A SCARECROW-RETINOBLASTOMA Protein Network Controls Protective Quiescence in the Arabidopsis Root Stem Cell Organizer

Alfredo Cruz-Ramírez,Mario Arteága-Vázquez,Ikram Blilou,Yujuan Du,Ben Scheres,Rene Benjamins,Sara Díaz-Triviño,Hongtao Zhang,Anne B Neef,Guy Wachsman,Vicki Chandler,Mark Estelle

doi:10.1371/journal.pbio.1001724

Alfredo Cruz-Ramírez, Mario Arteága-Vázquez + Show 10 more

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https://doi.org/10.1371/journal.pbio.1001724

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Abstract

Author SummaryIn the plant Arabidposis thaliana, root meristems (in the growing tip of the root) contain slowly dividing cells that act as an organizing center for the root stem cells that surround them. This centre is called the quiescent centre (QC). In this study, we show that the slow rate of division in the QC is regulated by the interaction between two proteins: Retinoblastoma homolog (RBR) and SCARECROW (SCR), a transcription factor that controls stem cell maintenance. RBR and SCR regulate quiescence in the QC by repressing an asymmetric cell division that generates short-term stem cells. Here we genetically manipulate the cells in the QC to alter their quiescence by regulating the RBR/SCR interaction to demonstrate that quiescence is not needed for the organizing capacity of the QC but instead provides cells with a higher resistance to genotoxic stress, allowing stem cells in the QC to survive even if more rapidly cycling stem cells are damaged. A role for mitotic quiescence has been reported in animal stem cells, in which Rb has been implicated. These findings indicate that it might serve a similar role in plant stem cells.

Highlights

The development of multicellular organisms depends on the ability of stem cells to self-renew and to generate new cellular progeny
We show that the slow rate of division in the quiescent centre (QC) is regulated by the interaction between two proteins: Retinoblastoma homolog (RBR) and SCARECROW (SCR), a transcription factor that controls stem cell maintenance
We genetically manipulate the cells in the QC to alter their quiescence by regulating the RBR/SCR interaction to demonstrate that quiescence is not needed for the organizing capacity of the QC but instead provides cells with a higher resistance to genotoxic stress, allowing stem cells in the QC to survive even if more rapidly cycling stem cells are damaged

Summary

Introduction

The development of multicellular organisms depends on the ability of stem cells to self-renew and to generate new cellular progeny. There were no evident effects on stem cell niche activity and organization in 25 dpg pWOX5::amiGORBR or pSCR::SCRAxCxA:YFP; scr-4 roots (Figure 5A–C). These observations demonstrate that quiescence of the organizing cells is not strictly necessary for function or structural integrity of the niche over this time span, and that the shootward daughter after ACD retains full QC function in its continued ability to maintain the stem cell niche. In plants the pathways do not seem to be additive as in mammalian cells, because hydroxyurea treatment of pWOX5::amiGORBR has no effect in QC division frequency. WT-24 hpz WT-48 hpz WT-72 hpz pWOX5:amiGO-24 hpz pWOX5:amiGO-48 hpz pWOX5:amiGO-72 hpz pSCR::SCRAxCxA:YFP-24 hpz pSCR::SCRAxCxA:YFP-48 hpz pSCR::SCRAxCxA:YFP-72 hpz doi:10.1371/journal.pbio.1001724.t003

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