Paracrine brassinosteroid signaling at the stem cell niche controls cellular regeneration

Abstract

Stem cell regeneration is crucial for both cell turnover and tissue healing in multicellular organisms. In Arabidopsis roots, a reduced group of cells known as the quiescent center (QC) act as a cell reservoir for surrounding stem cells during both normal growth and in response to external damage. Although cells of the QC have a very low mitotic activity, plant hormones such as brassinosteroids (BRs) can promote QC divisions. Here, we used a tissue-specific strategy to investigate the spatial signaling requirements of BR-mediated QC divisions. We generated stem cell niche-specific receptor knockout lines by placing an artificial microRNA against BRI1 (BRASSINOSTEROID INSENSITIVE 1) under the control of the QC-specific promoter WOX5. Additionally, QC-specific knock-in lines for BRI1 and its downstream transcription factor BES1 (BRI1-EMS-SUPPRESOR1) were also created using the WOX5 promoter. By analyzing the roots of these lines, we show that BES1-mediated signaling cell-autonomously promotes QC divisions, that BRI1 is essential for sensing nearby inputs and triggering QC divisions and that DNA damage promotes BR-dependent paracrine signaling in the stem cell niche as a prerequisite to stem cell replenishment.

Integrated omics networks reveal the temporal signaling events of brassinosteroid response inArabidopsis

“…We found that cyclin genes, specifically CYCD3;1 and CYCP4;1, are induced by BL and repressed by BRON, suggesting that BR induces these cyclins through its repression of BRON ( Fig 5C). These results are supported by multiple studies which elucidate the role of CYCD3;1 in BR-induced cell division (14,19) and describe how BR specifically induces QC division in the root (14,30,53…”

“…We found that anl2 mutant roots shorten more than WT when treated with BL, demonstrating that the anl2 mutants are hypersensitive to BL (Fig S4, Table S2). It has also been shown that BL can induce excessive QC divisions in the root (14,30,53). Thus, we checked the anl2 mutant roots for QC divisions as a secondary BR response phenotype: however, we found that anl2 mutant roots do not display excessive QC divisions ( Fig S4).…”

Overexpression of the vascular brassinosteroid receptor BRL3 confers drought resistance without penalizing plant growth

“…We suggest that this is accomplished through the transcriptional control of metabolic pathways that produce osmoprotectant metabolites that accumulate in the roots. While spatial BR signaling has been shown to contribute to stem cell replenishment in response to genotoxic stress 31 , 34 , here we show that ectopic expression of vascular-enriched BRL3 receptors can promote growth during drought. Altogether, our results suggest that spatial regulation of BR signaling can affect plant stress responses.…”

“…Recently, greater attention is being placed on the spatial regulation of hormonal signaling pathways in attempt to further understand the coordination of plant growth and stress responses 26 , 31 – 34 . For instance, while the BRI1 receptor is widely localized in many tissues 35 , the BRI1-LIKE receptor homologs BRL1 and BRL3 signal from the innermost tissues of the plant and thereby contribute to vascular development 12 , 33 , 36 .…”

Precise transcriptional control of cellular quiescence by BRAVO/WOX5 complex in Arabidopsis roots

“…The QC prevents differentiation of the surrounding stem cells (van den Berg et al, 1997), and its low proliferation rate provides a way to preserve the genome from replication errors. It also acts as a root stem cells reservoir, having the ability of promoting its own division rate to replenish the stem cells when they are damaged (Fulcher & Sablowski, 2009;Lozano-Elena et al, 2018).…”