Lateral Inhibition by a Peptide Hormone-Receptor Cascade during Arabidopsis Lateral Root Founder Cell Formation

In plants, the position of lateral roots (LRs) depends on initiation sites induced by auxin. The domain of high auxin response responsible for LR initiation stretches over several cells, but only a pair of pericycle cells (LR founder cells) will develop into LRs. In this work, we identified a signal...

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Veröffentlicht in:Developmental cell 2019-01, Vol.48 (1), p.64-75.e5
Hauptverfasser: Toyokura, Koichi, Goh, Tatsuaki, Shinohara, Hidefumi, Shinoda, Akinori, Kondo, Yuki, Okamoto, Yoshie, Uehara, Takeo, Fujimoto, Koichi, Okushima, Yoko, Ikeyama, Yoshifumi, Nakajima, Keiji, Mimura, Tetsuro, Tasaka, Masao, Matsubayashi, Yoshikatsu, Fukaki, Hidehiro
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container_end_page 75.e5
container_issue 1
container_start_page 64
container_title Developmental cell
container_volume 48
creator Toyokura, Koichi
Goh, Tatsuaki
Shinohara, Hidefumi
Shinoda, Akinori
Kondo, Yuki
Okamoto, Yoshie
Uehara, Takeo
Fujimoto, Koichi
Okushima, Yoko
Ikeyama, Yoshifumi
Nakajima, Keiji
Mimura, Tetsuro
Tasaka, Masao
Matsubayashi, Yoshikatsu
Fukaki, Hidehiro
description In plants, the position of lateral roots (LRs) depends on initiation sites induced by auxin. The domain of high auxin response responsible for LR initiation stretches over several cells, but only a pair of pericycle cells (LR founder cells) will develop into LRs. In this work, we identified a signaling cascade controlling LR formation through lateral inhibition. It comprises a peptide hormone TARGET OF LBD SIXTEEN 2 (TOLS2), its receptor RLK7, and a downstream transcription factor PUCHI. TOLS2 is expressed at the LR founder cells and inhibits LR initiation. Time-lapse imaging of auxin-responsive DR5:LUCIFERASE reporter expression revealed that occasionally two pairs of LR founder cells are specified in close proximity even in wild-type and that one of them exists only transiently and disappears in an RLK7-dependent manner. We propose that the selection of LR founder cells by the peptide hormone-receptor cascade ensures proper LR spacing. •Lateral root founder cells (LRFCs) express TOLS2 peptide, inhibiting nearby LRFCs•The receptor RLK7 and transcription factor PUCHI make up the TOLS2 signaling pathway•DR5, an LRFC marker, is occasionally activated in proximity to pre-existing LRFCs•TOLS2-RLK7-PUCHI inhibits LRFC identity in proximal cells, ensuring proper LR spacing Lateral roots form at regulated intervals. Toyokura and Goh et al. identify a peptide hormone, TOLS2, expressed in lateral root founder cells in Arabidopsis thaliana. TOLS2 and its receptor, RLK7, inhibit the formation of closely spaced lateral root founder cells.
doi_str_mv 10.1016/j.devcel.2018.11.031
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The domain of high auxin response responsible for LR initiation stretches over several cells, but only a pair of pericycle cells (LR founder cells) will develop into LRs. In this work, we identified a signaling cascade controlling LR formation through lateral inhibition. It comprises a peptide hormone TARGET OF LBD SIXTEEN 2 (TOLS2), its receptor RLK7, and a downstream transcription factor PUCHI. TOLS2 is expressed at the LR founder cells and inhibits LR initiation. Time-lapse imaging of auxin-responsive DR5:LUCIFERASE reporter expression revealed that occasionally two pairs of LR founder cells are specified in close proximity even in wild-type and that one of them exists only transiently and disappears in an RLK7-dependent manner. 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TOLS2 and its receptor, RLK7, inhibit the formation of closely spaced lateral root founder cells.</description><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>auxin</subject><subject>Cell Communication - physiology</subject><subject>Cell Differentiation - physiology</subject><subject>Cell Division - physiology</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Indoleacetic Acids - metabolism</subject><subject>lateral root</subject><subject>LBD16</subject><subject>Organogenesis, Plant - physiology</subject><subject>peptide hormone</subject><subject>Plant Roots - metabolism</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>PUCHI</subject><subject>RLK7</subject><subject>TOLS2/PIPL3</subject><issn>1534-5807</issn><issn>1878-1551</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE2L2zAQhkVp2c1u9x-URcde7Gpsy1YuhRD2IxBoCe1ZjORxq2BbWcleyL9fhWR77Elfz7wzehj7AiIHAfW3fd7Sq6U-LwSoHCAXJXxgC1CNykBK-Jj2sqwyqURzzW5i3ItUBkpcsetSSAUJWjC_xYkC9nwz_nXGTc6P3Bw58p90mFxL_NmHwY-U7cimGx_4GqPF9NDOwY1_-Cqgca0_RBf5e9bO-4k_-nlsKfHU9-kQBjyFf2afOuwj3V3WW_b78eHX-jnb_njarFfbzFZNNWXdEq1BRMK6Vl1dyMY0qsEC09BkJBF1y9rQUpRGiKKTZVlZasuO6qJTRizLW_b1nHsI_mWmOOnBxWSrx5H8HHUBtQBZpOSEVmfUBh9joE4fghswHDUIfVKt9_qsWp9UawCdVKey-0uH2QzU_it6d5uA72eA0j9fHQUdraMxzekC2Um33v2_wxsLKpMK</recordid><startdate>20190107</startdate><enddate>20190107</enddate><creator>Toyokura, Koichi</creator><creator>Goh, Tatsuaki</creator><creator>Shinohara, Hidefumi</creator><creator>Shinoda, Akinori</creator><creator>Kondo, Yuki</creator><creator>Okamoto, Yoshie</creator><creator>Uehara, Takeo</creator><creator>Fujimoto, Koichi</creator><creator>Okushima, Yoko</creator><creator>Ikeyama, Yoshifumi</creator><creator>Nakajima, Keiji</creator><creator>Mimura, Tetsuro</creator><creator>Tasaka, Masao</creator><creator>Matsubayashi, Yoshikatsu</creator><creator>Fukaki, Hidehiro</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20190107</creationdate><title>Lateral Inhibition by a Peptide Hormone-Receptor Cascade during Arabidopsis Lateral Root Founder Cell Formation</title><author>Toyokura, Koichi ; 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subjects Arabidopsis - metabolism
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
auxin
Cell Communication - physiology
Cell Differentiation - physiology
Cell Division - physiology
Gene Expression Regulation, Plant - physiology
Indoleacetic Acids - metabolism
lateral root
LBD16
Organogenesis, Plant - physiology
peptide hormone
Plant Roots - metabolism
Plants, Genetically Modified - metabolism
PUCHI
RLK7
TOLS2/PIPL3
title Lateral Inhibition by a Peptide Hormone-Receptor Cascade during Arabidopsis Lateral Root Founder Cell Formation
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