centric view to a more integrated view of nutrient homeostasis. Finally, we discuss advances toward improving PUE and future research priorities.

Short-Chain Chitin Oligomers: Promoters of Plant Growth.

Chitin is the second most abundant biopolymer in nature after cellulose, and it forms an integral part of insect exoskeletons, crustacean shells, krill and the cell walls of fungal spores, where it is present as a high-molecular-weight molecule. In this study, we showed that a chitin oligosaccharide of lower molecular weight (tetramer) induced genes in Arabidopsis that are principally related to vegetative growth, development and carbon and nitrogen metabolism. Based on plant responses to this chitin tetramer, a low-molecular-weight chitin mix (CHL) enriched to 92% with dimers (2mer), trimers (3mer) and tetramers (4mer) was produced for potential use in biotechnological processes. Compared with untreated plants, CHL-treated plants had increased in vitro fresh weight (10%), radicle length (25%) and total carbon and nitrogen content (6% and 8%, respectively). Our data show that low-molecular-weight forms of chitin might play a role in nature as bio-stimulators of plant growth, and they are also a known direct source of carbon and nitrogen for soil biomass. The biochemical properties of the CHL mix might make it useful as a non-contaminating bio-stimulant of plant growth and a soil restorer for greenhouses and fields.

Transcriptionally Driven DNA Replication Program of the Human Parasite Leishmania major.

Faithful inheritance of eukaryotic genomes requires the orchestrated activation of multiple DNA replication origins (ORIs). Although origin firing is mechanistically conserved, how origins are specified and selected for activation varies across different model systems. Here, we provide a complete analysis of the nucleosomal landscape and replication program of the human parasite Leishmania major, building on a better evolutionary understanding of replication organization in Eukarya. We found that active transcription is a driving force for the nucleosomal organization of the L. major genome and that both the spatial and the temporal program of DNA replication can be explained as associated to RNA polymerase kinetics. This simple scenario likely provides flexibility and robustness to deal with the environmental changes that impose alterations in the genetic programs during parasitic life cycle stages. Our findings also suggest that coupling replication initiation to transcription elongation could be an ancient solution used by eukaryotic cells for origin maintenance.

Kinetics of Nif gene expression in a nitrogen-fixing bacterium.

Nitrogen fixation is a tightly regulated trait. Switching from N2 fixation-repressing conditions to the N2-fixing state is carefully controlled in diazotrophic bacteria mainly because of the high energy demand that it imposes. By using quantitative real-time PCR and quantitative immunoblotting, we show here how nitrogen fixation (nif) gene expression develops in Azotobacter vinelandii upon derepression. Transient expression of the transcriptional activator-encoding gene, nifA, was followed by subsequent, longer-duration waves of expression of the nitrogenase biosynthetic and structural genes. Importantly, expression timing, expression levels, and NifA dependence varied greatly among the nif operons. Moreover, the exact concentrations of Nif proteins and their changes over time were determined for the first time. Nif protein concentrations were exquisitely balanced, with FeMo cofactor biosynthetic proteins accumulating at levels 50- to 100-fold lower than those of the structural proteins. Mutants lacking nitrogenase structural genes or impaired in FeMo cofactor biosynthesis showed overenhanced responses to derepression that were proportional to the degree of nitrogenase activity impairment, consistent with the existence of at least two negative-feedback regulatory mechanisms. The first such mechanism responded to the levels of fixed nitrogen, whereas the second mechanism appeared to respond to the levels of the mature NifDK component. Altogether, these findings provide a framework to engineer N2 fixation in nondiazotrophs.

Role of Azotobacter vinelandii FdxN in FeMo-co biosynthesis.

Biosynthesis of metal clusters for the nitrogenase component proteins NifH and NifDK involves electron donation events. Yet, electron donors specific to the biosynthetic pathways of the [4Fe-4S] cluster of NifH, or the P-cluster and the FeMo-co of NifDK, have not been identified. Here we show that an Azotobacter vinelandii mutant lacking fdxN was specifically impaired in FeMo-co biosynthesis. The ΔfdxN mutant produced 5-fold less NifB-co, an early FeMo-co biosynthetic intermediate, than wild type. As a consequence, it accumulated FeMo-co-deficient apo-NifDK and was impaired in NifDK activity. We conclude that FdxN plays a role in FeMo-co biosynthesis, presumably by donating electrons to support NifB-co synthesis by NifB. This is the first role in nitrogenase biosynthesis unequivocally assigned to any A. vinelandii ferredoxin.

BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis.

Plants interpret a decrease in the red to far-red light ratio (R:FR) as a sign of impending shading by neighboring vegetation. This triggers a set of developmental responses known as shade avoidance syndrome. One of these responses is reduced branching through suppression of axillary bud outgrowth. The Arabidopsis thaliana gene BRANCHED1 (BRC1), expressed in axillary buds, is required for branch suppression in response to shade. Unlike wild-type plants, brc1 mutants develop several branches after a shade treatment. BRC1 transcription is positively regulated 4 h after exposure to low R:FR. Consistently, BRC1 is negatively regulated by phytochrome B. Transcriptional profiling of wild-type and brc1 buds of plants treated with simulated shade has revealed groups of genes whose mRNA levels are dependent on BRC1, among them a set of upregulated abscisic acid response genes and two networks of cell cycle- and ribosome-related downregulated genes. The downregulated genes have promoters enriched in TEOSINTE BRANCHED1, CYCLOIDEA, and PCF (TCP) binding sites, suggesting that they could be transcriptionally regulated by TCP factors. Some of these genes respond to BRC1 in seedlings and buds, supporting their close relationship with BRC1 activity. This response may allow the rapid adaptation of plants to fluctuations in the ratio of R:FR light.

Resident bacteria on leaves enhance survival of immigrant cells of Salmonella enterica.

Although Salmonella enterica apparently has comparatively low epiphytic fitness on plants, external factors that would influence its ability to survive on plants after contamination would be of significance in the epidemiology of human diseases caused by this human pathogen. Viable population sizes of S. enterica applied to plants preinoculated with Pseudomonas syringae or either of two Erwinia herbicola strains was ≥10-fold higher than that on control plants that were not precolonized by such indigenous bacteria when assessed 24 to 72 h after the imposition of desiccation stress. The protective effect of P. fluorescens, which exhibited antibiosis toward S. enterica in vitro, was only ≈50% that conferred by other bacterial strains. Although S. enterica could produce small cellular aggregates after incubation on wet leaves for several days, and the cells in such aggregates were less susceptible to death upon acute dehydration than solitary cells (as determined by propidium iodide staining), most Salmonella cells were found as isolated cells when it was applied to leaves previously colonized by other bacterial species. The proportion of solitary cells of S. enterica coincident with aggregates of cells of preexisting epiphytic species that subsequently were judged as nonviable by viability staining on dry leaves was as much as 10-fold less than those that had landed on uncolonized portions of the leaf. Thus, survival of immigrant cells of S. enterica on plants appears to be strongly context dependent, and the presence of common epiphytic bacteria on plants can protect such immigrants from at least one key stress (i.e., desiccation) encountered on leaf surfaces.

Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds.

Shoot branching patterns depend on a key developmental decision: whether axillary buds grow out to give a branch or whether they remain dormant in the axils of leaves. This decision is controlled by endogenous and environmental stimuli mediated by hormonal signals. Although genes involved in the long-distance signaling of this process have been identified, the genes responding inside the buds to cause growth arrest remained unknown in Arabidopsis thaliana. Here, we describe an Arabidopsis gene encoding a TCP transcription factor closely related to teosinte branched1 (tb1) from maize (Zea mays), BRANCHED1 (BRC1), which represents a key point at which signals controlling branching are integrated within axillary buds. BRC1 is expressed in developing buds, where it arrests bud development. BRC1 downregulation leads to branch outgrowth. BRC1 responds to developmental and environmental stimuli controlling branching and mediates the response to these stimuli. Mutant and expression analyses suggest that BRC1 is downstream of the MORE AXILLARY GROWTH pathway and that it is required for auxin-induced apical dominance. Therefore, BRC1 acts inside the buds as an integrator of signals controlling bud outgrowth and translates them into a response of cell growth arrest. The conservation of BRC1/tb1 function among distantly related angiosperm species suggests that a single ancestral mechanism of branching control integration evolved before the radiation of flowering plants.

Role of TCP Gene BRANCHED1 in the Control of Shoot Branching in Arabidopsis.

Branching patterns are major determinants of plant architecture. They depend both on leaf phillotaxy (branch primordia are formed in the axils of leaves) and on the decision of buds to grow out to give a branch or to remain dormant. In Arabidopsis, several genes involved in the long-distance signalling of the control of branch outgrowth have been identified. However, the genes acting inside the buds to cause growth arrest remained unknown until now. In the February issue of Plant Cell we have described the function of BRANCHED1 (BRC1), an Arabidopsis gene coding for a plant-specific transcription factor of the TCP family that is expressed in the buds and prevents their development. Loss of BRC1 function leads to accelerated AM initiation, precocious progression of bud development and excess of shoot branching. BRC1 transcription is affected by endogenous and environmental signals controlling branching and we have shown that BRC1 function mediates the response to these stimuli. Therefore we have proposed that BRC1 function represents the point at which signals controlling branching are integrated within axillary buds.

The Erwinia chrysanthemi phoP-phoQ operon plays an important role in growth at low pH, virulence and bacterial survival in plant tissue.

We have studied the role of acidic pH as a barrier for the colonization of the plant apoplast by Erwinia chrysanthemi. A minitransposon containing a promoterless reporter gene, gus, was used for random mutagenesis of the bacterial genome. An acid-sensitive mutant, named BT119, was isolated and had the following differential features with respect to the wild-type strain: (i) inability to grow at pH

Erwinia chrysanthemi genes specifically induced during infection in chicory leaves.

Summary Twelve Erwinia chrysanthemi genes specifically up-regulated during infection in chicory leaves have been identified using GUS reporter gene fusions. According to sequence comparisons with GenBank databases, the possible functions of the identified genes included: virulence, adaptation to apoplast environment, chemotaxis, transposition, regulation, and metabolic functions. The level of gene up-regulation in planta was measured, and ranged from 1.39 to 47.11 times that found in liquid culture. This technique has been proven to be useful in the identification of bacterial up-regulated genes in plant-microbe interactions.