A dynamic WUSCHEL/Layer 1 interplay directs shoot apical meristem formation during regeneration in tobacco

Manoj Kumar, Dana Ayzenshtat, Gulzar A. Rather, Hanita Zemach, Eduard Belausov, Leor Eshed Williams, Samuel Bocobza*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

De novo shoot apical meristem (SAM) organogenesis during regeneration in tissue culture has been investigated for several decades, but the precise mechanisms governing early-stage cell fate specification remain elusive. In contrast to SAM establishment during embryogenesis, in vitro SAM formation occurs without positional cues and is characterized by autonomous initiation of cellular patterning. Here, we report on the initial stages of SAM organogenesis and on the molecular mechanisms that orchestrate gene patterning to establish SAM homeostasis. We found that SAM organogenesis in tobacco calli starts with protuberance formation followed by the formation of an intact L1 layer covering the nascent protuberance. We also exposed a complex interdependent relationship between L1 and WUS expression and revealed that any disruption in this interplay compromises shoot formation. Silencing WUS in nascent protuberances prevented L1 formation and caused the disorganization of the outer cell layers exhibiting both anticlinal and periclinal divisions, suggesting WUS plays a critical role in the proper establishment and organization of L1 during SAM organogenesis. We further discovered that silencing TONNEAU1 prevents the exclusive occurrence of anticlinal divisions in the outermost layer of the protuberances and suppresses the acquisition of L1 cellular identity and L1 formation, ultimately impeding SAM formation and regeneration. This study provides a novel molecular framework for the characterization of a WUS/L1 interplay that mediates SAM formation during regeneration.

Original languageEnglish
Pages (from-to)578-597
Number of pages20
JournalPlant Journal
Volume120
Issue number2
DOIs
StatePublished - Oct 2024

Bibliographical note

Publisher Copyright:
© 2024 Society for Experimental Biology and John Wiley & Sons Ltd.

Keywords

  • LONELY GUY4 (LOG4)
  • MERISTEM LAYER1 (ML1)
  • TONNEAU1 (TON1)
  • WUSCHEL (WUS)
  • epidermal cell differentiation
  • meristem formation
  • morphogenesis
  • shoot apical meristem

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