Multi‐scale mechanisms driving root regeneration: From regeneration competence to tissue repatterning

• Published in: The Plant journal : for cell and molecular biology Vol. 119; no. 3; pp. 1183 - 1196
• Main Authors: García‐Gómez, Monica L., Tusscher, Kirsten
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.08.2024
• Subjects: Arabidopsis thaliana; Cell fate; cell fate transitions; cell reprogramming; Chemical synthesis; Damage localization; Environmental conditions; Gene expression; Gene Expression Regulation, Plant; Hormones; Mechanical properties; Meristem - genetics; Meristem - physiology; Organ removal; Plant Growth Regulators - metabolism; Plant Roots - growth & development; Plant Roots - physiology; Regeneration; Regeneration - physiology; Regulatory sequences; root development; Sessile species; Signal Transduction; Stem cells; Temporal variations; Transcription factors; wound signaling; Arabidopsis thaliana; wound signaling; cell reprogramming; root development; cell fate transitions; regeneration
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16860

SUMMARY Plants possess an outstanding capacity to regenerate enabling them to repair damages caused by suboptimal environmental conditions, biotic attacks, or mechanical damages impacting the survival of these sessile organisms. Although the extent of regeneration varies greatly between localized cell damage and whole organ recovery, the process of regeneration can be subdivided into a similar sequence of interlinked regulatory processes. That is, competence to regenerate, cell fate reprogramming, and the repatterning of the tissue. Here, using root tip regeneration as a paradigm system to study plant regeneration, we provide a synthesis of the molecular responses that underlie both regeneration competence and the repatterning of the root stump. Regarding regeneration competence, we discuss the role of wound signaling, hormone responses and synthesis, and rapid changes in gene expression observed in the cells close to the cut. Then, we consider how this rapid response is followed by the tissue repatterning phase, where cells experience cell fate changes in a spatial and temporal order to recreate the lost stem cell niche and columella. Lastly, we argue that a multi‐scale modeling approach is fundamental to uncovering the mechanisms underlying root regeneration, as it allows to integrate knowledge of cell‐level gene expression, cell‐to‐cell transport of hormones and transcription factors, and tissue‐level growth dynamics to reveal how the bi‐directional feedbacks between these processes enable self‐organized repatterning of the root apex. Significance Statement This review proposes a conceptual model of the molecular mechanisms underlying root tip regeneration, from regeneration competence to the spatio‐temporal repatterning of the root stump. We also discuss the use of multi‐scale modeling to address open questions in the field.