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Ranocha, P.

Publications and source records attributed to Ranocha, P..

6 recordsLinked to original sources

A single genetic innovation at the origin of plant terrestrialization

How the functional innovations that enabled plants to first colonize land 450 million years ago evolved remains puzzling. Here, we show that the gain of a single family of enzymes was pivotal in the evolution of two of these innovations, the cuticle that protect plants from dehydration and UV light, and the Arbuscular Mycorrhizal symbiosis promoting water and nutrient uptake. We show that functional phosphatase domain Glycerol-3-Phosphate Acyl Transferase (p-GPATs) evolved in the first land plants, concomitantly with the cuticle and symbiosis. Mutation of two p-GPATs from the liverwort Marchantia paleacea is sufficient to abolish both cuticle formation and AM symbiosis, leading to major developmental defects. We propose that the evolution of p-GPATs in land plants acted as a two birds-one stone innovation, diverting intracellular lipids to the extracellular space and providing a simple path to the evolution of two traits essential for the colonization of land.

plant biology↗

TBL38 is an atypical homogalacturonan acetylesterase with a peculiar cell wall microdomain localization in Arabidopsis seed mucilage secretory cells

Plant cell walls are made of complex polysaccharidic/proteinaceous network whose biosynthesis and dynamics implicate several cell compartments and impact plant development. The synthesis and remodeling of homogalacturonan pectins is associated with multiple developmental processes ranging from growth to response to biotic/abiotic stress. It encompasses Golgi-localized methylation and acetylation and subsequent demethylation and deacetylation in the cell wall. In the last decade, our comprehension of plant polysaccharides acetylation has increased significantly thanks to the study of the TRICHOME BIREFRINGENCE-LIKE (TBL) protein family. TBLs are mostly described as Golgi-localized acetyltransferases specifically targeting diverse hemicelluloses or pectins. Various tbl mutants showed altered wall mechanical properties and dynamics. Here, we study TBL38 that is co-expressed with PECTIN METHYLESTERASE INHIBITOR6 (PMEI6) and PEROXIDASE 36 (PRX36) during the development of Arabidopsis seed mucilage secretory cells (MSCs). We demonstrate the atypical TBL38 cell wall localization restricted to the PMEI6/PRX36 MSC cell wall microdomain. A tbl38 mutant displays an intriguing homogalacturonan immunological phenotype in this cell wall microdomain and in a MSC surface-enriched abrasion powder. This fraction was further characterized by mass spectrometry oligosaccharide profiling revealing an increased homogalacturonan acetylation phenotype. Finally, a recombinant TBL38 is shown to display pectin acetylesterase activity in vitro. These results indicate that TBL38 is an atypical cell wall-localized TBL that displays a homogalacturonan acetylesterase activity rather than a Golgi-localized acetyltransferase activity as observed in previously studied TBLs. TBL38 function during seed development is discussed.

plant biology↗

Apoplastic class III peroxidases PRX62 and PRX69 regulate ROS-homeostasis and cell wall associated extensins linked to root hair growth at low-temperature in Arabidopsis thaliana

Root Hairs (RHs) growth is highly influenced by endogenous as well as by external environmental signals that coordinately regulate its final cell size. RHs actively expand the root surface responsible for nutrient uptake and water absorption. We have recently determined that RH growth was unexpectedly boosted when Arabidopsis thaliana seedlings are cultivated at low temperatures. It was proposed that RH growth plasticity in response to low temperature was linked to a reduced nutrient availability in the media. Here, we explored the molecular basis of this strong RH growth response by using the Genome Wide Association Studies (GWAS) approach on Arabidopsis thaliana natural accessions. We identified the poorly characterized PEROXIDASE 62 (PRX62) as a key protein triggering this conditional growth under a moderate low-temperature stress. In addition, we identified the related protein PRX69 as an important factor in this developmental process. The prx62 prx69 double mutant and the PRX62 and PRX69 over-expressing lines showed contrasting RH phenotypes, peroxidase activities and cyt/apoReactive Oxygen Species (ROS) levels. Strikingly, a cell wall protein extensin (EXT) reporter revealed the effect of peroxidase activity on the EXT cell wall association at 10{degrees}C in the RH apical zone. EXT cell wall insolubilization was enhanced at 10{degrees}C, which was completely abolished under the PRX inhibitor salicylhydroxamic acid (SHAM) treatment. Finally, we demonstrated that the Root Hair defective 6-like 4 (RSL4) bHLH family transcription factor directly controls the expression of PRX69. Collectively, our results indicate that both PRX62 and PRX69 are key apoplastic PRXs that modulate ROS-homeostasis and cell wall EXT-insolubilization linked to RH elongation at low-temperature.

plant biology↗

Global non-animal peroxidases analysis provides insights into the evolutionary study of this gene family in green lineage

The non-animal peroxidases belong to a superfamily of oxidoreductases that reduce the hydrogen peroxide and oxidize numerous substrates. Since their initial characterization in 1992, several advances have provided an understanding into the origin and evolutionary history of this family of proteins. Here, we report for the first time an exhaustive evolutionary analysis of non-animal peroxidases using integrated in silico and biochemical strategies. Thanks to the availability of numerous genomic sequences from many species belonging to different kingdoms together with expert and exhaustive annotation of peroxidase sequences centralized in a dedicated database, we have deepened our understanding of the evolutionary process underlying non-animal peroxidases through phylogenetic reconstructions. We analysed the distribution of all non-animal peroxidases in more than 200 eukaryotic organisms in silico. First, we show that the presence or absence of non-animal peroxidases can be correlated with the presence or absence of certain organelles or with specific biological processes. Examining a wide range of organisms, we confirmed that ascorbate peroxidases (APx) and cytochromes c peroxidases (CcP) were detected respectively in chloroplast and mitochondria containing organisms. Plants, which contain both organelles, are an exception and contain only APxs without CcP. Class III peroxidases (CIII Prx) were only detected in plants and Class II peroxidases (CII Prx) in fungi related to wood decay and plant degradation. Moreover, we demonstrate that biochemical activities (APx, CcP and CIII Prx) assayed in protein extracts obtained from 30 different eukaryotic organisms strongly support the distribution of the sequences resulting from our in silico analysis. The biochemical results confirmed both the presence and classification of non-animal peroxidase encoding sequences.

evolutionary biology↗

A powerful framework for an integrative study with heterogeneous omics data: from univariate statistics to multi-block analysis

The high-throughput data generated by new biotechnologies used in biological studies require specific and adapted statistical treatments. In this work, we propose a novel and powerful framework to manage and analyse multi-omics heterogeneous data to carry out an integrative analysis. We illustrate it using the package mixOmics for the R software as it specifically addresses data integration issues. Our work also aims at confronting the most recent functionalities of mixOmics to real data sets because, even if multi-block integrative methodologies exist, they still have to be used to enlarge our know-how and to provide an operational framework to biologists. Natural populations of the model plant Arabidopsis thaliana are employed in this work but the framework proposed is not limited to this plant and can be deployed whatever the organisms of interest and the biological question. Four omics data sets (phenomics, metabolomics, cell wall proteomics and transcriptomics) have been collected, analysed and integrated in order to study the cell wall plasticity of plants exposed to sub-optimal temperature growth conditions. The methodologies presented start from basic univariate statistics and lead to multi-block integration analysis, and we highlight the fact that each method is associated to one biological issue. Using this powerful framework led us to novel biological conclusions that could not have been reached using standard statistical approaches.

systems biology↗

The Molecular Link Between Auxin And ROS-Mediated Polar Growth

Root hair polar growth is endogenously controlled by auxin and sustained by oscillating levels of reactive oxygen species (ROS). These cells extend several hundred-fold their original size toward signals important for plant survival. Although their final cell size is of fundamental importance, the molecular mechanisms that control it remain largely unknown. Here, we show that ROS production is controlled by the transcription factors RSL4, which in turn is transcriptionally regulated by auxin through several Auxin Responsive Factors (ARFs). In this manner, auxin controls ROS-mediated polar growth by activating RSL4, which then upregulates the expression of genes encoding NADPH oxidases (also known as RBOHs, RESPIRATORY BURST OXIDASE HOMOLOG proteins) and Class-III Peroxidases (PER), which catalyse ROS production. Chemical or genetic interference with the ROS balance or peroxidase activity affect root hair final cell size. Overall, our findings establish a molecular link between auxin regulated ARFs-RSL4 and ROS-mediated polar root hair growth.\n\nSignificance StatementTip-growing root hairs are excellent model systems to decipher the molecular mechanism underlying reactive oxygen species (ROS)-mediated cell elongation. Root hairs are able to expand in response to external signals, increasing several hundred-fold their original size, which is important for survival of the plant. Although their final cell size is of fundamental importance, the molecular mechanisms that control it remain largely unknown. In this study, we propose a molecular mechanism that links the auxin-Auxin Response Factors (ARFs) module to activation of RSL4, which directly targets genes encoding ROS-producing enzymes, such as NADPH oxidases (or RBOHs) and secreted type-III peroxidases (PERs). Activation of these genes impacts apoplastic ROS homeostasis, thereby stimulating root hair cell elongation.

plant biology↗