Richard Berthomé

Ongoing climate change is driving unprecedented environmental fluctuations, with extreme events predicted to increase in frequency, intensity and duration. Among climatic parameters, temperature is expected to fluctuate the most by the end of the century and its elevation has already demonstrated to pose a major challenge to plant health. In this context, understanding how temperature modulates plant-pathogen interactions and their underlying genetic architecture is critical. Bacterial wilt, caused by strains of the Ralstonia solanacearum species complex, is a devastating disease affecting many plant species. Genetic resistance remains the most effective control strategy. In tomato, resistance is quantitative and mostly relies on quantitative trait loci (QTLs) bwr-6 and bwr-12 . However, as in other crops, high temperature and humidity can compromise this resistance in commercial tomato cultivars. We investigated temperature-dependent quantitative disease resistance (QDR) using a panel of 189 wild tomato accessions, predominantly Solanum pimpinellifolium , representing genetic diversity from contrasting ecological conditions. Disease progression was monitored from three to ten days post-inoculation at 28 °C and 32 °C, using a time-course phenotyping approach. Genome-wide association (GWA) analyses were performed, based on daily symptom scores and two reference genomes, to account for structural variations and improve QTL detection. This strategy identified 44 candidate genes and revealed a temporally dynamic genetic architecture of the plant response. Strikingly, no candidate genes were shared between temperatures, supporting distinct genetic determinants under different temperature conditions. Many candidate genes were expressed in roots and belong to gene families involved in plant immunity, with two candidates co-localizing with bwr-6 and bwr-12 , whose causal genes remain unknown. Altogether, our findings demonstrate that resistance to bacterial wilt in wild tomato is flexible, environment-dependent, and temporally dynamic, highlighting the importance of integrating environmental context and genomic diversity to better understand plant-pathogen interactions.

Climate change reshapes host-pathogen interactions by increasing pathogen aggressiveness and weakening plant immune responses, particularly under heat stress. Nucleotide-binding leucine-rich repeat (NLR) immune receptors, key players in pathogen recognition, are altered under elevated temperatures in both plants and mammals, posing a major challenge to disease resistance. In Arabidopsis thaliana, the well-described RPS4/RRS1 NLR pair confers resistance to the worldwide devastating phytopathogenic Ralstonia pseudosolanacearum. Here, by combining the exploration of natural genetic variation with genetic mapping, polymorphism analysis, structural modeling, and functional complementation, we demonstrated that the paucity of full thermostable resistance is primarily associated with a unique RPS4/RRS1 haplotype carrying key substitutions in leucine-rich repeat domains. These findings reveal natural genetic diversity as a source of thermostable resistance, highlighting promising opportunities to engineer climate-resilient plants.

Bacterial wilt, caused by bacterial strains of the Ralstonia solanacearum species complex, is one of the most harmful diseases striking many crops including tomato. Its spread is dependent upon temperature and humidity, which are expected to fluctuate strongly due to climate change. Previous results have highlighted that temperature elevation led to an increase in disease severity in commercial cultivars, whose resistance is quantitative and mostly relies on the Quantitative Trait Loci ( QTL ) bwr-6 and bwr-12 . In this study, we focused on temperature-dependent quantitative disease resistance (QDR) to bacterial wilt with the aim to unravel new resistance mechanisms that remain efficient at higher temperatures. For this purpose, a new panel of 189 accessions composed of tomato wild relatives, was assembled and sequenced thus creating a unique genomic resource. Its response to the Ralstonia pseudosolanacearum strain GMI1000 from three- to ten-days post-inoculation at 28°C and 32°C was explored. To discover the genetic basis underlying the responses of the panel, Genome-Wide Association (GWA) studies were conducted using the disease symptom scores recorded daily and monitored throughout the kinetics of the infection. To improve QTL detection, we have proposed a new approach using two reference genomes from within the panel. By correcting part of a single reference genome, especially when the only reference genome is a cultivar, this approach may be considered an alternative to pangenomic studies. As panel sequencing was highly resolutive, QTL positions allowed the identification of 44 candidate genes, which seemed to follow a temporal dynamic of activation after pathogen inoculation. Interestingly, no candidate genes were found to be common between the two phenotyping temperatures, highlighting the importance of the experimental design in addressing this type of question. Most of our quantitative disease resistance candidate genes belong to gene families described as being involved in immunity. Moreover, a significant proportion appears to be expressed in roots where bacterial infection occurs. Among them, two candidates are closely linked to the genomic positions of the bwr-6 and bwr-12 QTLs , the main QTLs of bacterial wilt Quantitative Disease Resistance (QDR) studied whose mechanisms of action are still unknown. Author summary: Bacterial wilt is a plant disease that affects more than 200 crop species (including tomato, potato and banana) leading to high yield losses. The most efficient way to deal with this disease is still the use of genetic resistance. However, previous studies have shown that numerous sources of resistance are negatively affected when plants face heat stress, which is alarming in a context of global warming. In this study, we have developed a new approach for discovering candidate genes in tomato capable of conferring thermostable resistance to bacterial wilt. Forty-four genes were sequentially detected over time, reflecting different temporal dynamics of induction after inoculation. Even if none were found to be common between the two temperatures, available information on their transcriptional regulation in roots and their involvement in immune processes confirms their relevance. Finally, we provide a short list of the candidate genes identified, some of which are currently undergoing functional validation and will be used in breeding programs to help overcome epidemics in future years.

Is there a specific calcium signal out there to decode combined biotic stress and temperature elevation?

Calcium signals are crucial for the activation and coordination of signaling cascades leading to the establishment of plant defense mechanisms. Here, we studied the contribution of CML8, an Arabidopsis calmodulin-like protein in response to Ralstonia solanacearum and to pathogens with different lifestyles, such as Xanthomonas campestris pv. campestris and Phytophtora capsici. We used pathogenic infection assays, gene expression, RNA-seq approaches, and comparative analysis of public data on CML8 knockdown and overexpressing Arabidopsis lines to demonstrate that CML8 contributes to defense mechanisms against pathogenic bacteria and oomycetes. CML8 gene expression is finely regulated at the root level and manipulated during infection with Ralstonia, and CML8 overexpression confers better plant tolerance. To understand the processes controlled by CML8, genes differentially expressed at the root level in the first hours of infection have been identified. Overexpression of CML8 also confers better tolerance against Xanthomonas and Phytophtora, and most of the genes differentially expressed in response to Ralstonia are differentially expressed in these different pathosystems. Collectively, CML8 acts as a positive regulator against Ralstonia solanaceraum and against other vascular or root pathogens, suggesting that CML8 is a multifunctional protein that regulates common downstream processes involved in the defense response of plants to several pathogens.

Summary: In their natural environment, plants are exposed to biotic or abiotic stresses that occur sequentially or simultaneously. Plant responses to these stresses have been studied widely and have been well characterised in simplified systems involving single plant species facing individual stress. Temperature elevation is a major abiotic driver of climate change and scenarios have predicted an increase in the number and severity of epidemics. In this context, here we review the available data on the effect of heat stress on plant–pathogen interactions. Considering 45 studies performed on model or crop species, we discuss the possible implications of the optimum growth temperature of plant hosts and pathogens, mode of stress application and temperature variation on resistance modulations. Alarmingly, most identified resistances are altered under temperature elevation, regardless of the plant and pathogen species. Therefore, we have listed current knowledge on heat‐dependent plant immune mechanisms and pathogen thermosensory processes, mainly studied in animals and human pathogens, that could help to understand the outcome of plant–pathogen interactions under elevated temperatures. Based on a general overview of the mechanisms involved in plant responses to pathogens, and integrating multiple interactions with the biotic environment, we provide recommendations to optimise plant disease resistance under heat stress and to identify thermotolerant resistance mechanisms.

Plant immunity is often negatively impacted by heat stress. However, the underlying molecular mechanisms remain poorly characterized. Based on a genome‐wide association mapping approach, this study aims to identify in Arabidopsis thaliana the genetic bases of robust resistance mechanisms to the devastating pathogen Ralstonia solanacearum under heat stress. A local mapping population was phenotyped against the R. solanacearum GMI1000 strain at 27 and 30 °C. To obtain a precise description of the genetic architecture underlying natural variation of quantitative disease resistance (QDR), we applied a genome‐wide local score analysis. Alongside an extensive genetic variation found in this local population at both temperatures, we observed a playful dynamics of quantitative trait loci along the infection stages. In addition, a complex genetic network of interacting loci could be detected at 30 °C. As a first step to investigate the underlying molecular mechanisms, the atypical meiotic cyclin SOLO DANCERS gene was validated by a reverse genetic approach as involved in QDR to R. solanacearum at 30 °C. In the context of climate change, the complex genetic architecture underlying QDR under heat stress in a local mapping population revealed candidate genes with diverse molecular functions.

C to U editing is one of the post-transcriptional steps which are required for the proper expression of chloroplast and mitochondrial genes in plants. It depends on several proteins acting together which include the PLS-class pentatricopeptide repeat proteins (PPR). DYW2 was recently shown to be required for the editing of many sites in both organelles. In particular almost all the sites associated with the E+ subfamily of PPR proteins are depending on DYW2, suggesting that DYW2 is required for the function of E+-type PPR proteins. Here we strengthened this link by identifying 16 major editing sites controlled by 3 PPR proteins: OTP90, a DYW-type PPR and PGN and MEF37, 2 E+-type PPR proteins. A re-analysis of the DYW2 editotype showed that the 49 sites known to be associated with the 18 characterized E+-type PPR proteins all depend on DYW2. Considering only the 288 DYW2-dependent editing sites as potential E+-type PPR sites, instead of the 795 known editing sites, improves the performances of binding predictions systems based on the PPR code for E+-type PPR proteins. However, it does not compensate for poor binding predictions.

Brassicaceae hydathode anatomy affects infection by the adapted vascular pathogen Xanthomonas campestris pv campestris.