# Brassinazole resistant 1 (BZR1)-dependent brassinosteroid signalling pathway leads to ectopic activation of quiescent cell division and suppresses columella stem cell differentiation

**Authors:** Hak-Soo Lee, Yoon Kim, Giang Pham, Ju Won Kim, Ji-Hye Song, Yew Lee, Yong-Sic Hwang, Stanley J. Roux, Soo-Hwan Kim

PMC · DOI: 10.1093/jxb/erv316 · Journal of Experimental Botany · 2015-07-01

## TL;DR

This study shows how brassinosteroids affect root cell division and differentiation in plants through the BZR1 protein, with opposite effects on different cell types.

## Contribution

The paper reveals that BZR1 promotes quiescent center division but suppresses columella stem cell differentiation, contrasting with BES1.

## Key findings

- BZR1 promotes quiescent center cell divisions in Arabidopsis roots.
- BZR1 suppresses differentiation of columella stem cells, opposite to BES1.
- BR signaling alters PIN protein distribution, affecting auxin movement.

## Abstract

Brassinosteroids (BRs) lead to ectopic activation of quiescent centre division as well as modulation of the columella stem cells differentiation in Arabidopsis roots in a BR concentration- and BZR1-/BES1-dependent manner.

Previous publications have shown that BRI1 EMS suppressor 1 (BES1), a positive regulator of the brassinosteroid (BR) signalling pathway, enhances cell divisions in the quiescent centre (QC) and stimulates columella stem cell differentiation. Here, it is demonstrated that BZR1, a BES1 homologue, also promotes cell divisions in the QC, but it suppresses columella stem cell differentiation, opposite to the action of BES1. In addition, BR and its BZR1-mediated signalling pathway are shown to alter the expression/subcellular distribution of pin-formed (PINs), which may result in changes in auxin movement. BR promotes intense nuclear accumulation of BZR1 in the root tip area, and the binding of BZR1 to the promoters of several root development-regulating genes, modulating their expression in the root stem cell niche area. These BZR1-mediated signalling cascades may account for both the ectopic activation of QC cell divisions as well as the suppression of the columella stem cell differentiation. They could also inhibit auxin-dependent distal stem cell differentiation by antagonizing the auxin/WOX5-dependent pathway. In conclusion, BZR1-/BES1-mediated BR signalling pathways show differential effects on the maintenance of root apical meristem activities: they stimulate ectopic QC division while they show opposite effects on the differentiation of distal columella stem cells in a BR concentration- and BZR1-/BES1-dependent manner.

## Linked entities

- **Genes:** BZR1 (Brassinosteroid signaling positive regulator (BZR1) family protein) [NCBI Gene 843845], BES1 (Brassinosteroid signaling positive regulator (BZR1) family protein) [NCBI Gene 838518], GPSM2 (G protein signaling modulator 2) [NCBI Gene 29899], WOX5 (WUSCHEL related homeobox 5) [NCBI Gene 820297]
- **Chemicals:** brassinosteroids (PubChem CID 13039058), BR (PubChem CID 259)
- **Species:** Arabidopsis (taxon 3701)

## Full-text entities

- **Genes:** PP2A (serine/threonine protein phosphatase 2A) [NCBI Gene 843333] {aka F20P5.30, F20P5_30, TYPE 2A SERINE/THREONINE PROTEIN PHOSPHATASE, serine/threonine protein phosphatase 2A}, BZR1 (Brassinosteroid signaling positive regulator (BZR1) family protein) [NCBI Gene 843845] {aka BRASSINAZOLE-RESISTANT 1, F9E10.7, F9E10_7}, NAC070 (NAC domain containing protein 70) [NCBI Gene 826627] {aka ANAC070, BEARSKIN 2, BRN2, F24G24.150, F24G24_150, NAC domain containing protein 70}, UBC30 (ubiquitin-conjugating enzyme 30) [NCBI Gene 835714] {aka MDA7.21, MDA7_21, ubiquitin-conjugating enzyme 30}, WOX5 (WUSCHEL related homeobox 5) [NCBI Gene 820297] {aka WOX5B, WUSCHEL related homeobox 5, WUSCHEL related homeobox 5B}, PIN1 (Auxin efflux carrier family protein) [NCBI Gene 843693] {aka ARABIDOPSIS THALIANA PIN-FORMED 1, ATPIN1, F6D5.2, F6D5_2, PIN-FORMED 1}, BIN2 (Protein kinase superfamily protein) [NCBI Gene 827605] {aka ATSK21, BRASSINOSTEROID-INSENSITIVE 2, DWARF 12, DWF12, F28A21.120, F28A21_120}, SMB (NAC (No Apical Meristem) domain transcriptional regulator superfamily protein) [NCBI Gene 844296] {aka ANAC033, Arabidopsis NAC domain containing protein 33, F20B17.1, F20B17_1, SOMBRERO, UAS-TAGGED ROOT PATTERNING7}, BES1 (Brassinosteroid signaling positive regulator (BZR1) family protein) [NCBI Gene 838518] {aka 107 PROTEIN, BRASSINAZOLE-RESISTANT 2, BRI1-EMS-SUPPRESSOR 1, BZR2, F18O14.7, F18O14_7}, CUL3 (cullin 3) [NCBI Gene 839226] {aka ATCUL3, ATCUL3A, CUL3A, T24P13.25, cullin 3, cullin 3A}, NAC015 (NAC domain containing protein 15) [NCBI Gene 840223] {aka ANAC015, BEARSKIN 1, BRN1, NAC domain containing protein 15, T16O9.16, T16O9_16}, ARF [NCBI Gene 107770727], SCR (GRAS family transcription factor) [NCBI Gene 824589] {aka SCARECROW, SGR1, SHOOT GRAVITROPISM 1}, CPD (Cytochrome P450 superfamily protein) [NCBI Gene 830453] {aka CABBAGE 3, CBB3, CONSTITUTIVE PHOTOMORPHOGENIC DWARF, CYP90, CYP90A, CYP90A1}, PID (Protein kinase superfamily protein) [NCBI Gene 818030] {aka ABR, ABRUPTUS, PINOID, PROTEIN KINASE PINOID, T31E10.1, T31E10_1}, BRI1 (Leucine-rich receptor-like protein kinase family protein) [NCBI Gene 830095] {aka ATBRI1, BIN1, BR INSENSITIVE 1, BRASSINOSTEROID INSENSITIVE 1, CABBAGE 2, CBB2}, FEZ (NAC (No Apical Meristem) domain transcriptional regulator superfamily protein) [NCBI Gene 837796] {aka ANAC009, Arabidopsis NAC domain containing protein 9, T2P11.6, T2P11_6}, PIN3 (Auxin efflux carrier family protein) [NCBI Gene 843432] {aka ARABIDOPSIS PIN-FORMED 3, ATPIN3, F15H11.14, F15H11_14, PIN-FORMED 3}, AT5G07310 (Integrase-type DNA-binding superfamily protein) [NCBI Gene 830622] {aka ERF115, ETHYLENE RESPONSE FACTOR 115, T2I1.20, T2I1_20}, PP2A-2 (protein phosphatase 2A-2) [NCBI Gene 837583] {aka PROTEIN PHOSPHATASE 2A, T10O24.4, T10O24_4, protein phosphatase 2A-2}, PIN4 (Auxin efflux carrier family protein) [NCBI Gene 814670] {aka ARABIDOPSIS PIN-FORMED 4, ATPIN4, AUXIN TRANSPORTER SPLICE VARIANT B, F10A8.27, PIN-FORMED 4}, MYB56 (myb domain protein 56) [NCBI Gene 831648] {aka AtMYB56, BRASSINOSTEROIDS AT VASCULAR AND ORGANIZING CENTER, BRAVO, MVA3.150, MVA3_150, myb domain protein 56}, DWF4 (Cytochrome P450 superfamily protein) [NCBI Gene 824229] {aka AtDWF4, CLM, CLOMAZONE-RESISTANT, CYP90B1, CYTOCHROME P450 90B1, DWARF 4}, UBC1 (ubiquitin carrier protein 1) [NCBI Gene 838002] {aka ATUBC1, F14L17.17, F14L17_17, UBIQUITIN CARRIER PROTEIN 1, UBIQUITIN CONJUGATING ENZYME 1, ubiquitin carrier protein 1}, ARF10 (auxin response factor 10) [NCBI Gene 817382] {aka T1B3.13, T1B3_13, auxin response factor 10}, SNRK2.2 (SNF1-related protein kinase 2.2) [NCBI Gene 824214] {aka PROTEIN KINASE, SNF1-RELATED PROTEIN KINASE 2-2, SNF1-related protein kinase 2.2, SNRK2-2, SPK-2-2, SRK2D}, ARF16 (auxin response factor 16) [NCBI Gene 829131] {aka F6G3.110, F6G3_110, auxin response factor 16}, EIR1 (Auxin efflux carrier family protein) [NCBI Gene 835813] {aka AGR, AGR1, AGRAVITROPIC ROOT, AGRAVITROPIC ROOT 1, ARABIDOPSIS THALIANA PIN-FORMED 2, ATPIN2}, PIN7 (Auxin efflux carrier family protein) [NCBI Gene 838916] {aka ARABIDOPSIS PIN-FORMED 7, ATPIN7, PIN-FORMED 7, T26J12.14, T26J12_14}, BRL1 (BRI1 like) [NCBI Gene 842010] {aka BRI1 like, F20N2.4}, BRL3 (BRI1-like 3) [NCBI Gene 820538] {aka BRI1-like 3}, HTB9 (Histone superfamily protein) [NCBI Gene 823741] {aka H2B, HISTONE 2B, HISTONE H2B}, ACS5 (ACC synthase 5) [NCBI Gene 836709] {aka 1-AMINO-1-CYCLOPROPANECARBOXYLATE SYNTHASE, ACC synthase 5, ATACS5, CIN5, CYTOKININ-INSENSITIVE 5, ETHYLENE OVERPRODUCER 2}, SHR (GRAS family transcription factor) [NCBI Gene 829919] {aka F19F18.140, F19F18_140, SGR7, SHOOT GRAVITROPISM 7, SHORT ROOT}, ETO1 (tetratricopeptide repeat (TPR)-containing protein) [NCBI Gene 824340] {aka ARABIDOPSIS ETHYLENE OVERPRODUCER 1, ATEOL1, ETHYLENE OVERPRODUCER 1, ETHYLENE OVERPRODUCER1}, BAK1 (BRI1-associated receptor kinase) [NCBI Gene 829480] {aka ATBAK1, ATSERK3, BRI1-associated receptor kinase, ELG, ELONGATED, F17M5.190}
- **Diseases:** CC (MESH:D002292), swelling (MESH:D004487), hypophysis (MESH:D004393)
- **Chemicals:** phosphate (MESH:D010710), Auxin (MESH:D007210), HCl (MESH:D006851), SYBR green (MESH:C098022), EtOH (MESH:D000431), bikinin (MESH:C543414), ethylene (MESH:C036216), agar (MESH:D000362), BR (MESH:D060406), Ne (MESH:D009356), BR (MESH:D001966), glycerol (MESH:D005990), periodic acid (MESH:D010504), 1-naphthaleneacetic acid (MESH:C034182), Aux (-), PI (MESH:D010716), CoCl2 (MESH:C018021), steroid hormones (MESH:D013256), ABA (MESH:D000040), formaldehyde (MESH:D005557), chloral hydrate (MESH:D002697), He (MESH:D006371), AgNO3 (MESH:D012835), Brassinazole (MESH:C412342), H2O (MESH:D014867), acetic acid (MESH:D019342), Triton X-100 (MESH:D017830), propidium iodide (MESH:D011419), acetone (MESH:D000096), ACC (MESH:C023863), sodium metabisulphite (MESH:C005200), argon (MESH:D001128), BK (MESH:D001603), methanol (MESH:D000432), AVG (MESH:C088137), starch (MESH:D013213), Brassinolide (MESH:C023623), EDTA (MESH:D004492),  (MESH:D014230)
- **Species:** Arabidopsis thaliana (mouse-ear cress, species) [taxon 3702], Nicotiana tabacum (American tobacco, species) [taxon 4097]
- **Cell lines:** p35S::BES1 — Mus musculus (Mouse), Mouse erythroid leukemia, Cancer cell line (CVCL_WN68), En-2 — Felis catus (Cat), Finite cell line (CVCL_S220), D — Drosophila melanogaster (Fruit fly), Spontaneously immortalized cell line (CVCL_IZ09), bzr1-D — Homo sapiens (Human), Induced pluripotent stem cell (CVCL_RG58), Col-0 — Homo sapiens (Human), Familial hypertrophic cardiomyopathy type 26, Induced pluripotent stem cell (CVCL_A6XE), S2 — Drosophila melanogaster (Fruit fly), Spontaneously immortalized cell line (CVCL_Z232)

## Full text

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## Figures

6 figures with captions in the complete paper: https://tomesphere.com/paper/PMC4507784/full.md

## References

61 references — full list in the complete paper: https://tomesphere.com/paper/PMC4507784/full.md

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Source: https://tomesphere.com/paper/PMC4507784