PHABULOSA controls the quiescent center-independent root meristem activities in Arabidopsis thaliana

PLoS Genet. 2015 Mar 2;11(3):e1004973. doi: 10.1371/journal.pgen.1004973. eCollection 2015 Mar.

Abstract

Plant growth depends on stem cell niches in meristems. In the root apical meristem, the quiescent center (QC) cells form a niche together with the surrounding stem cells. Stem cells produce daughter cells that are displaced into a transit-amplifying (TA) domain of the root meristem. TA cells divide several times to provide cells for growth. SHORTROOT (SHR) and SCARECROW (SCR) are key regulators of the stem cell niche. Cytokinin controls TA cell activities in a dose-dependent manner. Although the regulatory programs in each compartment of the root meristem have been identified, it is still unclear how they coordinate one another. Here, we investigate how PHABULOSA (PHB), under the posttranscriptional control of SHR and SCR, regulates TA cell activities. The root meristem and growth defects in shr or scr mutants were significantly recovered in the shr phb or scr phb double mutant, respectively. This rescue in root growth occurs in the absence of a QC. Conversely, when the modified PHB, which is highly resistant to microRNA, was expressed throughout the stele of the wild-type root meristem, root growth became very similar to that observed in the shr; however, the identity of the QC was unaffected. Interestingly, a moderate increase in PHB resulted in a root meristem phenotype similar to that observed following the application of high levels of cytokinin. Our protoplast assay and transgenic approach using ARR10 suggest that the depletion of TA cells by high PHB in the stele occurs via the repression of B-ARR activities. This regulatory mechanism seems to help to maintain the cytokinin homeostasis in the meristem. Taken together, our study suggests that PHB can dynamically regulate TA cell activities in a QC-independent manner, and that the SHR-PHB pathway enables a robust root growth system by coordinating the stem cell niche and TA domain.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / growth & development
  • Arabidopsis Proteins / biosynthesis
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Cell Division / genetics
  • Cytokinins / genetics
  • Cytokinins / metabolism
  • DNA-Binding Proteins / genetics
  • Gene Expression Regulation, Plant
  • Homeodomain Proteins / biosynthesis
  • Homeodomain Proteins / genetics*
  • Homeostasis
  • Meristem / genetics*
  • Meristem / growth & development
  • Phenotype
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plants, Genetically Modified / growth & development
  • Stem Cell Niche / genetics*
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • ARR10 protein, Arabidopsis
  • Arabidopsis Proteins
  • Cytokinins
  • DNA-Binding Proteins
  • Homeodomain Proteins
  • PHB protein, Arabidopsis
  • SCR protein, Arabidopsis
  • SHORT ROOT protein, Arabidopsis
  • Transcription Factors

Grant support

This work was supported by National Science Foundation (IOS-0818071, www.nsf.gov), Triad Foundation, National Research Foundation of Korea (2013R1A1A3009272, www.nrf.re.kr/nrf_eng_cms), and Seoul National University Research grants to JYL and Ministry of Education, Youth and Sports of the Czech Republic (MSM 6198959216) and ED0007/01/01 Centre of the Region Haná for Biotechnological and Agricultural Research grants to PT. KHR and ESK are supported by Brain Korea 21 Plus Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.