Apical dominance control by TAR-YUC-mediated auxin biosynthesis is a deep homology of land plants
A key aim in biology is to identify which genetic changes contributed to the evolution of form through time. Apical dominance, the inhibitory effect exerted by shoot apices on the initiation or outgrowth of distant lateral buds, is a major regulatory mechanism of plant form.1 Nearly a century of stu...
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Veröffentlicht in: | Current biology 2022-09, Vol.32 (17), p.3838-3846.e5 |
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creator | Thelander, Mattias Landberg, Katarina Muller, Arthur Cloarec, Gladys Cunniffe, Nik Huguet, Stéphanie Soubigou-Taconnat, Ludivine Brunaud, Véronique Coudert, Yoan |
description | A key aim in biology is to identify which genetic changes contributed to the evolution of form through time. Apical dominance, the inhibitory effect exerted by shoot apices on the initiation or outgrowth of distant lateral buds, is a major regulatory mechanism of plant form.1 Nearly a century of studies in the sporophyte of flowering plants have established the phytohormone auxin as a front-runner in the search for key factors controlling apical dominance,2,3 identifying critical roles for long-range polar auxin transport and local auxin biosynthesis in modulating shoot branching.4-10 A capacity for lateral branching evolved by convergence in the gametophytic shoot of mosses and primed its diversification;11 however, polar auxin transport is relatively unimportant in this developmental process,12 the contribution of auxin biosynthesis genes has not been assessed, and more generally, the extent of conservation in apical dominance regulation within the land plants remains largely unknown. To fill this knowledge gap, we sought to identify genetic determinants of apical dominance in the moss Physcomitrium patens. Here, we show that leafy shoot apex decapitation releases apical dominance through massive and rapid transcriptional reprogramming of auxin-responsive genes and altering auxin biosynthesis gene activity. We pinpoint a subset of P. patens TRYPTOPHAN AMINO-TRANSFERASE (TAR) and YUCCA FLAVIN MONOOXYGENASE-LIKE (YUC) auxin biosynthesis genes expressed in the main and lateral shoot apices and show that they are essential for coordinating branch initiation and outgrowth. Our results demonstrate that local auxin biosynthesis acts as a pivotal regulator of apical dominance in moss and constitutes a shared mechanism underpinning shoot architecture control in land plants. |
doi_str_mv | 10.1016/j.cub.2022.06.064 |
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Apical dominance, the inhibitory effect exerted by shoot apices on the initiation or outgrowth of distant lateral buds, is a major regulatory mechanism of plant form.1 Nearly a century of studies in the sporophyte of flowering plants have established the phytohormone auxin as a front-runner in the search for key factors controlling apical dominance,2,3 identifying critical roles for long-range polar auxin transport and local auxin biosynthesis in modulating shoot branching.4-10 A capacity for lateral branching evolved by convergence in the gametophytic shoot of mosses and primed its diversification;11 however, polar auxin transport is relatively unimportant in this developmental process,12 the contribution of auxin biosynthesis genes has not been assessed, and more generally, the extent of conservation in apical dominance regulation within the land plants remains largely unknown. To fill this knowledge gap, we sought to identify genetic determinants of apical dominance in the moss Physcomitrium patens. Here, we show that leafy shoot apex decapitation releases apical dominance through massive and rapid transcriptional reprogramming of auxin-responsive genes and altering auxin biosynthesis gene activity. We pinpoint a subset of P. patens TRYPTOPHAN AMINO-TRANSFERASE (TAR) and YUCCA FLAVIN MONOOXYGENASE-LIKE (YUC) auxin biosynthesis genes expressed in the main and lateral shoot apices and show that they are essential for coordinating branch initiation and outgrowth. 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Apical dominance, the inhibitory effect exerted by shoot apices on the initiation or outgrowth of distant lateral buds, is a major regulatory mechanism of plant form.1 Nearly a century of studies in the sporophyte of flowering plants have established the phytohormone auxin as a front-runner in the search for key factors controlling apical dominance,2,3 identifying critical roles for long-range polar auxin transport and local auxin biosynthesis in modulating shoot branching.4-10 A capacity for lateral branching evolved by convergence in the gametophytic shoot of mosses and primed its diversification;11 however, polar auxin transport is relatively unimportant in this developmental process,12 the contribution of auxin biosynthesis genes has not been assessed, and more generally, the extent of conservation in apical dominance regulation within the land plants remains largely unknown. To fill this knowledge gap, we sought to identify genetic determinants of apical dominance in the moss Physcomitrium patens. Here, we show that leafy shoot apex decapitation releases apical dominance through massive and rapid transcriptional reprogramming of auxin-responsive genes and altering auxin biosynthesis gene activity. We pinpoint a subset of P. patens TRYPTOPHAN AMINO-TRANSFERASE (TAR) and YUCCA FLAVIN MONOOXYGENASE-LIKE (YUC) auxin biosynthesis genes expressed in the main and lateral shoot apices and show that they are essential for coordinating branch initiation and outgrowth. Our results demonstrate that local auxin biosynthesis acts as a pivotal regulator of apical dominance in moss and constitutes a shared mechanism underpinning shoot architecture control in land plants.</description><subject>Biochemistry, Molecular Biology</subject><subject>Botanics</subject><subject>Genomics</subject><subject>Life Sciences</subject><subject>Vegetal Biology</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNo9kV9LwzAUxYMoOqcfwLc86kPnTdqkyeMY6oSBINuDTyHNH5fRNrXpxH17OybC4V64_Dj3wEHojsCMAOGPu5nZVzMKlM6AjyrO0ISIUmZQFOwcTUByyKSg9Apdp7QDIFRIfomuciYKIiRMkJ53wega29iEVrfGYRPboY81rg54PX_PPjaLrHE26MFZrPc_ocVViOnQDluXQsKjNLbOdXgbm1jHzwOOHte6tbgb55Bu0IXXdXK3f3uKNs9P68UyW729vC7mq8zkjA2ZcYUhjLPS5CSXQjhtaCnBOwIMfFEZWTBuPefMaiu8L8EJai3xklfGVFU-RQ8n362uVdeHRvcHFXVQy_lKHW-Ql5yXlH2Tkb0_sV0fv_YuDaoJybh6DOziPinK5fiWUDii5ISaPqbUO__vTUAdW1A7Nbagji0o4KOK_BfYPHmu</recordid><startdate>20220912</startdate><enddate>20220912</enddate><creator>Thelander, Mattias</creator><creator>Landberg, Katarina</creator><creator>Muller, Arthur</creator><creator>Cloarec, Gladys</creator><creator>Cunniffe, Nik</creator><creator>Huguet, Stéphanie</creator><creator>Soubigou-Taconnat, Ludivine</creator><creator>Brunaud, Véronique</creator><creator>Coudert, Yoan</creator><general>Elsevier</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0001-7912-7220</orcidid><orcidid>https://orcid.org/0000-0002-6246-3161</orcidid><orcidid>https://orcid.org/0000-0003-1891-8875</orcidid></search><sort><creationdate>20220912</creationdate><title>Apical dominance control by TAR-YUC-mediated auxin biosynthesis is a deep homology of land plants</title><author>Thelander, Mattias ; Landberg, Katarina ; Muller, Arthur ; Cloarec, Gladys ; Cunniffe, Nik ; Huguet, Stéphanie ; Soubigou-Taconnat, Ludivine ; Brunaud, Véronique ; Coudert, Yoan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c355t-ce4c15657c313988eac2790fe1050f4bc9456df665dad8ff70e82dd1f96bccbb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biochemistry, Molecular Biology</topic><topic>Botanics</topic><topic>Genomics</topic><topic>Life Sciences</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Thelander, Mattias</creatorcontrib><creatorcontrib>Landberg, Katarina</creatorcontrib><creatorcontrib>Muller, Arthur</creatorcontrib><creatorcontrib>Cloarec, Gladys</creatorcontrib><creatorcontrib>Cunniffe, Nik</creatorcontrib><creatorcontrib>Huguet, Stéphanie</creatorcontrib><creatorcontrib>Soubigou-Taconnat, Ludivine</creatorcontrib><creatorcontrib>Brunaud, Véronique</creatorcontrib><creatorcontrib>Coudert, Yoan</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Thelander, Mattias</au><au>Landberg, Katarina</au><au>Muller, Arthur</au><au>Cloarec, Gladys</au><au>Cunniffe, Nik</au><au>Huguet, Stéphanie</au><au>Soubigou-Taconnat, Ludivine</au><au>Brunaud, Véronique</au><au>Coudert, Yoan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Apical dominance control by TAR-YUC-mediated auxin biosynthesis is a deep homology of land plants</atitle><jtitle>Current biology</jtitle><date>2022-09-12</date><risdate>2022</risdate><volume>32</volume><issue>17</issue><spage>3838</spage><epage>3846.e5</epage><pages>3838-3846.e5</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>A key aim in biology is to identify which genetic changes contributed to the evolution of form through time. Apical dominance, the inhibitory effect exerted by shoot apices on the initiation or outgrowth of distant lateral buds, is a major regulatory mechanism of plant form.1 Nearly a century of studies in the sporophyte of flowering plants have established the phytohormone auxin as a front-runner in the search for key factors controlling apical dominance,2,3 identifying critical roles for long-range polar auxin transport and local auxin biosynthesis in modulating shoot branching.4-10 A capacity for lateral branching evolved by convergence in the gametophytic shoot of mosses and primed its diversification;11 however, polar auxin transport is relatively unimportant in this developmental process,12 the contribution of auxin biosynthesis genes has not been assessed, and more generally, the extent of conservation in apical dominance regulation within the land plants remains largely unknown. To fill this knowledge gap, we sought to identify genetic determinants of apical dominance in the moss Physcomitrium patens. Here, we show that leafy shoot apex decapitation releases apical dominance through massive and rapid transcriptional reprogramming of auxin-responsive genes and altering auxin biosynthesis gene activity. We pinpoint a subset of P. patens TRYPTOPHAN AMINO-TRANSFERASE (TAR) and YUCCA FLAVIN MONOOXYGENASE-LIKE (YUC) auxin biosynthesis genes expressed in the main and lateral shoot apices and show that they are essential for coordinating branch initiation and outgrowth. Our results demonstrate that local auxin biosynthesis acts as a pivotal regulator of apical dominance in moss and constitutes a shared mechanism underpinning shoot architecture control in land plants.</abstract><pub>Elsevier</pub><pmid>35841890</pmid><doi>10.1016/j.cub.2022.06.064</doi><orcidid>https://orcid.org/0000-0001-7912-7220</orcidid><orcidid>https://orcid.org/0000-0002-6246-3161</orcidid><orcidid>https://orcid.org/0000-0003-1891-8875</orcidid><oa>free_for_read</oa></addata></record> |
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title | Apical dominance control by TAR-YUC-mediated auxin biosynthesis is a deep homology of land plants |
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