Life at the borderlands: microbiomes of interfaces critical to One Health.

Microbiomes are foundational components of the environment that provide essential services relating to food security, carbon sequestration, human health, and the overall well-being of ecosystems. Microbiota exert their effects primarily through complex interactions at interfaces with their plant, animal, and human hosts, as well as within the soil environment. This review aims to explore the ecological, evolutionary, and molecular processes governing the establishment and function of microbiome-host relationships, specifically at interfaces critical to One Health-a transdisciplinary framework that recognizes that the health outcomes of people, animals, plants, and the environment are tightly interconnected. Within the context of One Health, the core principles underpinning microbiome assembly will be discussed in detail, including biofilm formation, microbial recruitment strategies, mechanisms of microbial attachment, community succession, and the effect these processes have on host function and health. Finally, this review will catalogue recent advances in microbiology and microbial ecology methods that can be used to profile microbial interfaces, with particular attention to multi-omic, advanced imaging, and modelling approaches. These technologies are essential for delineating the general and specific principles governing microbiome assembly and functions, mapping microbial interconnectivity across varying spatial and temporal scales, and for the establishment of predictive frameworks that will guide the development of targeted microbiome-interventions to deliver One Health outcomes.

Streptomyces and their specialised metabolites for phytopathogen control - comparative in vitro and in planta metabolic approaches.

In the search for new crop protection microbial biocontrol agents, isolates from the genus Streptomyces are commonly found with promising attributes. Streptomyces are natural soil dwellers and have evolved as plant symbionts producing specialised metabolites with antibiotic and antifungal activities. Streptomyces biocontrol strains can effectively suppress plant pathogens via direct antimicrobial activity, but also induce plant resistance through indirect biosynthetic pathways. The investigation of factors stimulating the production and release of Streptomyces bioactive compounds is commonly conducted in vitro, between Streptomyces sp. and a plant pathogen. However, recent research is starting to shed light on the behaviour of these biocontrol agents in planta, where the biotic and abiotic conditions share little similarity to those of controlled laboratory conditions. With a focus on specialised metabolites, this review details (i) the various methods by which Streptomyces biocontrol agents employ specialised metabolites as an additional line of defence against plant pathogens, (ii) the signals shared in the tripartite system of plant, pathogen and biocontrol agent, and (iii) an outlook on new approaches to expedite the identification and ecological understanding of these metabolites under a crop protection lens.

Metatranscriptomics captures dynamic shifts in mycorrhizal coordination in boreal forests.

Carbon storage and cycling in boreal forests-the largest terrestrial carbon store-is moderated by complex interactions between trees and soil microorganisms. However, existing methods limit our ability to predict how changes in environmental conditions will alter these associations and the essential ecosystem services they provide. To address this, we developed a metatranscriptomic approach to analyze the impact of nutrient enrichment on Norway spruce fine roots and the community structure, function, and tree-microbe coordination of over 350 root-associated fungal species. In response to altered nutrient status, host trees redefined their relationship with the fungal community by reducing sugar efflux carriers and enhancing defense processes. This resulted in a profound restructuring of the fungal community and a collapse in functional coordination between the tree and the dominant Basidiomycete species, and an increase in functional coordination with versatile Ascomycete species. As such, there was a functional shift in community dominance from Basidiomycetes species, with important roles in enzymatically cycling recalcitrant carbon, to Ascomycete species that have melanized cell walls that are highly resistant to degradation. These changes were accompanied by prominent shifts in transcriptional coordination between over 60 predicted fungal effectors, with more than 5,000 Norway spruce transcripts, providing mechanistic insight into the complex molecular dialogue coordinating host trees and their fungal partners. The host-microbe dynamics captured by this study functionally inform how these complex and sensitive biological relationships may mediate the carbon storage potential of boreal soils under changing nutrient conditions.

Metabolic control of arginine and ornithine levels paces the progression of leaf senescence.

Leaf senescence can be induced by stress or aging, sometimes in a synergistic manner. It is generally acknowledged that the ability to withstand senescence-inducing conditions can provide plants with stress resilience. Although the signaling and transcriptional networks responsible for a delayed senescence phenotype, often referred to as a functional stay-green trait, have been actively investigated, very little is known about the subsequent metabolic adjustments conferring this aptitude to survival. First, using the individually darkened leaf (IDL) experimental setup, we compared IDLs of wild-type (WT) Arabidopsis (Arabidopsis thaliana) to several stay-green contexts, that is IDLs of two functional stay-green mutant lines, oresara1-2 (ore1-2) and an allele of phytochrome-interacting factor 5 (pif5), as well as to leaves from a WT plant entirely darkened (DP). We provide compelling evidence that arginine and ornithine, which accumulate in all stay-green contexts-likely due to the lack of induction of amino acids (AAs) transport-can delay the progression of senescence by fueling the Krebs cycle or the production of polyamines (PAs). Secondly, we show that the conversion of putrescine to spermidine (SPD) is controlled in an age-dependent manner. Thirdly, we demonstrate that SPD represses senescence via interference with ethylene signaling by stabilizing the ETHYLENE BINDING FACTOR1 and 2 (EBF1/2) complex. Taken together, our results identify arginine and ornithine as central metabolites influencing the stress- and age-dependent progression of leaf senescence. We propose that the regulatory loop between the pace of the AA export and the progression of leaf senescence provides the plant with a mechanism to fine-tune the induction of cell death in leaves, which, if triggered unnecessarily, can impede nutrient remobilization and thus plant growth and survival.

Gene atlas of iron-containing proteins in Arabidopsis thaliana.

Iron (Fe) is an essential element for the development and physiology of plants, owing to its presence in numerous proteins involved in central biological processes. Here, we established an exhaustive, manually curated inventory of genes encoding Fe-containing proteins in Arabidopsis thaliana, and summarized their subcellular localization, spatiotemporal expression and evolutionary age. We have currently identified 1068 genes encoding potential Fe-containing proteins, including 204 iron-sulfur (Fe-S) proteins, 446 haem proteins and 330 non-Fe-S/non-haem Fe proteins (updates of this atlas are available at https://conf.arabidopsis.org/display/COM/Atlas+of+Fe+containing+proteins). A fourth class, containing 88 genes for which iron binding is uncertain, is indexed as 'unclear'. The proteins are distributed in diverse subcellular compartments with strong differences per category. Interestingly, analysis of the gene age index showed that most genes were acquired early in plant evolutionary history and have progressively gained regulatory elements, to support the complex organ-specific and development-specific functions necessitated by the emergence of terrestrial plants. With this gene atlas, we provide a valuable and updateable tool for the research community that supports the characterization of the molecular actors and mechanisms important for Fe metabolism in plants. This will also help in selecting relevant targets for breeding or biotechnological approaches aiming at Fe biofortification in crops.

Another thread in the tangled knot of leaf senescence.

The emergence of yellow and red hued foliage in plants, which we commonly associate with vegetal decline or a foreshadowing of winter, signals the progression of a process known as leaf senescence. It is characterised by a series of carefully orchestrated degradation events, which liberate nutrients from senescing tissues and redistribute them to growing organs such as young leaves and reproductive structures. As the timing and execution of this process is essential to maximising the viability of succeeding plant generations and fruit production, it has tremendous implications for the agricultural industry. In this issue of Physiologia Plantarum, Zhang et al. (2020) describes the way in which a novel microRNA (miRNA) affects the timing of leaf senescence in tomato (Solanum lycopersicum) by modulating biosynthesis of the phytohormone cytokinin.

Centralization Within Sub-Experiments Enhances the Biological Relevance of Gene Co-expression Networks: A Plant Mitochondrial Case Study.

Gene co-expression networks (GCNs) can be prepared using a variety of mathematical approaches based on data sampled across diverse developmental processes, tissue types, pathologies, mutant backgrounds, and stress conditions. These networks are used to identify genes with similar expression dynamics but are prone to introducing false-positive and false-negative relationships, especially in the instance of large and heterogenous datasets. With the aim of optimizing the relevance of edges in GCNs and enhancing global biological insight, we propose a novel approach that involves a data-centering step performed simultaneously per gene and per sub-experiment, called centralization within sub-experiments (CSE). Using a gene set encoding the plant mitochondrial proteome as a case study, our results show that all CSE-based GCNs assessed had significantly more edges within the majority of the considered functional sub-networks, such as the mitochondrial electron transport chain and its complexes, than GCNs not using CSE; thus demonstrating that CSE-based GCNs are efficient at predicting canonical functions and associated pathways, here referred to as the core gene network. Furthermore, we show that correlation analyses using CSE-processed data can be used to fine-tune prediction of the function of uncharacterized genes; while its use in combination with analyses based on non-CSE data can augment conventional stress analyses with the innate connections underpinning the dynamic system being examined. Therefore, CSE is an effective alternative method to conventional batch correction approaches, particularly when dealing with large and heterogenous datasets. The method is easy to implement into a pre-existing GCN analysis pipeline and can provide enhanced biological relevance to conventional GCNs by allowing users to delineate a core gene network. AUTHOR SUMMARY: Gene co-expression networks (GCNs) are the product of a variety of mathematical approaches that identify causal relationships in gene expression dynamics but are prone to the misdiagnoses of false-positives and false-negatives, especially in the instance of large and heterogenous datasets. In light of the burgeoning output of next-generation sequencing projects performed on a variety of species, and developmental or clinical conditions; the statistical power and complexity of these networks will undoubtedly increase, while their biological relevance will be fiercely challenged. Here, we propose a novel approach to generate a "core" GCN with enhanced biological relevance. Our method involves a data-centering step that effectively removes all primary treatment/tissue effects, which is simple to employ and can be easily implemented into pre-existing GCN analysis pipelines. The gain in biological relevance resulting from the adoption of this approach was assessed using a plant mitochondrial case study.

Finding the metabolomic signature of drought resistance in poplar.

Efforts to decipher the processes underpinning biological systems now have a plethora of approaches from which to choose. Transcriptomics and proteomics provide a global snapshot of the abundance of gene products in a sample, from which researchers can learn a great deal about the inner machinations of a cell. However, when attempting to piece together a roadmap of an organism's metabolism, these strategies illuminate only a portion of the cellular landscape, and the evidence provided is often once- or even twice-removed from the actual players (the metabolites) involved. In this issue of Physiologia Plantarum, Jia et al. (2020) used metabolomic approaches to directly analyse the molecular soup of substrates and products contained in plant cells (known as the metabolome) to unravel the metabolic and physiological differences separating a drought-sensitive and a drought-tolerant species of the ecologically and economically important woody plant, poplar.

From the stench of death to an antidote for plant aluminium toxicity.

Putrescine is a member of a group of aliphatic compounds, known as polyamines, which are derived from the breakdown of amino acids in living (and dead) cells. Along with the grimly named cadaverine, putrescine was discovered in 1885 by the German physician Ludwig Brieger, who identified these polyamines as the primary constituent of the foul odours we associate with the rot and putrification of flesh. From this morbid origin, it is difficult to believe that putrescine has since been recognised as having numerous beneficial roles for living cells, ranging from increasing the tolerance of plants to biotic and abiotic stresses to possible roles in treating major mood disorders in humans. In this issue of Physiologia Plantarum, Zhu et al. (2019) describes how the addition of putrescine to the roots of rice (Oryza sativa) can alter the building blocks of the cell wall and, in doing so, alleviate aluminium toxicity.

Eucalypt seedlings are aided by phosphorus in the face of drought.

Drought is an increasingly common climatic event that can devastate ecosystems, as well as surrounding agricultural and forestry industries. Few places face this challenge more than Australia, where millennia of droughts linked to geography and climatic drivers, such as El Niño, have shaped the flora and fauna into forms predicated on resilience and economy. How an organism responds to these cyclic challenges is a combination of the inherent tolerance mechanisms encoded in their genome and outside influences, such as the effect of nutrients and symbiotic interactions. In this issue of Physiologia Plantarum, Tariq et al. (2019) describes how the presence of the element phosphorus can bolster the physiological and biochemical response of eucalypt seedlings to severe drought conditions.

The genetic program at the root of the biological stock exchange.

Beneath the gardens, farmlands and forest floors that surround us, a hidden world blooms in careful cooperation and intense competition. The mutualistic symbiosis of the thread-like hyphae of fungi and plant roots (collectively termed mycorrhizae from the Greek mýkes - meaning 'fungus', and rhiza - for 'root') is present in the vast majority of plant species. As with most intimate relationships, this symbiosis functions on a principle of 'give and take'. As an autotroph, the plant is able to synthesize all the sugars it requires through photosynthesis; however, its immobility hinders its capacity to forage for nutrients vital for its growth and survival. With an expansive network of hyphae, the heterotrophic fungus is able to locate and remobilize water and nutrients, such as phosphorus (P) and nitrogen (N), and barter them for precious sugars with the plant. An article in this issue of Physiologia Plantarum (Zhao et al. 2019) describes alterations in the genetic programming that takes place in the plant root upon the establishment of this fascinating relationship, which has profound implications for plant productivity and soil management methods.

Functional, Structural and Biochemical Features of Plant Serinyl-Glutathione Transferases.

Glutathione transferases (GSTs) belong to a ubiquitous multigenic family of enzymes involved in diverse biological processes including xenobiotic detoxification and secondary metabolism. A canonical GST is formed by two domains, the N-terminal one adopting a thioredoxin (TRX) fold and the C-terminal one an all-helical structure. The most recent genomic and phylogenetic analysis based on this domain organization allowed the classification of the GST family into 14 classes in terrestrial plants. These GSTs are further distinguished based on the presence of the ancestral cysteine (Cys-GSTs) present in TRX family proteins or on its substitution by a serine (Ser-GSTs). Cys-GSTs catalyze the reduction of dehydroascorbate and deglutathionylation reactions whereas Ser-GSTs catalyze glutathione conjugation reactions and eventually have peroxidase activity, both activities being important for stress tolerance or herbicide detoxification. Through non-catalytic, so-called ligandin properties, numerous plant GSTs also participate in the binding and transport of small heterocyclic ligands such as flavonoids including anthocyanins, and polyphenols. So far, this function has likely been underestimated compared to the other documented roles of GSTs. In this review, we compiled data concerning the known enzymatic and structural properties as well as the biochemical and physiological functions associated to plant GSTs having a conserved serine in their active site.

New tools for engineering tomorrow's forests.

It is difficult to overstate the role of wood in the story of humanity. In times that predate recorded history it provided shelter from the elements, light and warmth when burned, and a supple material with which early humans could craft their first tools. Today, it is still one of our chief building materials and an emerging industry is extending its applications through the development of novel biomaterials, such as cellulose fiber-derived nanocomposites. An article in this issue of Physiologia Plantarum (Johnsson et al. 2019) describes the influence the phytohormones auxin and gibberellic acid (GA) have on the process of wood formation, and reveals possible targets for optimizing cell wall properties in fiber cells.

Differences in pH influence the fate of CO2 in plants.

Soils represent the largest and most stable carbon pools on Earth, exceeding even the carbon aggregate found in the atmosphere and global phytomass. However, our understanding of how CO2 travels from the soil to the atmosphere, and the role of plants in this journey, is not fully understood. An article in this issue of Physiologia Plantarum (Shimono et al. 2019) sheds light on this process and unearths the dramatic effect pH can have on the fate of CO2 in plants.

Sobering challenges faced by the brewing industry in a warming world.

Barley (Hordeum vulgare), a vital crop to the food and beverage industry, is highly vulnerable to unstable conditions on the climatic horizon. An article in this special issue of Physiologia Plantarum by Mahalingam and Bregitzer (2019) describes the impact that individual and combined stresses linked to climate change could have on the agronomic source of one of our favourite libations, as well as offering achievable solutions that will be needed if crop yield and quality are to be maintained.

Darkened Leaves Use Different Metabolic Strategies for Senescence and Survival.

In plants, an individually darkened leaf initiates senescence much more rapidly than a leaf from a whole darkened plant. Combining transcriptomic and metabolomic approaches in Arabidopsis (Arabidopsis thaliana), we present an overview of the metabolic strategies that are employed in response to different darkening treatments. Under darkened plant conditions, the perception of carbon starvation drove a profound metabolic readjustment in which branched-chain amino acids and potentially monosaccharides released from cell wall loosening became important substrates for maintaining minimal ATP production. Concomitantly, the increased accumulation of amino acids with a high nitrogen-carbon ratio may provide a safety mechanism for the storage of metabolically derived cytotoxic ammonium and a pool of nitrogen for use upon returning to typical growth conditions. Conversely, in individually darkened leaf, the metabolic profiling that followed our 13C-enrichment assays revealed a temporal and differential exchange of metabolites, including sugars and amino acids, between the darkened leaf and the rest of the plant. This active transport could be the basis for a progressive metabolic shift in the substrates fueling mitochondrial activities, which are central to the catabolic reactions facilitating the retrieval of nutrients from the senescing leaf. We propose a model illustrating the specific metabolic strategies employed by leaves in response to these two darkening treatments, which support either rapid senescence or a strong capacity for survival.

Characterization of a novel ß-barrel protein (AtOM47) from the mitochondrial outer membrane of Arabidopsis thaliana.

In plant cells, mitochondria are major providers of energy and building blocks for growth and development as well as abiotic and biotic stress responses. They are encircled by two lipid membranes containing proteins that control mitochondrial function through the import of macromolecules and metabolites. Characterization of a novel ß-barrel protein, OUTER MEMBRANE PROTEIN 47 (OM47), unique to the green lineage and related to the voltage-dependent anion channel (VDAC) protein family, showed that OM47 can complement a VDAC mutant in yeast. Mutation of OM47 in Arabidopsis thaliana by T-DNA insertion had no effect on the import of proteins, such as the ß-barrel proteins translocase of the outer membrane 40 (TOM40) or sorting and assembly machinery 50 (SAM50), into mitochondria. Molecular and physiological analyses revealed a delay in chlorophyll breakdown, higher levels of starch, and a delay in the induction of senescence marker genes in the mutant lines. While there was a reduction of >90% in OM47 protein in mitochondria isolated from 3-week-old om47 mutants, in mitochondria isolated from 8-week-old plants OM47 levels were similar to that of the wild type. This recovery was achieved by an up-regulation of OM47 transcript abundance in the mutants. Combined, these results highlight a role in leaf senescence for this plant-specific ß-barrel protein, probably mediating the recovery and recycling of chloroplast breakdown products by transporting metabolic intermediates into and out of mitochondria.