Aug 2026· Proceedings of the National Academy of Sciences of the United States of America· Vol 123 34, pp.
e2536998123
· 0 citations· 41 references
Medicine
TL;DR
It is shown that the Arabidopsis NatA N-terminal-acetyltransferase complex acts as a leaf-intrinsic brake on these root-to-leaf systemic responses to ISR priming, enabling plants to sustain lifelong ISR priming without growth penalty.
Abstract
Root-associated beneficial microbes prime host plants for induced systemic resistance (ISR) in leaves. Although continuous immune activation triggered by root endophytic fungi would impair leaf growth, how host plants avoid autoimmunity during endophytic fungi-mediated ISR priming is unknown. Here, we show that the Arabidopsis NatA N-terminal-acetyltransferase complex acts as a leaf-intrinsic brake on these root-to-leaf systemic responses. Impairment of the NatA subunit SUF1 (also named HYPK) or NAA15 unleashed chronic N-hydroxy-pipecolic-acid (NHP)/salicylic-acid (SA) signaling activation, converting beneficial ISR priming into growth-inhibitory leaf senescence. Transcriptome and quantitative proteomic analysis revealed the selective activation of defense and SA signaling pathways in the leaves of NatA mutants. Crossing suf1 or naa15 with fmo1 and eds5 abolished autoimmunity, confirming that the phenotype requires FMO1-dependent NHP and downstream SA synthesis and signaling activation. Thus, by destabilizing defense proteins, NatA enables plants to sustain lifelong ISR priming without growth penalty, guiding breeders to consider ISR control traits.
Benzoxazinoids are indole-derived specialized metabolites released into the soil through root exudates. Initially studied for their allelopathic and toxic effects, they are now recognized as broad regulators of plant–organism interactions, including microbiome-mediated pathogen resistance. However, whether benzoxazinoid-containing root exudates can directly influence disease susceptibility in neighboring plants remains unclear. Using an agriculturally relevant rice–maize co-culture system, we show that benzoxazinoids naturally exuded by maize roots are taken up by rice roots and are associated with reduced rice blast disease in leaves. This protection occurs without detectable benzoxazinoid accumulation in rice leaves, constitutive immune activation or decreased plant height. Instead, benzoxazinoid uptake by rice roots is associated with chromatin hyperacetylation, increased expression of key phenylpropanoid biosynthetic genes and broad metabolic reprogramming. These responses extend systemically to leaves, where rice establishes a defense-related chemical state distinct from the systemic acquired resistance previously observed in benzoxazinoid-dependent, microbiome-mediated plant–soil feedbacks. Our findings support a model in which specialized metabolites exuded by one crop species are acquired by a neighbouring species and trigger chromatin-associated metabolic reprogramming linked to systemic chemical defence. This study provides a molecular framework connecting plant–plant chemical interactions, root exudation, chromatin regulation and disease susceptibility.
Laura Mathieu, Rémi Pélissier, Inès Bénameur et al.· bioRxiv· 0 citations
Induced systemic resistance (ISR) is activated in leaves upon root colonization by beneficial microbes, yet the signals linking rhizosphere perception to shoot immunity remain unknown. In the Arabidopsis thaliana-Pseudomonas simiae WCS417 model interaction, the root-specific transcription factor MYB72 and its target gene BGLU42 regulate ISR and the production, activation, and root secretion of coumarins, specialized metabolites involved in plant iron (Fe) acquisition and rhizosphere microbiome assembly. Overexpression of BGLU42 confers constitutive ISR in leaves, suggesting a link between coumarin metabolism and systemic immunity. Here, two-photon multispectral imaging and targeted metabolite profiling revealed that, under Fe-sufficient conditions, WCS417 induces a distinct spatial pattern of F6’H1-dependent coumarin accumulation along the root system. These WCS417-induced coumarin signatures differed from those observed under Fe deficiency, indicating activation of a microbiota-specific coumarin metabolic program. Increased coumarin accumulation in roots was followed by a rise in coumarin levels in shoots. Time-resolved transcriptome profiling supported this metabolic reprogramming, showing rapid activation of Fe acquisition and coumarin biosynthesis genes in roots, including F6’H1, MYB72, and BGLU42, followed by delayed but similar transcriptional responses in shoots. Functional analyses demonstrated that coumarin biosynthesis is required for WCS417-ISR: the f6’h1 mutant failed to mount systemic resistance, whereas F6’H1 overexpression conferred constitutive resistance to bacterial and fungal pathogens. In addition, WCS417-mediated coumarin accumulation systemically modulated flg22-triggered reactive oxygen species production in leaves in an F6’H1-dependent manner. Together, our results identify coumarins as key mediators linking rhizobacterial perception in roots to systemic immune signaling and resistance in leaves.
S. Hsu, Max J. J. Stassen, Kévin Robe et al.· bioRxiv· 0 citations
The microbiota is being increasingly recognized for its ability to regulate host physiology through the production of small bioactive molecules. However, how host-derived nutrients are metabolically transformed by root-associated microbes to influence plant immunity remains poorly understood. Here, we show that vitamin B3 (VB3; niacin) secreted by plant roots shapes the assembly of a functionally specialized root microbiota, which, in turn, metabolizes VB3 into an immune-active signal that enhances plant disease resistance. VB3 secretion selectively increases the abundance of root-associated bacteria harboring a conserved nic biosynthetic gene cluster (BGC), which enables the conversion of VB3 into 6-hydroxynicotinate (6-OHNA), a previously uncharacterized microbial metabolite involved in plant-microbe interactions. Microbially produced 6-OHNA is transported from roots to shoots, where it primes systemic immune responses in a salicylic acid–dependent manner. Disruption of the microbial nic BGC abolishes immune priming, whereas increased VB3 exudation from plant roots enhances disease resistance. Together, these findings reveal a metabolically mediated dialog between plant hosts and their microbiota that links host nutrient secretion to microbial functional specialization and the activation of systemic plant immunity.
It is shown that salicylic acid (SA) signaling plays a critical role in potato NHR against the oomycete pathogen Phytophthora capsici, and new insights are provided into the regulatory framework underlying potato-oomycete interactions.
Microbial volatile organic compounds (mVOCs) enable plants to perceive microbial activity prior to physical contact, yet the contribution of individual bacterial volatiles to immune signalling and disease resistance remains incompletely understood. Here, headspace GC-MS analysis demonstrates that the hemibiotrophic pathogen Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) emits a distinct volatile blend containing the bacterium-specific compounds 2-methylbutanoic acid (2-MBA) and 3-methylbutanoic acid (3-MBA), with 2MBA as a dominant component. Exposure of Arabidopsis thaliana to the complete Pst DC3000 mVOC blend induced extensive transcriptional reprogramming activation of pattern-recognition receptor-associated genes, MAP kinase signalling components, WRKY transcription factors, camalexin biosynthetic genes and early defense responses. The latter included cytosolic Ca2+ ([Ca2+]cyt) elevation, K+ channel activation, hydrogen peroxide accumulation, and nitric oxide production, which culminated in camalexin accumulation in wild-type shoots and roots. In contrast, these early signaling and physiological responses were strongly attenuated in the camalexin-deficient pad3 mutant. Phenotypic priming assays confirmed that mVOC pre-exposure enhances resistance against subsequent Pst DC3000 infection largely through this PAD3-dependent mechanism, while exogenous camalexin administration proved independently sufficient to restore robust pathogen protection, indicating that PAD3-dependent camalexin biosynthesis contributes substantially, but not exclusively, to volatile-induced resistance. Application of synthetic 2-MBA, and to a lesser extent 3-MBA, was sufficient to recreate rapid [Ca2+]cyt elevation and ROS production. Quantitative expression profiling revealed that synthetic 2-MBA modulates gene expression in an organ-specific manner, upregulating shoot volatile perception and salicylic acid pathways, inducing root calcium and immune responses, and systemically activating auxin signaling and tryptophan biosynthetic genes. Together, these findings identify 2-MBA as a primary active component of the Pst DC3000 volatile blend and indicate that full volatile-induced defence depends on PAD3-dependent camalexin accumulation together with integration of multiple volatile signals. Our results reveal how plants integrate distinct bacterial volatiles to trigger early signaling and coordinate localized and systemic camalexin-dependent immunity.
I. Paponov, C. N. Kanchiswamy, Simone Bossi et al.· Plant, Cell and Environment· 0 citations
Salinity is a major constraint to crop productivity. Beneficial plant–fungus interactions represent a promising strategy to enhance stress resilience. Here, we investigated fungal endophytes isolated from the roots of Oryza sativa cultivated in saline-prone marshlands of the Guadalquivir River, Spain. From a collection of 38 isolates, five salt-tolerant strains exhibiting plant growth-promoting activity were identified, including a previously uncharacterized Reticulascus sp. strain S5. Co-cultivation assays with the non-native host plant Arabidopsis thaliana demonstrated that S5 increased the root and shoot biomass under salt stress. To elucidate the underlying molecular mechanisms, a comprehensive RNA-Seq analysis of the roots and shoots under control and saline conditions was performed. Fungal colonization induced pronounced transcriptomic changes, particularly in the shoots, including rewiring of the auxin- and abscisic acid-related pathways and the induction of genes associated with cell wall remodeling. Concurrently, defense-related processes, including glucosinolate biosynthesis and ethylene signaling, were broadly repressed, suggesting attenuated stress perception in colonized plants. In the roots, S5 inoculation suppressed the expression of genes involved in root hair development and cell wall organization, indicating a fungus-driven reconfiguration of root development. Moreover, comparative analysis with Fusarium sp. K-23, a fungus that has previously been demonstrated to promote plant growth under salinity stress, revealed distinct root-associated mechanisms but convergence on a shared regulatory module in shoots involving ABA-responsive transcription factors and osmotic stress regulators. Collectively, our findings demonstrate that Reticulascus sp. S5 enhances plant salt stress tolerance through the coordinated transcriptional reprogramming of growth, hormone signaling, and stress responses, highlighting a possible potential of habitat-adapted endophytes for sustainable crop improvement.
Silvia Martínez-Fenoll, Adrián González Ortega-Villaizán, E. Rodríguez-Dobreva et al.· International Journal of Mol...· 0 citations
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