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Sanchez-Rodriguez, C.

Publications and source records attributed to Sanchez-Rodriguez, C..

10 recordsLinked to original sources

The Receptor Kinase MEE39/ATHE Mediates Cell Wall Integrity Surveillance During Root Vascular Pathogen Infection

Plant cell wall (CW) integrity signaling enables early detection of microbial invasion, yet the receptors involved and their spatial and temporal dynamics during infection remain largely unknown. We identify ATHENA (ATHE)/MEE39, a previously uncharacterized malectin-like leucin-rich repeat receptor kinase (Mal-LRR-RK) that contributes to defense against the root vascular pathogen Fusarium oxysporum (Fo), particularly in outer root layers where colonization begins. ATHE abundance, localization, and endocytic trafficking are rapidly remodeled during infection, and loss of ATHE compromises basal immunity and early pathogen-induced transcriptional reprogramming. ATHE responds to altered cellulose synthesis, cellulose-derived oligosaccharides, mechanically induced CW perturbations, and the fungal secreted peptide Fo-RALF. In most of these contexts, ATHE acts together with the LRR-RK MIK2, forming a pathogen-strengthened RK complex that fine-tunes root responses to Fo. This represents the first example of a receptor complex visualized subcellularly in vivo during a plant-microbe interaction. Although Brassicaceae-specific, heterologous expression of ATHE enhanced tomato resistance to Fo, highlighting its functional relevance across plant lineages and its potential use for crop engineering. Our work reveals a previously unrecognized strategy by which plants decode microbial threats through dynamic CW-integrity surveillance.

plant biology↗

Vascular fungi alter the apoplastic purinergic signaling in plants by deregulating the homeostasis of extracellular ATP and its metabolite adenosine

Purinergic signaling activated by extracellular nucleotides and their derivative nucleosides trigger sophisticated signaling networks. The outcome of these pathways determine the capacity of the organism to survive under challenging conditions. Both extracellular ATP (eATP) and Adenosine (eAdo) act as secondary messengers in mammals, essential for immunosuppressive responses. Despite the clear role of eATP as a plant damage-associated molecular pattern, the function of its nucleoside, eAdo, and of the eAdo/eATP balance in plant stress response remain to be fully elucidated. This is particularly relevant in the context of plant/microbe interaction, where the intruder manipulates the extracellular matrix. Here, we identify Ado as a main elicitor secreted by the vascular fungus Fusarium oxysporum. We show that eAdo modulates the plants susceptibility to fungal colonization by altering eATP-mediated physiological immune responses, such as apoplastic pH and calcium homeostasis. Our work indicates that plant pathogens actively imbalance the eAdo/eATP levels as a virulence mechanism. One Sentence SummaryThe apoplastic Adenosine/ATP balance is a messenger for plant defense and can be manipulated by the fungal pathogen F. oxysporum.

plant biology↗

Peripheral membrane proteins modulate stress tolerance by safeguarding cellulose synthases

Controlled primary cell wall remodeling adapts plant growth under stressful conditions, but how these changes are conveyed to adjust cellulose synthesis is unknown. Here, we identify the Tetratricopeptide Thioredoxin-Like (TTL) proteins as new members of the cellulose synthase complex (CSC) and describe their unique and hitherto unknown dynamic association with the CSC under cellulose-deficient conditions. We find that TTLs are essential for maintaining cellulose synthesis under salinity stress, establishing a stress-resilient cortical microtubule array, and stabilizing CSCs at the plasma membrane. To fulfill these functions, TTLs interact with Cellulose Synthase1 (CESA1) and engage with cortical microtubules to promote their polymerization. We propose that TTLs function as bridges connecting stress perception with dynamic regulation of cellulose biosynthesis at the plasma membrane. One Sentence SummaryTTLs are peripheral membrane proteins that maintain the integrity of the cellulose synthase complex upon adverse conditions.

plant biology↗

A phospho-switch provided by LRR receptor-like kinase, ALK1/QSK1/KIN7, prioritizes ABCG36/PEN3/PDR8 transport toward defense

Based on its proposed substrate preferences, the ABC transporter, ABCG36/PDR8/PEN3, from the model plant Arabidopsis stands at the cross-road between growth and defence. Recently, ABCG36 was shown to export a few indolic compounds, including the auxin precursor, indole-3-butyric acid (IBA), and to be implicated in the export of the major phytoalexin of Arabidopsis, camalexin, although clear-cut proof of camalexin transport activity is still lacking. Here we provide strong evidence that ABCG36 catalyses the direct, ATP-dependent export of camalexin over the plasma membrane, however, most likely in functional interplay with non-camalexin transporting ABCG isoforms. We identify the leucin-rich repeat receptor-like kinase, Auxin-induced LRR Kinase1 (ALK1/KIN7/QSK1), as a functional kinase to physically interact with and phosphorylate ABCG36. ABCG36 phosphorylation by ALK1 represses unilaterally IBA but not camalexin export leading to a prioritization of ABCG transport toward defense. As a consequence, phospho-dead mutants of ABCG36, like alk1 and abcg36 alleles, are hypersensitive toward infection with the root pathogen, F. oxysporum, caused by elevated fungal progression. Our findings indicate a novel, direct regulatory circuit between a receptor kinase and an ABC transporter determining transporter substrate specificity. It appears that growth and defense balance decisions in plants are performed on the transporter level by means of a reversible phospho-switch.

plant biology↗

Impairment of the cellulose degradation machinery enhances fungal virulence but limits reproductive fitness

Fungal endophytes grow in the apoplastic space, in constant contact with the plant cell wall (CW) that hinders microbe progression, while representing a source of nutrients. Although numerous fungal CW modifying proteins have been identified, their role during host colonization remains underexplored. Here we show that the root-infecting plant pathogen Fusarium oxysporum (Fo) does not require its complete arsenal of cellulases to infect the host plant. Quite the opposite, Fo mutants impaired in cellulose degradation become hypervirulent by enhancing the secretion of virulence factors. On the other hand, the reduction on cellulase activity had a severe negative effect on saprophytic growth and microconidia production during the final stages of the Fo infection cycle. These findings enhance our understanding on the function of plant CW degradation on the outcome of host-microbe interactions and reveal an unexpected role of cellulose degradation in a pathogens evolutionary success. TeaserUnexpectedly, fungi compromised in their capacity to degrade plant cellulose are hypervirulent but impaired in sporulation.

microbiology↗

A Calcium/Palmitoylation Switch Interfaces the Signaling Networks of Stress Response and Transition to Flowering

The precise timing of flowering in adverse environments is critical for plants to secure reproductive success. We report a novel mechanism controlling the time of flowering by which the palmitoylation-dependent nuclear import of protein SOS3/CBL4, a Ca2+-signaling intermediary in the plant response to salinity, results in the selective stabilization of the flowering time regulator GIGANTEA inside the nucleus under salt stress, while degradation of GIGANTEA in the cytosol releases the protein kinase SOS2 to achieve salt tolerance. S-acylation of SOS3 was critical for its nuclear localization and the promotion of flowering, but dispensable for salt tolerance. SOS3 interacted with the photoperiodic flowering components GIGANTEA and FKF1 on the CONSTANS gene promoter to sustain the transcription of CO and FT under salinity. Thus, SOS3 acts as a Ca2+- and palmitoylation-dependent molecular switch that fine-tunes flowering in a saline environment through the shared spatial separation and selective stabilization of GIGANTEA. The SOS3 protein connects two signaling networks to co-regulate stress adaptation and time of flowering. Short summaryS-acylation promoted the nuclear import of SOS3/CBL4 for the selective stabilization of the photoperiodic floral regulator GIGANTEA to fine-tune flowering time in a saline environment. Spatial separation of SOS3 acts as a molecular switch co-regulating stress adaptation and time of flowering.

plant biology↗

A chromosome-scale genome assembly for the Fusarium oxysporum strain Fo5176 to establish a model Arabidopsis-fungal pathosystem

Plant pathogens cause widespread yield losses in agriculture. Understanding the drivers of plant-pathogen interactions requires decoding the molecular dialog leading to either resistance or disease. However, progress in deciphering pathogenicity genes has been severely hampered by suitable model systems and incomplete fungal genome assemblies. Here, we report a significant improvement of the assembly and annotation of the genome of the Fusarium oxysporum (Fo) strain Fo5176. Fo comprises a large number of serious plant pathogens on dozens of plant species with largely unresolved pathogenicity factors. The strain Fo5176 infects Arabidopsis thaliana and, hence, constitutes a highly promising model system. We use high-coverage Pacific Biosciences Sequel long-read and Hi-C sequencing data to assemble the genome into 19 chromosomes and a total genome size of 67.98 Mb. The genome has a N50 of 4 Mb and a 99.1% complete BUSCO score. Phylogenomic analyses based on single-copy orthologs clearly place the Fo5176 strain in the Fo f sp. conglutinans clade as expected. We generated RNAseq data from culture medium and plant infections to train gene predictions and identified [~]18,000 genes including ten effector genes known from other Fo clades. We show that Fo5176 is able to infect cabbage and Brussel sprouts of the Brassica oleracea, expanding the usefulness of the Fo5176 model pathosystem. Finally, we performed large-scale comparative genomics analyses comparing the Fo5176 to 103 additional Fo genomes to define core and accessory genomic regions. In conjunction with the molecular tool sets available for A. thaliana, the Fo5176 genome and annotation provides a crucial step towards the establishment of a highly promising pathosystem.

genomics↗

Arabidopsis phytochelatin synthase 1, but not phytochelatin synthesis, functions in extracellular defense against multiple fungal pathogens

Phytochelatin synthase (PCS) is a key component of heavy metal detoxification in plants. PCS catalyzes both the synthesis of the peptide phytochelatin from glutathione as well as the degradation of glutathione conjugates via peptidase activity. Here, we describe a hitherto uncharacterized role for PCS in disease resistance against plant pathogenic fungi. The pen4 mutant, which is allelic to cadmium insensitive 1 (cad1/pcs1) mutants, was recovered from a screen for Arabidopsis mutants with reduced resistance to the non-adapted barley fungal pathogen, Blumeria graminis f. sp. hordei. PCS1, which is found in the cytoplasm of cells of healthy plants, translocates upon pathogen attack and colocalizes with the PEN2 myrosinase on the surface of immobilized mitochondria. pcs1 and pen2 mutant plants exhibit a similar metabolic defect in the accumulation of pathogen-inducible indole glucosinolate-derived compounds, suggesting that PEN2 and PCS1 act in the same metabolic pathway. The function of PCS1 in this pathway is independent of phytochelatin synthesis and deglycination of glutathione conjugates, as catalytic-site mutants of PCS1 are still functional in indole glucosinolate metabolism. In uncovering a previously unknown function for PCS1, we reveal this enzyme to be a moonlighting protein important for plant responses to both biotic and abiotic stresses.

plant biology↗

Pathogen-induced pH changes regulate the growth-defense balance of plants

Environmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall-related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplastic acidification by phosphorylation-based proton pump activation was followed by an acidification of the cortical side of the plasma membrane in response to the fungus Fusarium oxysporum. The proton chemical gradient modulation immediately reduced cellulose synthesis and cell growth and, furthermore, had a direct influence on the pathogenicity of the fungus. All these effects were dependent on the COMPANION OF CELLULOSE SYNTHASE proteins that are thus at the nexus of plant growth and defense. Hence, our discoveries show a remarkable connection between plant biomass production, immunity, and pH control, and advance our ability to investigate the plant growth-defense balance.

plant biology↗

A molecular mechanism for salt stress-induced microtubule array formation in Arabidopsis

Microtubules are filamentous structures necessary for cell division, motility and morphology, with dynamics critically regulated by microtubule-associated proteins (MAPs). We outline the molecular mechanism by which the MAP, COMPANION OF CELLULOSE SYNTHASE1 (CC1), controls microtubule bundling and dynamics to sustain plant growth under salt stress. CC1 contains an intrinsically disordered N-terminus that links microtubules at evenly distributed distances through four conserved hydrophobic regions. NMR analyses revealed that two neighboring residues in the first hydrophobic binding motif are crucial for the microtubule interaction, which we confirmed through live cell analyses. The microtubule-binding mechanism of CC1 is remarkably similar to that of the prominent neuropathology-related protein Tau, indicating evolutionary convergence of MAP functions across animal and plant cells.

cell biology↗