An auxin signaling network translates low-sugar-state input into compensated cell enlargement in the fugu5 cotyledon

PLoS Genet. 2021 Aug 5;17(8):e1009674. doi: 10.1371/journal.pgen.1009674. eCollection 2021 Aug.


In plants, the effective mobilization of seed nutrient reserves is crucial during germination and for seedling establishment. The Arabidopsis H+-PPase-loss-of-function fugu5 mutants exhibit a reduced number of cells in the cotyledons. This leads to enhanced post-mitotic cell expansion, also known as compensated cell enlargement (CCE). While decreased cell numbers have been ascribed to reduced gluconeogenesis from triacylglycerol, the molecular mechanisms underlying CCE remain ill-known. Given the role of indole 3-butyric acid (IBA) in cotyledon development, and because CCE in fugu5 is specifically and completely cancelled by ech2, which shows defective IBA-to-indoleacetic acid (IAA) conversion, IBA has emerged as a potential regulator of CCE. Here, to further illuminate the regulatory role of IBA in CCE, we used a series of high-order mutants that harbored a specific defect in IBA-to-IAA conversion, IBA efflux, IAA signaling, or vacuolar type H+-ATPase (V-ATPase) activity and analyzed the genetic interaction with fugu5-1. We found that while CCE in fugu5 was promoted by IBA, defects in IBA-to-IAA conversion, IAA response, or the V-ATPase activity alone cancelled CCE. Consistently, endogenous IAA in fugu5 reached a level 2.2-fold higher than the WT in 1-week-old seedlings. Finally, the above findings were validated in icl-2, mls-2, pck1-2 and ibr10 mutants, in which CCE was triggered by low sugar contents. This provides a scenario in which following seed germination, the low-sugar-state triggers IAA synthesis, leading to CCE through the activation of the V-ATPase. These findings illustrate how fine-tuning cell and organ size regulation depend on interplays between metabolism and IAA levels in plants.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / drug effects
  • Arabidopsis Proteins / genetics
  • Cell Enlargement / drug effects
  • Cotyledon / drug effects
  • Cotyledon / genetics
  • Cotyledon / physiology
  • Enoyl-CoA Hydratase / genetics
  • Germination
  • Indoleacetic Acids / metabolism*
  • Indoles / pharmacology*
  • Inorganic Pyrophosphatase / genetics*
  • Loss of Function Mutation
  • Organ Size
  • Signal Transduction / drug effects
  • Sugars / metabolism
  • Vacuolar Proton-Translocating ATPases / genetics*


  • Arabidopsis Proteins
  • Indoleacetic Acids
  • Indoles
  • Sugars
  • indolebutyric acid
  • Vacuolar Proton-Translocating ATPases
  • Inorganic Pyrophosphatase
  • ECH2 protein, Arabidopsis
  • Enoyl-CoA Hydratase

Grant support

This work was supported by Grant-in-Aid for Scientific Research (B) (16H04803 to A.F.); Grant-in-Aid for Scientific Research on Innovative Areas (25113002 to H.Ts. and A.F.; 25113010 to M.Y.H.); Grant-in-Aid for Scientific Research on Innovative Areas (18H05487 to A.F.); Grant-in-Aid for Scientific Research on Innovative Areas (19H05672 to H.Ts.); and The Naito Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.