A multi-organ maize metabolic model connects temperature stress with energy production and reducing power generation.

Climate change has adversely affected maize productivity. Thereby, a holistic understanding of metabolic crosstalk among its organs is important to address this issue. Thus, we reconstructed the first multi-organ maize metabolic model, iZMA6517, and contextualized it with heat and cold stress transcriptomics data using expression distributed reaction flux measurement (EXTREAM) algorithm. Furthermore, implementing metabolic bottleneck analysis on contextualized models revealed differences between these stresses. While both stresses had reducing power bottlenecks, heat stress had additional energy generation bottlenecks. We also performed thermodynamic driving force analysis, revealing thermodynamics-reducing power-energy generation axis dictating the nature of temperature stress responses. Thus, a temperature-tolerant maize ideotype can be engineered by leveraging the proposed thermodynamics-reducing power-energy generation axis. We experimentally inoculated maize root with a beneficial mycorrhizal fungus, Rhizophagus irregularis, and as a proof-of-concept demonstrated its efficacy in alleviating temperature stress. Overall, this study will guide the engineering effort of temperature stress-tolerant maize ideotypes.

Corrigendum: Genotypic Variation of Nitrogen Use Efficiency and Amino Acid Metabolism in Barley.

[This corrects the article DOI: 10.3389/fpls.2021.807798.].

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.

Genotypic Variation of Nitrogen Use Efficiency and Amino Acid Metabolism in Barley.

Owing to the large genetic diversity of barley and its resilience under harsh environments, this crop is of great value for agroecological transition and the need for reduction of nitrogen (N) fertilizers inputs. In the present work, we investigated the diversity of a North African barley genotype collection in terms of growth under limiting N (LN) or ample N (HN) supply and in terms of physiological traits including amino acid content in young seedlings. We identified a Moroccan variety, Laanaceur, accumulating five times more lysine in its leaves than the others under both N nutritional regimes. Physiological characterization of the barley collection showed the genetic diversity of barley adaptation strategies to LN and highlighted a genotype x environment interaction. In all genotypes, N limitation resulted in global biomass reduction, an increase in C concentration, and a higher resource allocation to the roots, indicating that this organ undergoes important adaptive metabolic activity. The most important diversity concerned leaf nitrogen use efficiency (LNUE), root nitrogen use efficiency (RNUE), root nitrogen uptake efficiency (RNUpE), and leaf nitrogen uptake efficiency (LNUpE). Using LNUE as a target trait reflecting barley capacity to deal with N limitation, this trait was positively correlated with plant nitrogen uptake efficiency (PNUpE) and RNUpE. Based on the LNUE trait, we determined three classes showing high, moderate, or low tolerance to N limitation. The transcriptomic approach showed that signaling, ionic transport, immunity, and stress response were the major functions affected by N supply. A candidate gene encoding the HvNRT2.10 transporter was commonly up-regulated under LN in the three barley genotypes investigated. Genes encoding key enzymes required for lysine biosynthesis in plants, dihydrodipicolinate synthase (DHPS) and the catabolic enzyme, the bifunctional Lys-ketoglutarate reductase/saccharopine dehydrogenase are up-regulated in Laanaceur and likely account for a hyperaccumulation of lysine in this genotype. Our work provides key physiological markers of North African barley response to low N availability in the early developmental stages.

Plant Defense Stimulator Mediated Defense Activation Is Affected by Nitrate Fertilization and Developmental Stage in Arabidopsis thaliana.

Plant defense stimulators, used in crop protection, are an attractive option to reduce the use of conventional crop protection products and optimize biocontrol strategies. These products are able to activate plant defenses and thus limit infection by pathogens. However, the effectiveness of these plant defense stimulators remains erratic and is potentially dependent on many agronomic and environmental parameters still unknown or poorly controlled. The developmental stage of the plant as well as its fertilization, and essentially nitrogen nutrition, play major roles in defense establishment in the presence of pathogens or plant defense stimulators. The major nitrogen source used by plants is nitrate. In this study, we investigated the impact of Arabidopsis thaliana plant developmental stage and nitrate nutrition on its capacity to mount immune reactions in response to two plant defense stimulators triggering two major defense pathways, the salicylic acid and the jasmonic acid pathways. We show that optimal nitrate nutrition is needed for effective defense activation and protection against the pathogenic bacteria Dickeya dadantii and Pseudomonas syringae pv. tomato. Using an npr1 defense signaling mutant, we showed that nitrate dependent protection against D. dadantii requires a functional NPR1 gene. Our results indicate that the efficacy of plant defense stimulators is strongly affected by nitrate nutrition and the developmental stage. The nitrate dependent efficacy of plant defense stimulators is not only due to a metabolic effect but also invloves NPR1 mediated defense signaling. Plant defense stimulators may have opposite effects on plant resistance to a pathogen. Together, our results indicate that agronomic use of plant defense stimulators must be optimized according to nitrate fertilization and developmental stage.

Beneficial soil-borne bacteria and fungi: a promising way to improve plant nitrogen acquisition.

Nitrogen (N) is an essential element for plant productivity, thus, it is abundantly applied to the soil in the form of organic or chemical fertilizers that have negative impacts on the environment. Exploiting the potential of beneficial microbes and identifying crop genotypes that can capitalize on symbiotic associations may be possible ways to significantly reduce the use of N fertilizers. The best-known example of symbiotic association that can reduce the use of N fertilizers is the N2-fixing rhizobial bacteria and legumes. Bacterial taxa other than rhizobial species can develop associative symbiotic interactions with plants and also fix N. These include bacteria of the genera Azospirillum, Azotobacter, and Bacillus, some of which are commercialized as bio-inoculants. Arbuscular mycorrhizal fungi are other microorganisms that can develop symbiotic associations with most terrestrial plants, favoring access to nutrients in a larger soil volume through their extraradical mycelium. Using combinations of different beneficial microbial species is a promising strategy to boost plant N acquisition and foster a synergistic beneficial effect between symbiotic microorganisms. Complex biological mechanisms including molecular, metabolic, and physiological processes dictate the establishment and efficiency of such multipartite symbiotic associations. In this review, we present an overview of the current knowledge and future prospects regarding plant N nutrition improvement through the use of beneficial bacteria and fungi associated with plants, individually or in combination.

A secreted metal-binding protein protects necrotrophic phytopathogens from reactive oxygen species.

Few secreted proteins involved in plant infection common to necrotrophic bacteria, fungi and oomycetes have been identified except for plant cell wall-degrading enzymes. Here we study a family of iron-binding proteins that is present in Gram-negative and Gram-positive bacteria, fungi, oomycetes and some animals. Homolog proteins in the phytopathogenic bacterium Dickeya dadantii (IbpS) and the fungal necrotroph Botrytis cinerea (BcIbp) are involved in plant infection. IbpS is secreted, can bind iron and copper, and protects the bacteria against H2O2-induced death. Its 1.7 Å crystal structure reveals a classical Venus Fly trap fold that forms dimers in solution and in the crystal. We propose that secreted Ibp proteins binds exogenous metals and thus limit intracellular metal accumulation and ROS formation in the microorganisms.

Quantitative Methods to Assess Differential Susceptibility of Arabidopsis thaliana Natural Accessions to Dickeya dadantii.

Among the most devastating bacterial diseases of plants, soft rot provoked by Dickeya spp. cause crop yield losses on a large range of species with potato being the most economically important. The use of antibiotics being prohibited in most countries in the field, identifying tolerance genes is expected to be one of the most effective alternate disease control approaches. A prerequisite for the identification of tolerance genes is to develop robust disease quantification methods and to identify tolerant plant genotypes. In this work, we investigate the feasibility of the exploitation of Arabidopsis thaliana natural variation to find tolerant genotypes and to develop robust quantification methods. We compared different quantification methods that score either symptom development or bacterial populations in planta. An easy to set up and reliable bacterial quantification method based on qPCR amplification of bacterial DNA was validated. This study demonstrates that it is possible to conduct a robust phenotyping of soft rot disease, and that Arabidopsis natural accessions are a relevant source of tolerance genes.

Immunity to plant pathogens and iron homeostasis.

Iron is essential for metabolic processes in most living organisms. Pathogens and their hosts often compete for the acquisition of this nutrient. However, iron can catalyze the formation of deleterious reactive oxygen species. Hosts may use iron to increase local oxidative stress in defense responses against pathogens. Due to this duality, iron plays a complex role in plant-pathogen interactions. Plant defenses against pathogens and plant response to iron deficiency share several features, such as secretion of phenolic compounds, and use common hormone signaling pathways. Moreover, fine tuning of iron localization during infection involves genes coding iron transport and iron storage proteins, which have been shown to contribute to immunity. The influence of the plant iron status on the outcome of a given pathogen attack is strongly dependent on the nature of the pathogen infection strategy and on the host species. Microbial siderophores emerged as important factors as they have the ability to trigger plant defense responses. Depending on the plant species, siderophore perception can be mediated by their strong iron scavenging capacity or possibly via specific recognition as pathogen associated molecular patterns. This review highlights that iron has a key role in several plant-pathogen interactions by modulating immunity.

New insights into the role of siderophores as triggers of plant immunity: what can we learn from animals?

Microorganisms use siderophores to obtain iron from the environment. In pathogenic interactions, siderophores are involved in iron acquisition from the host and are sometimes necessary for the expression of full virulence. This review summarizes the main data describing the role of these iron scavengers in animal and plant defence systems. To protect themselves against iron theft, mammalian hosts have developed a hypoferremia strategy that includes siderophore-binding molecules called siderocalins. In addition to microbial ferri-siderophore sequestration, siderocalins are involved in triggering immunity. In plants, no similar mechanisms have been described and many fewer data are available, although recent advances have shed light on the role of siderophores in plant-pathogen interactions. Siderophores can trigger immunity in plants in several contexts. The most frequently described situation involving siderophores is induced systemic resistance (ISR) triggered by plant-growth-promoting rhizobacteria. Although ISR responses have been observed after treating roots with certain siderophores, the underlying mechanisms are poorly understood. Immunity can also be triggered by siderophores in leaves. Siderophore perception in plants appears to be different from the well-known perception mechanisms of other microbial compounds, known as microbe-associated molecular patterns. Scavenging iron per se appears to be a novel mechanism of immunity activation, involving complex disturbance of metal homeostasis. Receptor-specific recognition of siderophores has been described in animals, but not in plants. The review closes with an overview of the possible mechanisms of defence activation, via iron scavenging by siderophores or specific siderophore recognition by the plant host.