Publications

2025

1. BioRxiv

   Zinc deficiency induces spatially distinct responses in roots and impacts ZIP12-dependent zinc homeostasis in Arabidopsis

   Noémie Thiébaut, Daniel Pergament Persson, Manon C. M. Sarthou, Pauline Stévenne, Bernard Bosman, Monique Carnol, Steven Fanara, Nathalie Verbruggen, and Marc Hanikenne

   2025

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   How zinc (Zn) deficiency shapes root development remains unclear, with conflicting reports on its effect on primary root growth in Arabidopsis thaliana (Arabidopsis). The impact of Zn short-age on the root apical meristem (RAM) in particular has not been systematically explored. Using an integrative approach combining cell biology, transcriptomics, and ionomics, we dissected how Zn deficiency alters root zonation and function. We showed that Zn deficiency triggers a striking reorganization of the root tip (RT): the RAM size is reduced, yet meristematic activity and local Zn levels are preserved. This is accompanied by promoted cell elongation and differentiation. Transcriptome profiling revealed a distinct Zn deficiency response in the RAM-enriched RT com-pared to mature root tissues, with ZIP12 emerging as the most strongly induced gene in the RT. Functional analysis of zip12 mutants uncovered major defects in root growth, RAM structure, expression of Zn-responsive genes, and metal partitioning. Our work unveiled a new layer of root developmental plasticity under Zn deficiency and identified ZIP12 as a central player in main-taining Zn homeostasis and root meristem function in Arabidopsis. These findings provide a framework to better understand how plants adapt root growth to fluctuating micronutrient availability.

2. Plant J.

   Arabidopsis thaliana root responses to Cd exposure: insights into root tip-specific changes and the role of HY5 in limiting Cd accumulation and promoting tolerance

   Ludwig Richtmann, Santiago Prochetto, Noémie Thiébaut, Manon C.M. Sarthou, Stéphanie Boutet, Marc Hanikenne, Stephan Clemens, and Nathalie Verbruggen

   The Plant Journal, Jun 2025

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   Cadmium (Cd) is a major environmental pollutant with high toxicity. While Cd exposure reduces root growth, its specific impact on the root meristem and differentiating parts remains poorly understood. This study investigates the spatial and temporal responses of Arabidopsis thaliana roots to Cd stress by dividing roots into root tips (RT) and remaining roots (RR) and employing transcriptomic, ionomic, and metabolomic analyses. Cd exposure altered mineral profiles, with RT accumulating less Cd but showing distinct changes in other elements compared to RR. Metabolomic analysis revealed root part-specific changes in phytochelatins, flavonoids, and glucosinolates. Transcriptomic data highlighted constitutive differences between RT and RR, reflecting functional specialization. Also, they revealed Cd-induced root part-specific and time-dependent transcriptional responses, including modulation of Fe-related genes. Phenotypic validation identified ELONGATED HYPOCOTYL 5 as a key regulator limiting Cd accumulation and promoting tolerance, as hy5 mutants exhibited increased Cd sensitivity and accumulation. Additionally, mutants of genes regulated by HY5, such as xyloglucan endotransglucosylase/hydrolase genes (XTH) and MYB12, also showed altered root growth under Cd stress, implicating cell wall remodeling and flavonoid biosynthesis in Cd responses. This study provides a spatially and temporally resolved understanding of Cd’s impact on root growth, and highlights HY5’s role in Cd tolerance, thereby advancing our knowledge of plant responses to trace metal excess.

3. New Phytol

   Specific redox and iron homeostasis responses in the root tip of Arabidopsis upon zinc excess

   Noémie Thiébaut, Ludwig Richtmann, Manon Sarthou, Daniel P. Persson, Alok Ranjan, Marie Schloesser, Stéphanie Boutet, Lucas Rezende, Stephan Clemens, Nathalie Verbruggen, and Marc Hanikenne

   New Phytologist, May 2025

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   - Zinc (Zn) excess negatively impacts primary root growth in Arabidopsis thaliana. Yet, the effects of Zn excess on specific growth processes in the root tip (RT) remain largely unexplored.
   - Transcriptomics, ionomics, and metabolomics were used to examine the specific impact of Zn excess on the RT compared with the remaining root (RR).
   - Zn excess exposure resulted in a shortened root apical meristem and elongation zone, with differentiation initiating closer to the tip of the root. Zn accumulated at a lower concentration in the RT than in the RR. This pattern was associated with lower expression of Zn homeostasis and iron (Fe) deficiency response genes. A distinct distribution of Zn and Fe in RT and RR was highlighted by laser ablation inductively coupled plasma-mass spectrometry analysis. Specialized tryptophan (Trp)-derived metabolism genes, typically associated with redox and biotic stress responses, were specifically upregulated in the RT upon Zn excess, among those Phyotoalexin Deficient 3 (PAD3) encoding the last enzyme of camalexin synthesis. In the roots of wild-type seedlings, camalexin concentration increased by sixfold upon Zn excess, and a pad3 mutant displayed increased Zn sensitivity and an altered ionome.
   - Our results indicate that distinct redox and iron homeostasis mechanisms are key elements of the response to Zn excess in the RT.

2022

1. J. Hazard. Mater.

   Calcium-permeable cation channels are involved in uranium uptake in Arabidopsis thaliana

   Manon C.M. Sarthou, Fabienne Devime, Célia Baggio, Sylvie Figuet, Claude Alban, Jacques Bourguignon, and Stéphane Ravanel

   Journal of Hazardous Materials, May 2022

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   Uranium (U) is a non-essential and toxic element that is taken up by plants from the environment. The assimilation pathway of U is still unknown in plants. In this study, we provide several evidences that U is taken up by the roots of Arabidopsis thaliana through Ca2+-permeable cation channels. First, we showed that deprivation of Arabidopsis plants with calcium induces a 1.5-fold increase in the capacity of roots to accumulate U, suggesting that calcium deficiency promotes the radionuclide import pathway. Second, we showed that external calcium inhibits U accumulation in roots, suggesting a common route for the uptake of both cations. Third, we found that gadolinium, nifedipine and verapamil inhibit the absorption of U, suggesting that different types of Ca2+-permeable channels serve as a route for U uptake. Last, we showed that U bioaccumulation in Arabidopsis mutants deficient for the Ca2+-permeable channels MCA1 and ANN1 is decreased by 40%. This suggests that MCA1 and ANN1 contribute to the absorption of U in different zones and cell layers of the root. Together, our results describe for the first time the involvement of Ca2+-permeable cation channels in the cellular uptake of U.

2. PhD thesis

   Study of molecular mechanisms linked to uranium accumulation in Arabidopsis thaliana

   Manon Sarthou

   Mar 2022

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   Uranium is a naturally occurring radionuclide in the environment. Anthropogenic activities related to its exploitation are sources of environmental pollution. Exposure to this toxic element is detrimental to health because its accumulation in water and soil leads to contamination of the food chain, which is potentially hazardous for the population. It is therefore necessary to remediate these environments and to this end, the decontamination of contaminated areas can be achieved by using plants. Phytoremediation is based on the ability of plants to absorb pollutants, including metals. Thus, in order to use plants in phytoremediation and to optimise the technique, it is essential to understand the molecular processes involved in the accumulation of uranium. Uranium-stress interferes with plant biology at different levels: growth is inhibited, homeostasis of essential elements is modified, oxidative stress is generated, but the intracellular proteins that bind uranium or the proteins responsible for its transport are still unknown. In a first part of my PhD thesis, we developed a metalloproteomic approach to identify uranium-binding proteins in Arabidopsis thaliana cells. This approach is based on the chromatographic fractionation of the proteome and quantification of metals associated with the different protein fractions. This work led to the identification of several protein fractions containing uranium, demonstrating for the first time the existence of uranium-binding proteins in Arabidopsis. The continuation of this work allowed the biochemical and structural characterisation of two uranium-binding proteins. In a second step, we focused on the accumulation of uranium in A. thaliana roots, and more particularly on the import mechanisms of the radionuclide. We studied uranium accumulation in roots using a physiological approach based on the induction of essential element transporters during nutritional deficiency. This study allowed us to identify calcium channels as the main pathway for uranium uptake in roots. We then showed that the three calcium channels MCA1, MCA2 and ANN1 are involved in uranium uptake in roots. Finally, in a third part, we performed a genome-wide association study (GWAS) on uranium accumulation in roots and leaves of A. thaliana. By analysing these traits in 142 ecotypes, we were able to show that uranium accumulation in roots is probably not determined by a single strong gene, but by several genes and/or environmental factors. We also identified 34 genes that could be involved in the translocation of the metal from roots to leaves and/or its accumulation in leaves. Further characterisation of these genes should provide new insights into these processes, which are still poorly understood.

2020

1. Metallomics

   Development of a metalloproteomic approach to analyse the response of Arabidopsis cells to uranium stress

   Manon C.M. Sarthou, Benoît H Revel, Florent Villiers, Claude Alban, Titouan Bonnot, Océane Gigarel, Anne-Marie Boisson, Stéphane Ravanel, and Jacques Bourguignon

   Metallomics, Jun 2020

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   Uranium is a naturally occurring radionuclide that is absorbed by plants and interferes with many aspects of their physiology and development. In this study, we used an ionomic, metalloproteomic, and biochemical approach to gain insights into the impact of uranyl ions on the proteome of Arabidopsis thaliana cells. First, we showed that most of the U was trapped in the cell wall and only a small amount of the radionuclide was found in the cell-soluble fraction. Also, the homeostasis of several essential elements was significantly modified in the cells challenged with U. Second, the soluble proteome from Arabidopsis cells was fractionated into 10 subproteomes using anion-exchange chromatography. Proteomic analyses identified 3676 proteins in the different subproteomes and the metal-binding proteins were profiled using inductively coupled plasma mass spectrometry. Uranium was detected in several chromatographic fractions, indicating for the first time that several pools of Arabidopsis proteins are capable of binding the uranyl ion in vivo. Third, we showed that the pattern of some lysine and arginine methylated proteins was modified following exposure to U. We further identified that the ribosomal protein RPS10C was dimethylated at two arginine residues in response to uranyl ion stress. Together, these results provide the first clues for the impact of U on the Arabidopsis proteome and pave the way for the future identification of U-binding proteins.

2. Plant Cell Environ.

   Protein lysine methylation contributes to modulating the response of sensitive and tolerant Arabidopsis species to cadmium stress

   Nelson B. C. Serre, Manon Sarthou, Océane Gigarel, Sylvie Figuet, Massimiliano Corso, Justine Choulet, Valérie Rofidal, Claude Alban, Véronique Santoni, Jacques Bourguignon, Nathalie Verbruggen, and Stéphane Ravanel

   Plant, Cell & Environment, Jun 2020

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   Abstract The mechanisms underlying the response and adaptation of plants to excess of trace elements are not fully described. Here, we analysed the importance of protein lysine methylation for plants to cope with cadmium. We analysed the effect of cadmium on lysine-methylated proteins and protein lysine methyltransferases (KMTs) in two cadmium-sensitive species, Arabidopsis thaliana and A. lyrata, and in three populations of A. halleri with contrasting cadmium accumulation and tolerance traits. We showed that some proteins are differentially methylated at lysine residues in response to Cd and that a few genes coding KMTs are regulated by cadmium. Also, we showed that 9 out of 23 A. thaliana mutants disrupted in KMT genes have a tolerance to cadmium that is significantly different from that of wild-type seedlings. We further characterized two of these mutants, one was knocked out in the calmodulin lysine methyltransferase gene and displayed increased tolerance to cadmium, and the other was interrupted in a KMT gene of unknown function and showed a decreased capacity to cope with cadmium. Together, our results showed that lysine methylation of non-histone proteins is impacted by cadmium and that several methylation events are important for modulating the response of Arabidopsis plants to cadmium stress.