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Peer-reviewedCC BY-NC 4.0Journal of Integrative Plant Biology

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

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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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BibTeX
@article{larriba2026role,
  title = {{Role of the tomato MARS1/ROUGH gene encoding a LYSINE‐SPECIFIC HISTONE DEMETHYLASE 1 in adventitious root and fruit skin formation}},
  author = {Eduardo Larriba and Cécile Bres and Aurora Alaguero-Cordovilla and Riyazuddin Riyazuddin and Qingyi Wang and Johann Petit and Jean‐philippe Mauxion and Lara Caballero and David Latrasse and Bénédicte Bakan and Rim Brik-Chaouche and David Esteve-Bruna and Moussa Benhamed and Christophe Rothan and José Manuel Pérez-Pérez},
  journal = {Journal of Integrative Plant Biology},
  year = {2026},
  month = may,
  doi = {10.1111/jipb.70287},
  url = {https://hal.science/hal-05624522v1},
  note = {CC BY-NC 4.0},
}
RIS
TY  - JOUR
TI  - Role of the tomato MARS1/ROUGH gene encoding a LYSINE‐SPECIFIC HISTONE DEMETHYLASE 1 in adventitious root and fruit skin formation
AU  - Eduardo Larriba
AU  - Cécile Bres
AU  - Aurora Alaguero-Cordovilla
AU  - Riyazuddin Riyazuddin
AU  - Qingyi Wang
AU  - Johann Petit
AU  - Jean‐philippe Mauxion
AU  - Lara Caballero
AU  - David Latrasse
AU  - Bénédicte Bakan
AU  - Rim Brik-Chaouche
AU  - David Esteve-Bruna
AU  - Moussa Benhamed
AU  - Christophe Rothan
AU  - José Manuel Pérez-Pérez
PY  - 2026
DA  - 2026/05/15
JO  - Journal of Integrative Plant Biology
DO  - 10.1111/jipb.70287
UR  - https://hal.science/hal-05624522v1
AB  - 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.
SN  - 1672-9072
ER  -