bioRxiv Science⌕ Search

Biology subjects

Mbengue, M.

Publications and source records attributed to Mbengue, M..

7 recordsLinked to original sources

EPP1 is an ancestral component of the plant Common SymbiosisPathway

The success of plants on land has been enabled by mutualistic intracellular associations with microbes for 450 million years (Delaux and Schornack 2021). Because of their intracellular nature, the establishment of these interactions requires tight regulation by the host plants. In particular, three genes - SYMRK, CCaMK and CYCLOPS - form the core of an ancestral common symbiosis pathway (CSP) for intracellular symbioses, and are conserved since the most recent common ancestor of land plants (Radhakrishnan et al. 2020; Delaux et al. 2015; Wang et al. 2010; Parniske 2008). Here, we describe EPP1 as a fourth gene committed to the CSP. Among land plants, EPP1 is conserved only in species able to associate with at least one type of intracellular symbiont. We found that loss-of-function epp1 mutants or EPP1 knock-down lines in four clades of land plants - legumes, Solanaceae, monocots and bryophytes - are all impaired in their ability to associate with arbuscular mycorrhizal fungi. We discovered that the plasma membrane-localized receptor-like SYMRK phosphorylates EPP1 on a conserved serine residue and that this phosphorylation is essential for symbiosis. Using a gain-of-function approach, we demonstrate that EPP1 is upstream of the nuclear kinase CCaMK. We propose that EPP1 is an ancestral component of the essential pathway that has regulated plant symbiosis for half a billion years.

plant biology↗

Conservation of symbiotic signalling across 450 million years of plant evolution

HighlightO_LIThe common symbiotic pathway is activated during arbuscular mycorrhizal symbiosis in Marchantia paleacea C_LIO_LIThe three core members of the common symbiotic pathway are essential for symbiosis in Marchantia paleacea C_LIO_LIThe molecular function of the CCaMK/CYCLOPS module is conserved across land plants C_LIO_LISymbiotic signalling has been conserved in plants for 450 million years C_LI The colonization of land by plants 450 million years ago revolutionized life on Earth1. The fossil record2 and genetic evidence in extant species3 suggest that this transition was facilitated by interactions with symbiotic arbuscular mycorrhizal (AM) fungi4. This ancestral symbiosis relied on the biosynthesis of chemicals by the host plant, both as signals5 and as nutrients3. In angiosperms, a signalling pathway involving the receptor-like kinase SYMRK/DMI26,7, the Calcium and Calmodulin-dependent protein kinase CCaMK/DMI38 and the transcription factor CYCLOPS/IPD39,10 has been described as the common symbiosis pathway (CSP), essential for the establishment of the AM symbiosis and the root-nodule symbiosis11. Phylogenetic and comparative phylogenomic analyses indicated an ancient origin of the CSP, present in all extant land plants forming intracellular symbioses12-15. Trans-complementation assays of the angiosperm mutants with orthologs from diverse species further indicated the conservation of the molecular function of the CSP across the embryophytes9,12,14-16. However, this correlative evidence did not allow testing the ancestral biological function of the CSP. In this study we demonstrate that SYMRK, CCaMK and CYCLOPS are essential for the colonization by AM fungi in bryophytes, indicating that plants have maintained a dedicated signalling pathway to support symbiotic interactions for 450 million years.

plant biology↗

LysM-RLK plays an ancestral symbiotic function in plants

Arbuscular mycorrhiza (AM) with soilborne Glomeromycota fungi was pivotal in the conquest of land by plants almost half a billion years ago. In flowering plants, it is hypothesised that AM is initiated by the perception of AM-fungi-derived chito- and lipochito-oligosaccharides (COs/LCOs) in the host via Lysin Motif Receptor-Like Kinases (LysM-RLKs). However, it remains uncertain whether plant perception of these molecules is a prerequisite for AM establishment and for its origin. Here, we made use of the reduced LysM-RLK complement present in the liverwort Marchantia paleacea to assess the conservation of the role played by this class of receptors during AM and in COs/LCOs perception. Our reverse genetic approach demonstrates the critical function of a single LysM-RLK, LYKa, in AM formation, thereby supporting an ancestral function for this receptor in symbiosis. Binding studies, cytosolic calcium variation recordings and genome-wide transcriptomics indicate that another LysM-RLK of M. paleacea, LYR, is also required for triggering a response to COs/LCOs, despite being dispensable for AM formation. Collectively, our results demonstrate that the perception of symbionts by LysM-RLK is an ancestral feature in land plants, and suggest the existence of yet-uncharacterised AM-fungi signals.

plant biology↗

The leucine-rich repeat receptor kinase QSK1 is a novel regulator of PRR-RBOHD complex and is employed by the bacterial effector HopF2Pto to modulate plant immunity

Plants detect pathogens using cell-surface pattern recognition receptors (PRRs) like EFR and FLS2, which recognize bacterial EF-Tu and flagellin, respectively. These PRRs, belonging to the leucine-rich repeat receptor kinase (LRR-RK) family, activate the production of reactive oxygen species via the NADPH oxidase RBOHD. The PRR-RBOHD complex is tightly regulated to prevent unwarranted or exaggerated immune responses. However, certain pathogenic effectors can subvert these regulatory mechanisms, thereby suppressing plant immunity. To elucidate the intricate dynamics of the PRR-RBOHD complex, we conducted a comparative co-immunoprecipitation analysis using EFR, FLS2, and RBOHD. We identified QSK1, an LRR-RK, as a novel component of the PRR-RBOHD complex. QSK1 functions as a negative regulator of PRR-triggered immunity (PTI) by downregulating the abundance of FLS2 and EFR. QSK1 is targeted by the bacterial effector HopF2Pto, a mono-ADP ribosyltransferase, resulting in the reduction of FLS2 and EFR levels through both transcriptional and transcription-independent pathways, thereby inhibiting PTI. Furthermore, HopF2Pto reduces transcript levels of PROSCOOP genes encoding important stress-regulated phytocytokines and their receptor MIK2. Importantly, HopF2Pto requires QSK1 for its accumulation and virulence functions within plants. In summary, our results provide novel insights into the mechanism by which HopF2Pto employs QSK1 to desensitize plants to pathogen attack. One Sentence SummaryQSK1, a novel component in the plant immune receptor complex, downregulates these receptors and phytocytokines, and is exploited by bacterial effector HopF2Pto to desensitize plants to pathogen attack.

plant biology↗

Transcriptional response to host chemical cues underpins expansion of host range in a fungal plant pathogen lineage

The host range of parasites is an important factor in assessing the dynamics of disease epidemics. The evolution of pathogens to accommodate new hosts may lead to host range expansion, a process the molecular bases of which are largely enigmatic. The fungus Sclerotinia sclerotiorum parasitizes more than 400 plant species from diverse eudicot families while its close relative, S. trifoliorum, is restricted to plants from the Fabaceae family. We analyzed S. sclerotiorum global transcriptome reprogramming on hosts from six botanical families and reveal a flexible, host-specific transcriptional program driven by core and host-response co-expression (SPREx) gene clusters. We generated a chromosome-level genome assembly for S. trifoliorum and found near-complete gene space conservation in broad and narrow host range Sclerotinia species. However, S. trifoliorum showed increased sensitivity to the Brassicaceae defense compound camalexin. Inter-specific transcriptome analyses revealed a lack of transcriptional response to camalexin in S. trifoliorum and provide evidence that cis-regulatory variation associates with the genetic accommodation of Brassicaceae in the Sclerotinia host range. Our work demonstrates adaptive plasticity of a broad host range pathogen with specific responses to different host plants and demonstrates the co-existence of signatures for generalist and polyspecialist life styles in the genome of a plant pathogen. We reason that this mechanism enables the emergence of new disease with no or limited gene flow between strains and species, and could underlie the emergence of new epidemics originating from wild plants in agricultural settings.

genomics↗

Rapid identification of an Arabidopsis NLR gene conferring susceptibility to Sclerotinia sclerotiorum using time-resolved automated phenotyping

The broad host range necrotrophic fungus Sclerotinia sclerotiorum is a devastating pathogen of many oil and vegetable crops. Plant genes conferring complete resistance against S. sclerotiorum have not been reported. Instead, plant populations challenged by S. sclerotiorum exhibit a continuum of partial resistance designated as quantitative disease resistance (QDR). Because of their complex interplay and their small phenotypic effect, the functional characterization of QDR genes remains limited. How broad host range necrotrophic fungi manipulate plant programmed cell death is for instance largely unknown. Here, we designed a time-resolved automated disease phenotyping pipeline and assessed the kinetics of disease symptoms caused by seven S. sclerotiorum isolates on six A. thaliana natural accessions with unprecedented resolution. We hypothesized that large effect polymorphisms common to the most resistant A. thaliana accessions, but absent from the most susceptible ones, would point towards disease susceptibility genes. This identified highly divergent alleles of the nucleotide-binding site leucine-rich repeat gene LAZ5 in the resistant accessions Rubenzhnoe and Lip-0. Two LAZ5-deficient mutant lines in the Col-0 genetic background showed enhanced QDR to S. sclerotiorum, whereas plants mutated in the closely related CSA1 gene responded like the wild type. These findings illustrate the value of time-resolved image-based phenotyping for unravelling the genetic bases of complex traits such as QDR. Our results suggest that S. sclerotiorum manipulates plant sphingolipid pathways guarded by LAZ5 to trigger programmed cell death and cause disease.

plant biology↗

Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight candidate host target genes associated with quantitative disease resistance

Plant pathogenic fungi secrete effector proteins and secondary metabolites to cause disease. Additionally, some produce small RNAs (sRNAs) that silence transcripts of host immunity genes through RNA interference. The fungus Sclerotinia sclerotiorum infects over 600 plant species, but little is known about its molecular interactions with its hosts. In particular, the role of sRNAs in S. sclerotiorum pathogenicity has not been determined. By sequencing sRNAs in vitro and during infection of two host species, we found that S. sclerotiorum produces at least 374 highly abundant sRNAs. These sRNAs mostly originated from polymorphic repeat-rich genomic regions. Predicted gene targets of these sRNAs, from 10 different host species, were enriched for immunity-related functional domains. Predicted A. thaliana gene targets of S. sclerotiorum sRNAs were significantly more down-regulated during infection than other genes. A. thaliana gene targets were also more likely to contain single nucleotide polymorphisms (SNPs) associated with quantitative disease resistance. In conclusion, sRNAs produced by S. sclerotiorum are likely capable of silencing immunity components in multiple hosts. Prediction of fungal sRNA targets in host plant genomes can be combined with other global approaches, such as genome wide association studies and transcriptomics, to assist identification of plant genes involved in disease resistance.

plant biology↗