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Catoni, M.

Publications and source records attributed to Catoni, M..

13 recordsLinked to original sources

Epigenomic Landscape of Oak (Quercus robur) across Seasons and Generations

O_LISeasonal fluctuations strongly shape the physiology of long-lived trees by coordinating growth, dormancy, and stress responses. Increasing evidence points to epigenetic mechanisms, particularly DNA methylation, as regulators of these processes, yet their role in long-lived trees across seasons and generations remains poorly understood. C_LIO_LIWe generated single-base resolution maps of cytosine methylation exploring the epigenetic landscape of 180 year-old mature oak (Quercus robur) trees (genetically homogeneous) along spring, summer and autumn, and in their progeny. C_LIO_LIGenome-wide DNA-methylation revealed a progressive increase in the CHH context (H = A, T or C) from Spring to Summer and Autumn, suggesting epigenetic reprogramming is happening over season. Differentially Methylated Regions (DMRs) were concentrated in promoter regions and terminal inverted repeat (TIR). Differentially methylated transposable elements (TEs) and genes were involved in leaf development and hormonal signalling. By contrast, generational differences (parents versus offspring) were most prominent in CG and CHG contexts and were concentrated in genic regions. C_LIO_LIOaks exhibit distinct seasonal and generational DNA methylation signatures, highlighting the plasticity and developmental specificity of epigenetic regulation. These findings provide a genomic foundation for understanding how epigenetic memory contributes to phenology, developmental programming and long-term adaptation in long-lived plants. C_LI

genetics↗

Gene networks are conserved across reproductive development between the fern Ceratopteris richardii and the flowering plant Arabidopsis thaliana

How plants first invented seeds is a longstanding unresolved evolutionary question. Seed-bearing plants arose from within seedless vascular plants, with ferns as their closest relatives, but how the seed developmental programme first originated has remained intractable through comparative morphology or the fossil record. To investigate this question at the level of gene network evolution, we established a transcriptional expression atlas across sporophyte and gametophyte reproductive development of the fern Ceratopteris richardii and compared reproductive-associated genes to those of Arabidopsis thaliana. Conservation was detected between distinct organs. As in flowering, the hormone gibberellin promoted sporing of the fern sporophyte shoot. Sporophyll genes were conserved with floral development. Gametophyte post-fertilization egg chamber (archegonium) genes were conserved with both pre- and post-fertilization seed development, as were two post-fertilization signals, auxin and sugar. We conclude that the seed may first have arisen through the mis-expression of archegonium developmental programmes within the developing sporophyte sporangium.

plant biology↗

Elicitor specific mechanisms of defence priming in oak seedlings against powdery mildew

Defence priming sensitises plant defences to enable a faster and/or stronger response to subsequent stress. Various chemicals can trigger priming; however, the response remains unexplored in oak. Here, we characterise salicylic acid (SA)-, jasmonic acid (JA)-, and {beta}-aminobutyric acid (BABA)-induced priming of oak seedlings against the causal agent of powdery mildew (Erysiphe alphitoides, PM). Whilst JA had no effects, BABA and SA enhanced resistance by priming callose deposition and SA-dependent gene expression, respectively. Untargeted transcriptome and metabolome analyses revealed genes and metabolites uniquely primed by BABA, SA, and JA. Enrichment analyses demonstrated a limited number of pathways differentiating the three treatments or the resistance-inducing elicitors BABA and SA. However, a similar mode of action between BABA and JA was identified. Moreover, our analyses revealed a lack of crosstalk between SA and JA. Interestingly, priming by BABA was linked to alkaloid, lignan, phenylpropanoid, and indolitic compounds biosynthesis. Moreover, integration of the omics analyses revealed the role of ubiquitination and protein degradation in priming by BABA. Our results confirm the existence of chemical-induced priming in oak and has identified specific molecular markers associated with well-characterised elicitor.

plant biology↗

mobileRNA: a tool for efficient analysis of mobile RNA molecules in multiple genomes.

In plants, mobile RNA molecules play a significant role in long distance signalling, with evidence of transport mechanisms and functional roles for both mobile messenger RNA (mRNA) and small RNA (sRNA) molecules. The movement of RNAs between distant tissues can be revealed in plant grafting experiments involving different genotypes (hetero-grafting) associated to genomic analysis, using the natural polymorphisms between the genotypes to discriminate between RNAs produced in the sampled tissue from those which have travelled from distant organs. However, the hight level of noise in the analyses of RNA sequencing datasets involving two different genotypes, and the lack of a standardised pipeline for the analysis of grafted plants, make the identification of natural mobile RNA molecules a challenge. Here, we introduce a pipeline integrated into an R package, mobileRNA, which performs simultaneous alignment of RNA sequencing samples on a merged reference genome. Using simulated datasets, we show that mobileRNA can identify putative mobile RNAs with unprecedented efficiency in absence of post-processing steps.

bioinformatics↗

Partial redundancy buffers deleterious effects of mutating DNA methyltransferase 1-1 (MET1-1) in polyploid wheat

DNA methylation is conserved across biological kingdoms, playing important roles in gene expression, transposable element silencing and genome stability. Altering DNA methylation could generate additional phenotypic variation for crop breeding, however the lethality of epigenetic mutants in crop species has hindered its investigation. Here, we exploit partial redundancy between homoeologs in polyploid wheat to generate viable mutants in the DNA methyltransferase 1-1 (MET1-1) gene with altered methylation profiles. In both Triticum turgidum (tetraploid wheat) and Triticum aestivum (hexaploid wheat) we identified clear segregation distortions of higher-order mutants (5/6 and 6/6 mutant met1-1 copies in hexaploid and 3/4 and 4/4 copies in tetraploid) when genotyping segregating seeds and seedlings, which we attribute to reduced transmission of null mutant gametes. We found that the reduced transmission occurred from both the maternal and paternal gametes, however, we did not detect any deleterious effects on pollen development. The loss of four or more functional copies of MET1-1 results in decreased CG methylation in hexaploid wheat. Changes to gene expression increase stepwise with the number of mutant alleles suggesting a dosage dependent effect. Finally, we identify heritable changes to flowering and awn phenotypes which segregate independently of MET1-1. Together our results demonstrate that polyploidy can be leveraged to generate quantitative changes to CG methylation without the lethal consequences observed in other crops, opening the potential to exploit novel epialleles in plant breeding.

plant biology↗

Gene body methylation buffers noise in gene expression in plants

Non-genetic variability in gene expression is an inevitable consequence of stochastic nature of processes driving transcription and translation. Largely thought to be deleterious to cell fitness, it is not uniform across the transcriptome. This implies the existence of (molecular) determinants affecting the degree of gene expression variability, although this remain poorly understood in multicellular systems. In this study, we found a link between gene body methylation and noise in gene expression in Arabidopsis thaliana. More specifically, genes with high levels of noise show low levels of gene body methylation, while genes with lower level of noise in gene expression show higher level of gene body methylation. Most importantly, loss of CpG methylation in gene bodies lead to a significant number of genes displaying higher noise in gene expression. This could be compensated by low but significant gain of non-CpG methylation at promoters of certain genes. Overall, our results show that gene body methylation has a functional role and specifically controls the noise in gene expression for a large number of genes.

molecular biology↗

UPF1 is required for gene expression in mitochondria and for the elimination of paternal mtDNA

UPF1 is a conserved RNA helicase in eukaryotes typically defined by its role in nonsense-mediated mRNA decay (NMD). This study presents ChIP-seq evidence indicating an RNA-dependent interaction of UPF1 with mtDNA, consistent with an RNA-mediated association. Mitochondrial localisation was observed as discrete foci throughout the mitochondrial network, frequently in proximity to nucleoids, as confirmed microscopically by immunostaining and GFP tagging of UPF1 in different fly tissues and S2 cells. Depletion of UPF1, but not depletion of the other core NMD factors UPF2 or UPF3, in salivary glands results in smaller mitochondria and, unexpectedly, increased respiratory activity. This increase is observed specifically in salivary glands and correlates with elevated expression of nuclear genes involved in respiratory chain assembly and mitochondrial translation. Changes in mtDNA-encoded gene expression are also observed upon the depletion of UPF1. These findings indicate that UPF1 operates in mitochondria and, independently of canonical NMD, is linked to mitochondrial gene expression and may coordinate nuclear and mitochondrial gene expression in a tissue-specific manner.

cell biology↗

Developmentally regulated generation of a systemic signal for long-lasting defence priming in tomato

Tomato plants can be chemically primed to express long-lasting induced resistance (IR) for the protection of fruit against pathogen infection. Here, we determined that priming results in maintenance of IR in fruit and progeny of tomato plants only when initiated at an early developmental stage. Global DNA methylation analysis revealed seedling-specific changes, which occurred in the context of lower basal methylation, suggesting a greater epigenetic imprinting capacity of young plants. Remarkably, IR was found to be transmissible from primed rootstock to grafted unprimed scions. In these scions, we identified a subset of mobile 24 nt small RNAs associated with genes with enhanced expression in response to Botrytis cinerea infection in fruit, suggesting the functional association of a systemic signal with long-lasting IR and priming. Through integrated omics approaches we have identified markers of long-lasting priming in tomato fruit which could also serve as targets for durable resistance in other crops.

plant biology↗

The widespread nature of Pack-TYPE transposons reveals their importance for plant genome evolution

Pack-TYPE transposable elements (TEs) are a group of non-autonomous DNA transposons found in plants. These elements can efficiently capture and shuffle coding DNA across the host genome, accelerating the evolution of genes. Despite their relevance for plant genome plasticity, the detection and study of Pack-TYPE TEs are challenging due to the high similarity these elements have with genes. Here, we produced an automated annotation procedure designed to study Pack-TYPE elements and used it to successfully annotate and analyse more than 4000 new Pack-TYPE TEs in the rice and maize genomes. Our analysis indicates that Pack-TYPE TEs are an abundant and heterogeneous group of elements. We found that these elements are associated with all main superfamilies of Class II DNA transposons in plants and likely share a similar mechanism to capture new chromosomal DNA sequences. Furthermore, we report examples of the direct contribution of these TEs to coding genes, suggesting a generalised and extensive role of Pack-TYPE TEs in plant genome evolution.

genomics↗

Epigenetic bases of grafting-induced vigour in eggplant

In horticulture, grafting is a popular technique used to combine positive traits from two different plants. This is achieved by joining the plant top part (scion) onto a rootstock which contains the stem and roots. Despite its wide use, the biological mechanisms driving rootstock-induced alterations of the scion phenotype remain largely unknown. Given that epigenetics plays a crucial role during distance signalling in plants, we studied the genome-wide changes induced by DNA methylation in eggplant (Solanum melongena) plants grafted onto two interspecific rootstocks used to increase scion vigour. As a control, we compared any epigenetic effect found in such grafts to patterns detected in self-grafted plants. We found that vigour was associated with a specific change in scion gene expression and a genome-wide hypomethylation in CHH context. Interestingly, this hypomethylation correlated with the down-regulation of younger and potentially more active LTR retrotransposons (LTR-TEs), suggesting that graft-induced epigenetic modifications are associated to both physiological and molecular phenotypes in grafted plants. We propose that rootstocks can promote vigour by reducing DNA methylation in the scion genome, following similar principles found in some heterotic hybrids.

plant biology↗

Environmental and epigenetic regulation of Rider retrotransposons in tomato

Transposable elements in crop plants are the powerful drivers of phenotypic variation that has been selected during domestication and breeding programs. In tomato, transpositions of the LTR (long terminal repeat) retrotransposon family Rider have contributed to various phenotypes of agronomical interest, such as fruit shape and colour. However, the mechanisms regulating Rider activity are largely unknown. We have developed a bioinformatics pipeline for the functional annotation of retrotransposons containing LTRs and defined all full-length Rider elements in the tomato genome. Subsequently, we showed that accumulation of Rider transcripts and transposition intermediates in the form of extrachromosomal DNA is triggered by drought stress and relies on abscisic acid signalling. We provide evidence that residual activity of Rider is controlled by epigenetic mechanisms involving siRNAs and the RNA-dependent DNA methylation pathway. Finally, we demonstrate the broad distribution of Rider-like elements in other plant species, including crops. Thus our work identifies Rider as an environment-responsive element and a potential source of genetic and epigenetic variation in plants.

plant biology↗

Mobilization of Pack-CACTA transposons in Arabidopsis reveals the mechanism of gene shuffling

Pack-TYPE transposons are a unique class of potentially mobile non-autonomous elements that can capture, merge and relocate fragments of chromosomal DNA. It has been postulated that their activity accelerates the evolution of host genes. However, this important presumption is based only on the sequences of currently inactive Pack-TYPE transposons and the acquisition of chromosomal DNA has not been recorded in real time. We have now for the first time witnessed the mobilization of novel Pack-TYPE elements related to the CACTA transposon family over several plant generations. Remarkably, these elements tend to insert into genes as closely spaced direct repeats and they frequently undergo incomplete excisions, resulting in the deletion of one of the end sequences. These properties constitute a mechanism of efficient acquisition of genic DNA residing between neighbouring Pack-TYPE transposons and its subsequent mobilization. Our work documents crucial steps in the formation in vivo of novel Pack-TYPE transposons and thus the mechanism of gene shuffling mediated by this type of mobile element.

genetics↗

Sensitive detection of pre-integration intermediates of LTR retrotransposons in crop plants

Retrotransposons have played an important role in the evolution of host genomes1,2. Their impact on host chromosomes is mainly deduced from the composition of DNA sequences, which have been fixed over evolutionary time. These studies provide important \"snapshots\" reflecting historical activities of transposons but do not predict current transposition potential. We previously reported Sequence-Independent Retrotransposon Trapping (SIRT) as a methodology that, by identification of extrachromosomal linear DNA (eclDNA), revealed the presence of active LTR retrotransposons in Arabidopsis9. Unfortunately, SIRT cannot be applied to large and transposon-rich genomes of crop plants. We have since developed an alternative approach named ALE-seq (amplification of LTR of eclDNAs followed by sequencing). ALE-seq reveals sequences of 5 LTRs of eclDNAs after two-step amplification: in vitro transcription and subsequent reverse transcription. Using ALE-seq in rice, we detected eclDNAs for a novel Copia family LTR retrotransposon, Go-on, which is activated by heat stress. Sequencing of rice accessions revealed that Go-on has preferentially accumulated in indica rice grown at higher temperatures. Furthermore, ALE-seq applied to tomato fruits identified a developmentally regulated Gypsy family of retrotransposons. Importantly, a bioinformatic pipeline adapted for ALE-seq data analyses allows the direct and reference-free annotation of new active retroelements. This pipeline allows assessment of LTR retrotransposon activities in organisms for which genomic sequences and/or reference genomes are unavailable or are of low quality.

plant biology↗