Sara Sopeña‐Torres

Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora"

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Lucía Jordá

Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria

Antonio Molina

Universidad de Santiago de Chile

Antonio Muñoz‐Barrios

Universidad Politécnica de Madrid

Viviana Escudero

Centre for Plant Biotechnology and Genomics

Hugo Mélida

Universidad de León

Antonio de Vicente

Universidad de Málaga

Diego Romero

Universidad de Málaga

Luis Díaz‐Martínez

Universidad de Málaga

Sanjay Swami

Universidad Politécnica de Madrid

Gemma López

Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria

Cooperative Institutions

Centre for Plant Biotechnology and Genomics

Universidad Politécnica de Madrid

Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria

Consejo Superior de Investigaciones Científicas

Universidad de Málaga

Max Planck Institute for Plant Breeding Research

Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora"

Universidad Complutense de Madrid

University of California, San Diego

Max Planck Society

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Sporulation is dispensable for the vegetable‐associated life cycle of the human pathogen Bacillus cereus

Microbial Biotechnology (2021)

María Luisa Antequera-Gómez Luis Díaz‐Martínez Juan Antonio Guadix Ana María Sánchez‐Tévar Sara Sopeña‐Torres

Bacillus cereus is a common food-borne pathogen that is responsible for important outbreaks of food poisoning in humans. Diseases caused by B. cereus usually exhibit two major symptoms, emetic or diarrheic, depending on the toxins produced. It is assumed that after the ingestion of contaminated vegetables or processed food, spores of enterotoxigenic B. cereus reach the intestine, where they germinate and produce the enterotoxins that are responsible for food poisoning. In our study, we observed that sporulation is required for the survival of B. cereus in leaves but is dispensable in ready-to-eat vegetables, such as endives. We demonstrate that vegetative cells of B. cereus that are originally impaired in sporulation but not biofilm formation are able to reach the intestine and cause severe disorders in a murine model. Furthermore, our findings emphasise that the number of food poisoning cases associated with B. cereus is underestimated and suggest the need to revise the detection protocols, which are based primarily on spores and toxins.

Cereus

Food poisoning

10.1111/1751-7915.13816

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Citations (17)

ERECTA and BAK1 Receptor Like Kinases Interact to Regulate Immune Responses in Arabidopsis

Frontiers in Plant Science (2016)

Lucía Jordá Sara Sopeña‐Torres Viviana Escudero Beatriz Núñez-Corcuera Magdalena Delgado-Cerezo

ERECTA (ER) receptor-like kinase (RLK) regulates Arabidopsis thaliana organ growth, and inflorescence and stomatal development by interacting with the ERECTA-family genes (ERf) paralogs, ER-like 1 (ERL1) and ERL2, and the receptor-like protein (RLP) TOO MANY MOUTHS (TMM). ER also controls immune responses and resistance to pathogens such as the bacterium Pseudomonas syringae pv. tomato DC3000 (Pto) and the necrotrophic fungus Plectosphaerella cucumerina BMM (PcBMM). We found that er null-mutant plants overexpressing an ER dominant-negative version lacking the cytoplasmic kinase domain (ERΔK) showed an enhanced susceptibility to PcBMM, suggesting that ERΔK associates and forms inactive complexes with additional RLKs/RLPs required for PcBMM resistance. Genetic analyses demonstrated that ER acts in a combinatorial specific manner with ERL1, ERL2, and TMM to control PcBMM resistance. Moreover, BAK1 (BRASSINOSTEROID INSENSITIVE 1-associated kinase 1) RLK, which together with ERf/TMM regulates stomatal patterning and resistance to Pto, was also found to have an unequal contribution with ER in regulating immune responses and resistance to PcBMM. Co-immunoprecipitation experiments in Nicotiana benthamiana further demonstrated BAK1-ER protein interaction. The secreted epidermal pattern factor peptides (EPF1 and EPF2), which are perceived by ERf members to specify stomatal patterning, do not seem to regulate ER-mediated immunity to PcBMM, since their inducible overexpression in A. thaliana did not impact on PcBMM resistance. Our results indicate that the multiproteic receptorsome formed by ERf, TMM and BAK1 modulates A. thaliana resistance to PcBMM, and suggest that the cues underlying ERf/TMM/BAK1-mediated immune responses are distinct from those regulating stomatal pattering.

Pseudomonas syringae

Plant Immunity

Protein kinase domain

Immune receptor

10.3389/fpls.2016.00897

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Citations (76)

Chemical interplay and complementary adaptative strategies toggle bacterial antagonism and co-existence

Cell Reports (2021)

Carlos Molina‐Santiago David Vela‐Corcía Daniel Petras Luis Díaz‐Martínez Alicia Isabel Pérez‐Lorente

Bacterial communities are in a continuous adaptive and evolutionary race for survival. In this work we expand our knowledge on the chemical interplay and specific mutations that modulate the transition from antagonism to co-existence between two plant-beneficial bacteria, Pseudomonas chlororaphis PCL1606 and Bacillus amyloliquefaciens FZB42. We reveal that the bacteriostatic activity of bacillaene produced by Bacillus relies on an interaction with the protein elongation factor FusA of P. chlororaphis and how mutations in this protein lead to tolerance to bacillaene and other protein translation inhibitors. Additionally, we describe how the unspecific tolerance of B. amyloliquefaciens to antimicrobials associated with mutations in the glycerol kinase GlpK is provoked by a decrease of Bacillus cell membrane permeability, among other pleiotropic responses. We conclude that nutrient specialization and mutations in basic biological functions are bacterial adaptive dynamics that lead to the coexistence of two primary competitive bacterial species rather than their mutual eradication.

Pseudomonas chlororaphis

Bacillus amyloliquefaciens

Glycerol kinase

Elongation factor

Multidrug tolerance

Bacillus (shape)

10.1016/j.celrep.2021.109449

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Citations (41)

Mitogen-Activated Protein Kinase Phosphatase 1 (MKP1) Negatively Regulates the Production of Reactive Oxygen Species During Arabidopsis Immune Responses

Molecular Plant-Microbe Interactions (2018)

Viviana Escudero Miguel Ángel Medina Torres Magdalena Delgado Sara Sopeña‐Torres Sanjay Swami

Genetic ablation of the β subunit of the heterotrimeric G protein complex in agb1-2 confers defective activation of microbe-associated molecular pattern (MAMP)-triggered immunity, resulting in agb1-2 enhanced susceptibility to pathogens like the fungus Plectosphaerella cucumerina BMM. A mutant screen for suppressors of agb1-2 susceptibility (sgb) to P. cucumerina BMM identified sgb10, a new null allele (mkp1-2) of the mitogen-activated protein kinase phosphatase 1 (MKP1). The enhanced susceptibility of agb1-2 to the bacterium Pseudomonas syringae pv. tomato DC3000 and the oomycete Hyaloperonospora arabidopsidis is also abrogated by mkp1-2. MKP1 negatively balances production of reactive oxygen species (ROS) triggered by MAMPs, since ROS levels are enhanced in mkp1. The expression of RBOHD, encoding a NADPH oxidase-producing ROS, is upregulated in mkp1 upon MAMP treatment or pathogen infection. Moreover, MKP1 negatively regulates RBOHD activity, because ROS levels upon MAMP treatment are increased in mkp1 plants constitutively overexpressing RBOHD (35S::RBOHD mkp1). A significant reprograming of mkp1 metabolic profile occurs with more than 170 metabolites, including antimicrobial compounds, showing differential accumulation in comparison with wild-type plants. These results suggest that MKP1 functions downstream of the heterotrimeric G protein during MAMP-triggered immunity, directly regulating the activity of RBOHD and ROS production as well as other immune responses.

10.1094/mpmi-08-18-0217-fi

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Citations (29)

YODA MAP3K kinase regulates plant immune responses conferring broad‐spectrum disease resistance

New Phytologist (2018)

Sara Sopeña‐Torres Lucía Jordá Clara Sánchez‐Rodríguez Eva Miedes Viviana Escudero

Summary Mitogen‐activated protein kinases (MAPKs) cascades play essential roles in plants by transducing developmental cues and environmental signals into cellular responses. Among the latter are microbe‐associated molecular patterns perceived by pattern recognition receptors (PRRs), which trigger immunity. We found that YODA (YDA) – a MAPK kinase kinase regulating several Arabidopsis developmental processes, like stomatal patterning – also modulates immune responses. Resistance to pathogens is compromised in yda alleles, whereas plants expressing the constitutively active YDA (CA‐YDA) protein show broad‐spectrum resistance to fungi, bacteria, and oomycetes with different colonization modes. YDA functions in the same pathway as ERECTA (ER) Receptor‐Like Kinase, regulating both immunity and stomatal patterning. ER‐YDA‐mediated immune responses act in parallel to canonical disease resistance pathways regulated by phytohormones and PRRs. CA‐YDA plants exhibit altered cell‐wall integrity and constitutively express defense‐associated genes, including some encoding putative small secreted peptides and PRRs whose impairment resulted in enhanced susceptibility phenotypes. CA‐YDA plants show strong reprogramming of their phosphoproteome, which contains protein targets distinct from described MAPKs substrates. Our results suggest that, in addition to stomata development, the ER‐YDA pathway regulates an immune surveillance system conferring broad‐spectrum disease resistance that is distinct from the canonical pathways mediated by described PRRs and defense hormones.

Plant Immunity

10.1111/nph.15007

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Citations (55)

Differential Expression of Fungal Genes Determines the Lifestyle of Plectosphaerella Strains During Arabidopsis thaliana Colonization

Molecular Plant-Microbe Interactions (2020)

Antonio Muñoz‐Barrios Sara Sopeña‐Torres Brisa Ramos Gemma López Irene del Hierro

The fungal genus Plectosphaerella comprises species and strains with different lifestyles on plants, such as P. cucumerina, which has served as model for the characterization of Arabidopsis thaliana basal and nonhost resistance to necrotrophic fungi. We have sequenced, annotated, and compared the genomes and transcriptomes of three Plectosphaerella strains with different lifestyles on A. thaliana, namely, PcBMM, a natural pathogen of wild-type plants (Col-0), Pc2127, a nonpathogenic strain on Col-0 but pathogenic on the immunocompromised cyp79B2 cyp79B3 mutant, and P0831, which was isolated from a natural population of A. thaliana and is shown here to be nonpathogenic and to grow epiphytically on Col-0 and cyp79B2 cyp79B3 plants. The genomes of these Plectosphaerella strains are very similar and do not differ in the number of genes with pathogenesis-related functions, with the exception of secreted carbohydrate-active enzymes (CAZymes), which are up to five times more abundant in the pathogenic strain PcBMM. Analysis of the fungal transcriptomes in inoculated Col-0 and cyp79B2 cyp79B3 plants at initial colonization stages confirm the key role of secreted CAZymes in the necrotrophic interaction, since PcBMM expresses more genes encoding secreted CAZymes than Pc2127 and P0831. We also show that P0831 epiphytic growth on A. thaliana involves the transcription of specific repertoires of fungal genes, which might be necessary for epiphytic growth adaptation. Overall, these results suggest that in-planta expression of specific sets of fungal genes at early stages of colonization determine the diverse lifestyles and pathogenicity of Plectosphaerella strains.

Epiphyte

Host adaptation

10.1094/mpmi-03-20-0057-r

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Citations (13)

Chemical interplay and complementary adaptative strategies toggle bacterial antagonism and co-existence

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Carlos Molina‐Santiago David Vela‐Corcía Daniel Petras Luis Díaz‐Martínez Alicia Isabel Pérez‐Lorente

Abstract Bacterial communities are in a continuous adaptive and evolutionary race for survival. A myriad of molecules that kill, defend, or mediate communication between bacterial cells of different lineages shape the final structure of the microbial community. In this work we expand our knowledge on the chemical interplay and specific mutations that modulate the transition from antagonism to co-existence between two plant-beneficial bacteria, Pseudomonas chlororaphis PCL1606 and Bacillus amyloliquefaciens FZB42. We reveal that the bacteriostatic activity of bacillaene produced by Bacillus relies on an interaction with the protein elongation factor FusA and how mutations in this protein lead to tolerance to bacillaene and other protein translation inhibitors. Additionally, we describe how the unspecific tolerance to antimicrobials associated with mutations in the glycerol kinase GlpK is provoked mainly by a decrease of Bacillus cell membrane permeability among other pleiotropic cellular responses. We conclude that nutrient specialization and mutations in basic biological functions are bacterial evolutive and adaptive strategies that lead to the coexistence of two primary competitive bacterial species rather than their mutual eradication.

Pseudomonas chlororaphis

Bacillus amyloliquefaciens

Glycerol kinase

Elongation factor

Multidrug tolerance

Bacillus (shape)

10.1101/2021.01.11.426172

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Citations (4)

Impacto de la matriz extracelular de Bacillus subtilis en la respuesta fisiológica de cucurbitáceas

Sara Sopeña‐Torres Antonio De-Vicente-Moreno Diego Francisco Romero-Hinojosa

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Arabidopsis thalianaZn2+-efflux ATPases HMA2 and HMA4 are required for resistance to the necrotrophic fungusPlectosphaerella cucumerinaBMM

Journal of Experimental Botany (2021)

Viviana Escudero Darío Ferreira Sánchez Isidro Abreu Sara Sopeña‐Torres Natalia Makarovsky-Saavedra

Abstract Zinc is an essential nutrient at low concentrations, but toxic at slightly higher ones. It has been proposed that hyperaccumulator plants may use the excess zinc to fend off pathogens and herbivores. However, there is little evidence of a similar response in other plants. Here we show that Arabidopsis thaliana leaves inoculated with the necrotrophic fungus Plectosphaerella cucumerina BMM (PcBMM) accumulate zinc and manganese at the infection site. Zinc accumulation did not occur in a double mutant in the zinc transporters HEAVY METAL ATPASE2 and HEAVY METAL ATPASE4 (HMA2 and HMA4), which has reduced zinc translocation from roots to shoots. Consistent with a role in plant immunity, expression of HMA2 and HMA4 was up-regulated upon PcBMM inoculation, and hma2hma4 mutants were more susceptible to PcBMM infection. This phenotype was rescued upon zinc supplementation. The increased susceptibility to PcBMM infection was not due to the diminished expression of genes involved in the salicylic acid, ethylene, or jasmonate pathways since they were constitutively up-regulated in hma2hma4 plants. Our data indicate a role of zinc in resistance to PcBMM in plants containing ordinary levels of zinc. This layer of immunity runs in parallel to the already characterized defence pathways, and its removal has a direct effect on resistance to pathogens.

Jasmonate

Efflux

Methyl jasmonate

10.1093/jxb/erab400

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Citations (15)

Non-branched β-1,3-glucan oligosaccharides trigger immune responses in Arabidopsis

The Plant Journal (2017)

Hugo Mélida Sara Sopeña‐Torres Laura Bacete María Garrido‐Arandia Lucía Jordá

Fungal cell walls, which are essential for environmental adaptation and host colonization by the fungus, have been evolutionarily selected by plants and animals as a source of microbe-associated molecular patterns (MAMPs) that, upon recognition by host pattern recognition receptors (PRRs), trigger immune responses conferring disease resistance. Chito-oligosaccharides [β-1,4-N-acetylglucosamine oligomers, (GlcNAc)n ] are the only glycosidic structures from fungal walls that have been well-demonstrated to function as MAMPs in plants. Perception of (GlcNAc)4-8 by Arabidopsis involves CERK1, LYK4 and LYK5, three of the eight members of the LysM PRR family. We found that a glucan-enriched wall fraction from the pathogenic fungus Plectosphaerella cucumerina which was devoid of GlcNAc activated immune responses in Arabidopsis wild-type plants but not in the cerk1 mutant. Using this differential response, we identified the non-branched 1,3-β-d-(Glc) hexasaccharide as a major fungal MAMP. Recognition of 1,3-β-d-(Glc)6 was impaired in cerk1 but not in mutants defective in either each of the LysM PRR family members or in the PRR-co-receptor BAK1. Transcriptomic analyses of Arabidopsis plants treated with 1,3-β-d-(Glc)6 further demonstrated that this fungal MAMP triggers the expression of immunity-associated genes. In silico docking analyses with molecular mechanics and solvation energy calculations corroborated that CERK1 can bind 1,3-β-d-(Glc)6 at effective concentrations similar to those of (GlcNAc)4 . These data support that plants, like animals, have selected as MAMPs the linear 1,3-β-d-glucans present in the walls of fungi and oomycetes. Our data also suggest that CERK1 functions as an immune co-receptor for linear 1,3-β-d-glucans in a similar way to its proposed function in the recognition of fungal chito-oligosaccharides and bacterial peptidoglycan MAMPs.

10.1111/tpj.13755

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Citations (123)