J Integr Plant Biol.

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Role of the tomato MARS1/ROUGH gene encoding a LYSINE‐SPECIFIC HISTONE DEMETHYLASE 1 in adventitious root and fruit skin formation

Eduardo Larriba1, Cécile Bres2,3, Aurora Alaguero-Cordovilla1, Riyazuddin Riyazuddin1†, Qingyi Wang4†, Johann Petit2†, Jean-Philippe Mauxion2, Lara Caballero1, David Latrasse4, Bénédicte Bakan5, Rim Brik-Chaouche4, David Esteve-Bruna1, Moussa Benhamed4, Christophe Rothan2 and José Manuel Pérez-Pérez1*   

  1. 1. Instituto de Bioingeniería, Universidad Miguel Hernández, Elche 03202, Spain
    2. UMR 1332 Biologie du Fruit et Pathologie, INRAE, University of Bordeaux, Villenave d'Ornon F33882, France
    3. UMR 1391 Interactions Sol Plante Atmosphère, INRAE, Bordeaux Sciences Agro, Villenave‐d'Ornon F33882, France
    4. Institute of Plant Sciences Paris‐Saclay (IPS2), Université Paris‐Saclay, CNRS, INRAE, Université Evry, Orsay 91405, France
    5. Unité Biopolymères, Interactions, Assemblages, INRAE, Nantes 44316, France
    These authors contributed equally to this work.
    *Correspondence: José Manuel Pérez‐Pérez (jmperez@umh.es)
  • Received:2025-08-29 Accepted:2026-04-14 Online:2026-05-15
  • Supported by:
    This research is supported by grants PID2021‐ 126840OB‐I00 and PID2024‐160653NB‐I00 funded by MCIN/ AEI/10.13039/501100011033, and by the “ERDF A way of making Europe”. R.R. and L.C. hold a postdoctoral contract (CIAPOS/2023/138) and “Programa INVESTIGO” contract (INVEST/2022/247) from the Generalitat Valenciana, respectively.

Abstract: In contrast to animals, plants possess a remarkable regenerative capacity and are capable of forming new organs or even entire organisms from a limited number of cells present in adult tissues, in response to injury or environmental changes. In this study, we describe the isolation and characterization of the more adventitious roots1-1 (mars1-1) mutant, which exhibits enhanced regenerative potential upon wounding in tomato hypocotyl explants. Additionally, the mars1-1 fruits exhibited a rough surface because of ectopic subepidermal cell proliferation, resulting in the formation of callus-like structures on their cuticle. The MARS1/ROUGH gene encodes a conserved lysine-specific histone demethylase, SlLDL1, which regulates processes such as cell proliferation, stem cell pluripotency, and embryogenesis in metazoans. Two CRISPR/Cas9 null alleles, mars1-2 and mars1-3, were generated, and their pleiotropic phenotypes were characterized. ChIP-seq analysis revealed elevated levels of methylated lysine 4 in histone 3 within specific regions of the mars1/rough genome. To determine the impact of altered epigenetic marks on gene expression regulation in mars1/rough mutants, we analyzed the transcriptome of tomato hypocotyls during adventitious root formation. Using specific bioinformatic workflows and the resolution of the directional RNA-seq data, we identified several dozen distinct genomic regions with de novo expression in the mars1/rough mutants. One such region includes a novel B-type cyclin gene that is upregulated in mars1/rough mutants and may account for adventitious root and fruit skin phenotypes. Our findings indicate that SlLDL1 plays a role in maintaining silencing in specific genomic regions that are essential for tissue-specific reprogramming.

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