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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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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•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.</description><identifier>ISSN: 1534-5807</identifier><identifier>EISSN: 1878-1551</identifier><identifier>DOI: 10.1016/j.devcel.2018.11.031</identifier><identifier>PMID: 30581155</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>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</subject><ispartof>Developmental cell, 2019-01, Vol.48 (1), p.64-75.e5</ispartof><rights>2018 Elsevier Inc.</rights><rights>Copyright © 2018 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-f9acbaaaea668f6257b787a2a155eb5eeef96be903b002f5334ced3fe62f8b093</citedby><cites>FETCH-LOGICAL-c474t-f9acbaaaea668f6257b787a2a155eb5eeef96be903b002f5334ced3fe62f8b093</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.devcel.2018.11.031$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30581155$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Toyokura, Koichi</creatorcontrib><creatorcontrib>Goh, Tatsuaki</creatorcontrib><creatorcontrib>Shinohara, Hidefumi</creatorcontrib><creatorcontrib>Shinoda, Akinori</creatorcontrib><creatorcontrib>Kondo, Yuki</creatorcontrib><creatorcontrib>Okamoto, Yoshie</creatorcontrib><creatorcontrib>Uehara, Takeo</creatorcontrib><creatorcontrib>Fujimoto, Koichi</creatorcontrib><creatorcontrib>Okushima, Yoko</creatorcontrib><creatorcontrib>Ikeyama, Yoshifumi</creatorcontrib><creatorcontrib>Nakajima, Keiji</creatorcontrib><creatorcontrib>Mimura, Tetsuro</creatorcontrib><creatorcontrib>Tasaka, Masao</creatorcontrib><creatorcontrib>Matsubayashi, Yoshikatsu</creatorcontrib><creatorcontrib>Fukaki, Hidehiro</creatorcontrib><title>Lateral Inhibition by a Peptide Hormone-Receptor Cascade during Arabidopsis Lateral Root Founder Cell Formation</title><title>Developmental cell</title><addtitle>Dev Cell</addtitle><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.</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 ; 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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-f9acbaaaea668f6257b787a2a155eb5eeef96be903b002f5334ced3fe62f8b093</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>auxin</topic><topic>Cell Communication - physiology</topic><topic>Cell Differentiation - physiology</topic><topic>Cell Division - physiology</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>Indoleacetic Acids - metabolism</topic><topic>lateral root</topic><topic>LBD16</topic><topic>Organogenesis, Plant - physiology</topic><topic>peptide hormone</topic><topic>Plant Roots - metabolism</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>PUCHI</topic><topic>RLK7</topic><topic>TOLS2/PIPL3</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Toyokura, Koichi</creatorcontrib><creatorcontrib>Goh, Tatsuaki</creatorcontrib><creatorcontrib>Shinohara, Hidefumi</creatorcontrib><creatorcontrib>Shinoda, Akinori</creatorcontrib><creatorcontrib>Kondo, Yuki</creatorcontrib><creatorcontrib>Okamoto, Yoshie</creatorcontrib><creatorcontrib>Uehara, Takeo</creatorcontrib><creatorcontrib>Fujimoto, Koichi</creatorcontrib><creatorcontrib>Okushima, Yoko</creatorcontrib><creatorcontrib>Ikeyama, Yoshifumi</creatorcontrib><creatorcontrib>Nakajima, Keiji</creatorcontrib><creatorcontrib>Mimura, Tetsuro</creatorcontrib><creatorcontrib>Tasaka, Masao</creatorcontrib><creatorcontrib>Matsubayashi, Yoshikatsu</creatorcontrib><creatorcontrib>Fukaki, Hidehiro</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Developmental cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Toyokura, Koichi</au><au>Goh, Tatsuaki</au><au>Shinohara, Hidefumi</au><au>Shinoda, Akinori</au><au>Kondo, Yuki</au><au>Okamoto, Yoshie</au><au>Uehara, Takeo</au><au>Fujimoto, Koichi</au><au>Okushima, Yoko</au><au>Ikeyama, Yoshifumi</au><au>Nakajima, Keiji</au><au>Mimura, Tetsuro</au><au>Tasaka, Masao</au><au>Matsubayashi, Yoshikatsu</au><au>Fukaki, Hidehiro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lateral Inhibition by a Peptide Hormone-Receptor Cascade during Arabidopsis Lateral Root Founder Cell Formation</atitle><jtitle>Developmental cell</jtitle><addtitle>Dev Cell</addtitle><date>2019-01-07</date><risdate>2019</risdate><volume>48</volume><issue>1</issue><spage>64</spage><epage>75.e5</epage><pages>64-75.e5</pages><issn>1534-5807</issn><eissn>1878-1551</eissn><abstract>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.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>30581155</pmid><doi>10.1016/j.devcel.2018.11.031</doi><oa>free_for_read</oa></addata></record> |
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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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