The rise of the green revolution brought about significant advancements in agricultural productivity through the breeding of high-yield crop varieties in dense monoculture and intensive use of fertilizers and pesticides. However, this shift towards monoculture farming has inadvertently accelerated the development of virulent pathogen strains and inflicted massive environmental damages. In response to these challenges, cultivar mixtures have emerged as a sustainable alternative, promising to maintain or increase crop yields while simultaneously reducing plant disease severity and minimizing pesticide use. Despite a comprehensive understanding of the epidemiological mechanisms that increase resistance durability in intraspecific mixtures, the molecular plant-plant interaction mechanisms controlling disease severity, independent of pathogen population dynamics, remain largely unexplored. Recent investigations have revealed that plant-plant interactions in wheat cultivar mixtures are associated with decreased leaf rust disease severity. This process, termed neighbor-modulated susceptibility, involves genotype-specific and root-derived physical/chemical cues that remain unknown. In addition, the molecular mechanisms at play in the leaf that reduce leaf rust severity remain unclear. However, certain allele combinations between wheat genotypes can reverse neighbor-decreased susceptibility, underscoring the critical need to unravel the genetic intricacies of plant-plant interactions to optimize the performances of wheat cultivar mixtures. This research project aims at the identification and functional validation of key genes involved in intraspecific interactions in hexaploid wheat, with a particular focus on root-mediated perception processes that influence disease susceptibility. Drawing parallels from the well-described genotypic recognition mechanisms in other taxa but remaining unknown in plant roots, this project hypothesizes that specialized metabolites and peptides biosynthesized in the roots play central roles in facilitating these interactions. By employing a multidisciplinary approach that integrates association genetics, comparative transcriptomics and metabolomics, and reverse genetics, the main goals of this project are: 1) identify the neighbor-emitted-cues responsible for modulating disease susceptibility by leveraging association genetics and advanced molecular profiling techniques; and 2) elucidate the genetic framework orchestrating neighbor-modulated susceptibility in the receiver wheat genotype by reconstructing its gene expression landscape, followed by 3) rigorous functional validation in controlled and field conditions. Unveiling the molecular foundations of neighbor-modulated susceptibility could pave the way to many applications in agriculture. In particular, it could have a significant impact on the development of agroecological practices based on crop diversity. This project also holds the potential to reveal a root-based genotypic recognition mechanism which has been a long-lasting subject of debate in the plant science community.

Small (s)RNA-directed RNA interference (RNAi) plays an important role in epigenetic regulation of gene expression, antiviral defence and cross-talk between eukaryotic organisms. In this project we will dissect the biogenesis and function of sRNAs in 3-way plant-virus-insect vector interactions and exploit trans-kingdom RNAi mediated by mobile sRNAs to investigate molecular mechanisms underlying virus transmission by vectors and to interfere with the transmission process. To this end we will use two related legume viruses of family Nanoviridae and aphid vectors causing economically-important diseases worldwide. Based on available evidence and preliminary data described below, we hypothesize that mobile viral sRNAs, generated by plant RNAi and ingested by phloem sap-feeding aphids, penetrate into aphid cells and target genes, thereby regulating gene expression to facilitate the passage of viral particles throughout aphid body and inoculation of a new host plant. Likewise, virus-induced mobile plant sRNAs may regulate aphid gene expression in favour of virus transmission. Finally, the plant genes presumably targeted by viral or virus-induced plant sRNAs, or mobile aphid sRNAs may also have impact on virus acquisition by aphids and hence transmission. To test these hypotheses we will profile sRNA-ome, transcriptome and RNA degradome of plants and aphids fed on virus-infected and control legume plants. We will then use virus-induced gene silencing (VIGS) and exogenous RNAi approaches to (i) validate the role of virus-regulated and sRNA-targeted genes in virus acquisition and transmission by aphids and (ii) investigate molecular mechanisms underlying the circulation and persistence of viral particles in the aphid body. Our results would ultimately contribute to designing RNAi-based tools and other novel approaches to control aphid-borne diseases not only by killing insect vectors but also by interfering with virus transmission without impacts on vector viability/fitness that may force selection for insect resistance.

Vector biology is an essential field within global health. For plant pathogens and their arthropod vectors, a major mode of transmission involves a very early but specific interaction with peculiar cuticular surfaces of the vector. These mechanisms nevertheless remain poorly understood but those of a few viral/bacterial models; they might involve either protein receptors of the stylet acrostyle (virus), or cibarial µterritories (bacteria). A reliable platform for in vitro interaction with native chitin-protein assemblies is currently lacking, and this is the subject of the ANR ArtiCute (Artificial Biomimetic Cuticles). These protein arrays should eventually allow a medium throughput screening of candidate proteins downstream of genomic annotations and quick a priori or experimental sorting. Validation work will concern our 2 hemipteran models and their viral (CaMV & TuMV) or bacterial (Dickeya dadantii & Serratia symbiotica) partners, as well as potential interaction blocking agents.

Behavioural epidemiology studies the interaction between human behaviour and the spread of infectious diseases. Plant pathogens and their insect vectors are among the main threats to global food security. The methods used to control plant pathogens and their vectors must be ecologically-friendly and sustainable. To date, the few models that couple grower behaviour with plant disease epidemics do not address pathogen evolution. However, grower decisions impose new selection pressures on pathogens, which evolve and adapt to control methods. Grower decisions may concern several control methods including the use of disease-resistant varieties, roguing (i.e., removing) infected hosts, and the use of biocontrol agents against pathogens or their insect vectors. Our biological models include the Citrus greening disease (caused by vector-borne bacteria), and nematodes of potato and tomato. The objective of this project is to develop a theory of behavioural epidemiology specific to plant health, with an evolutionary perspective. More specifically, we will explore the key mechanisms allowing the adoption (or not) of control methods in sufficient proportion to maintain disease incidence under an acceptable level, taking pathogen evolution into account. Such control methods are often expensive, and we aim at assessing to what extent subsidising them would stabilise their use in order to maximise plant health in the long-run. The consortium gathered around this project brings together expertise in plant disease epidemiology, mathematics, computer sciences, and economics. The interdisciplinary nature of the project will lead to original research in the field of plant disease epidemiology and evolution. From an applied perspective, this project will help design policies to control plant diseases that consider the dynamic behaviour of growers as well as pathogen evolution. This research aims to develop plant protection methods respectful of people and their environment.

The unpredictable outbreaks that recently emerged from tropical forest's wildlife highlight a tremendous lack of knowledge about viruses that circulate within such ecosystems. Indeed, only about 1% of eukaryotic viruses present on earth have been identified, which would constitute a major obstacle to the early detection and rapid control of any new epidemic event. However, detection and characterisation of animal and plant’s hosted viruses in a given ecosystem require provision of massive biological samples which is extremely difficult in these dense and hostile ecosystems where animal species are often inaccessible. It is therefore critical to identify new strategies and approaches for exploring viral ecology. To this end, the MAGNAN project proposes to use Dorylus army ants as an innovative and indirect wildlife’s sampling strategy. Hence, army ants figure amongst major arthropod predators and are considered to be key species in tropical forest ecosystems. Large nomadic colonies constituted of thousands of workers move, making spectacular raids on the ground, hunting and overwhelming a very wide range of live invertebrate and vertebrate preys in large quantities, but also scavenging animal carcasses or feeding directly on plants. Based on convincing preliminary results obtained by viral metagenomics methods, we have shown that army ants can accumulate large amounts of genomic sequences of vertebrate, invertebrate and plant’s hosted viruses. The project aims at providing better understanding of virome in tropical forest ecosystems as well as implementing a new, ground-breaking and non-invasive strategy for surveillance of viral zoonoses in environments where spillovers are frequent. This project represents a proof of concept that may pave the way towards large scale studies on all tropical forest ecosystems’ virome. It stands at the forefront of an innovative research field focused on virus ecology and emergence in One Health and Eco Health perspectives.