BUZZ: an essential gene for postinitiation root hair growth and a mediator of root architecture in Brachypodium distachyon
Summary Here, we discover a player in root development. Recovered from a forward‐genetic screen in Brachypodium distachyon, the buzz mutant initiates root hairs but they fail to elongate. In addition, buzz roots grow twice as fast as wild‐type roots. Also, lateral roots show increased sensitivity to...
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Veröffentlicht in: | The New phytologist 2023-09, Vol.239 (5), p.1723-1739 |
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creator | Lehman, Thiel A. Rosas, Miguel A. Brew‐Appiah, Rhoda A. T. Solanki, Shyam York, Zara B. Dannay, Rachel Wu, Ying Roalson, Eric H. Zheng, Ping Main, Dorrie Baskin, Tobias I. Sanguinet, Karen A. |
description | Summary
Here, we discover a player in root development. Recovered from a forward‐genetic screen in Brachypodium distachyon, the buzz mutant initiates root hairs but they fail to elongate. In addition, buzz roots grow twice as fast as wild‐type roots. Also, lateral roots show increased sensitivity to nitrate, whereas primary roots are less sensitive to nitrate.
Using whole‐genome resequencing, we identified the causal single nucleotide polymorphism as occurring in a conserved but previously uncharacterized cyclin‐dependent kinase (CDK)‐like gene. The buzz mutant phenotypes are rescued by the wild‐type B. distachyon BUZZ coding sequence and by an apparent homolog in Arabidopsis thaliana. Moreover, T‐DNA mutants in A. thaliana BUZZ have shorter root hairs.
BUZZ mRNA localizes to epidermal cells and develops root hairs and, in the latter, partially colocalizes with the NRT1.1A nitrate transporter. Based on qPCR and RNA‐Seq, buzz overexpresses ROOT HAIRLESS LIKE SIX‐1 and ‐2 and misregulates genes related to hormone signaling, RNA processing, cytoskeletal, and cell wall organization, and to the assimilation of nitrate.
Overall, these data demonstrate that BUZZ is required for tip growth after root hair initiation and root architectural responses to nitrate. |
doi_str_mv | 10.1111/nph.19079 |
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Here, we discover a player in root development. Recovered from a forward‐genetic screen in Brachypodium distachyon, the buzz mutant initiates root hairs but they fail to elongate. In addition, buzz roots grow twice as fast as wild‐type roots. Also, lateral roots show increased sensitivity to nitrate, whereas primary roots are less sensitive to nitrate.
Using whole‐genome resequencing, we identified the causal single nucleotide polymorphism as occurring in a conserved but previously uncharacterized cyclin‐dependent kinase (CDK)‐like gene. The buzz mutant phenotypes are rescued by the wild‐type B. distachyon BUZZ coding sequence and by an apparent homolog in Arabidopsis thaliana. Moreover, T‐DNA mutants in A. thaliana BUZZ have shorter root hairs.
BUZZ mRNA localizes to epidermal cells and develops root hairs and, in the latter, partially colocalizes with the NRT1.1A nitrate transporter. Based on qPCR and RNA‐Seq, buzz overexpresses ROOT HAIRLESS LIKE SIX‐1 and ‐2 and misregulates genes related to hormone signaling, RNA processing, cytoskeletal, and cell wall organization, and to the assimilation of nitrate.
Overall, these data demonstrate that BUZZ is required for tip growth after root hair initiation and root architectural responses to nitrate.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19079</identifier><identifier>PMID: 37421201</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Arabidopsis ; Arabidopsis Proteins - metabolism ; BASIC BIOLOGICAL SCIENCES ; Brachypodium ; Brachypodium distachyon ; BUZZ ; Cell walls ; Cytoskeleton ; Deoxyribonucleic acid ; DNA ; Gene Expression Regulation, Plant ; Genes ; Genes, Essential ; Genetic screening ; Genomes ; Hairless ; Hormones ; kinase ; Kinases ; mRNA ; Mutants ; nitrate ; Nitrates ; Nitrates - metabolism ; Nucleotide sequence ; Nucleotides ; Phenotypes ; Plant Roots - metabolism ; Polymorphism ; Ribonucleic acid ; RNA ; RNA processing ; root architecture ; Root development ; root hair ; Root hairs ; Roots ; RSLs ; Signal processing ; Single-nucleotide polymorphism</subject><ispartof>The New phytologist, 2023-09, Vol.239 (5), p.1723-1739</ispartof><rights>2023 The Authors. © 2023 New Phytologist Foundation</rights><rights>2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3759-3211b9b9cb338d4f18aa256c07d6c25fd174c21750eedbd6e9a353b633c4ed043</cites><orcidid>0009-0004-8485-5336 ; 0000-0003-1655-3681 ; 0000-0002-1162-2724 ; 0000-0003-1202-4870 ; 0000-0002-8043-0494 ; 0000-0003-2123-0828 ; 0000-0001-5189-3310 ; 0000-0002-1226-1422 ; 0000-0002-9686-7391 ; 0000000296867391 ; 0000000212261422 ; 0000000316553681 ; 0000000321230828 ; 0000000280430494 ; 0000000312024870 ; 0000000151893310 ; 0009000484855336 ; 0000000211622724</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.19079$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19079$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37421201$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1991247$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Lehman, Thiel A.</creatorcontrib><creatorcontrib>Rosas, Miguel A.</creatorcontrib><creatorcontrib>Brew‐Appiah, Rhoda A. T.</creatorcontrib><creatorcontrib>Solanki, Shyam</creatorcontrib><creatorcontrib>York, Zara B.</creatorcontrib><creatorcontrib>Dannay, Rachel</creatorcontrib><creatorcontrib>Wu, Ying</creatorcontrib><creatorcontrib>Roalson, Eric H.</creatorcontrib><creatorcontrib>Zheng, Ping</creatorcontrib><creatorcontrib>Main, Dorrie</creatorcontrib><creatorcontrib>Baskin, Tobias I.</creatorcontrib><creatorcontrib>Sanguinet, Karen A.</creatorcontrib><creatorcontrib>Univ. of Massachusetts, Amherst, MA (United States)</creatorcontrib><title>BUZZ: an essential gene for postinitiation root hair growth and a mediator of root architecture in Brachypodium distachyon</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Here, we discover a player in root development. Recovered from a forward‐genetic screen in Brachypodium distachyon, the buzz mutant initiates root hairs but they fail to elongate. In addition, buzz roots grow twice as fast as wild‐type roots. Also, lateral roots show increased sensitivity to nitrate, whereas primary roots are less sensitive to nitrate.
Using whole‐genome resequencing, we identified the causal single nucleotide polymorphism as occurring in a conserved but previously uncharacterized cyclin‐dependent kinase (CDK)‐like gene. The buzz mutant phenotypes are rescued by the wild‐type B. distachyon BUZZ coding sequence and by an apparent homolog in Arabidopsis thaliana. Moreover, T‐DNA mutants in A. thaliana BUZZ have shorter root hairs.
BUZZ mRNA localizes to epidermal cells and develops root hairs and, in the latter, partially colocalizes with the NRT1.1A nitrate transporter. Based on qPCR and RNA‐Seq, buzz overexpresses ROOT HAIRLESS LIKE SIX‐1 and ‐2 and misregulates genes related to hormone signaling, RNA processing, cytoskeletal, and cell wall organization, and to the assimilation of nitrate.
Overall, these data demonstrate that BUZZ is required for tip growth after root hair initiation and root architectural responses to nitrate.</description><subject>Arabidopsis</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Brachypodium</subject><subject>Brachypodium distachyon</subject><subject>BUZZ</subject><subject>Cell walls</subject><subject>Cytoskeleton</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Genes, Essential</subject><subject>Genetic screening</subject><subject>Genomes</subject><subject>Hairless</subject><subject>Hormones</subject><subject>kinase</subject><subject>Kinases</subject><subject>mRNA</subject><subject>Mutants</subject><subject>nitrate</subject><subject>Nitrates</subject><subject>Nitrates - metabolism</subject><subject>Nucleotide sequence</subject><subject>Nucleotides</subject><subject>Phenotypes</subject><subject>Plant Roots - metabolism</subject><subject>Polymorphism</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA processing</subject><subject>root architecture</subject><subject>Root development</subject><subject>root hair</subject><subject>Root hairs</subject><subject>Roots</subject><subject>RSLs</subject><subject>Signal processing</subject><subject>Single-nucleotide polymorphism</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp10U1vFSEUBmBibOy1uvAPGKIbXUzL18DgzjbaNmnUhU1MN4QBpkMzF0Zg0lx_vdxOdWEiGwJ5eHMOB4BXGB3juk7CPB5jiYR8AjaYcdl0mIqnYIMQ6RrO-I9D8DznO4SQbDl5Bg6pYAQThDfg1-n1zc0HqAN0ObtQvJ7grQsODjHBOebig6-XxccAU4wFjtoneJvifRnrKws13DpbQeVxWIlOZvTFmbIkB32Ap0mbcTdH65cttD6X_TGGF-Bg0FN2Lx_3I3D9-dP3s4vm6uv55dnHq8ZQ0cqGEox72UvTU9pZNuBOa9Jyg4TlhrSDxYIZgkWLnLO95U5q2tKeU2qYs4jRI_Bmzd13o7LZlzaaGEKtUGEpMWGioncrmlP8ubhc1NZn46ZJBxeXrEhHWyKQlKTSt__Qu7ikUFuoijHWIo5kVe9XZVLMOblBzclvddopjNR-aqpOTT1MrdrXj4lLX3_zr_wzpgpOVnDvJ7f7f5L68u1ijfwNJ2ahgA</recordid><startdate>202309</startdate><enddate>202309</enddate><creator>Lehman, Thiel A.</creator><creator>Rosas, Miguel A.</creator><creator>Brew‐Appiah, Rhoda A. T.</creator><creator>Solanki, Shyam</creator><creator>York, Zara B.</creator><creator>Dannay, Rachel</creator><creator>Wu, Ying</creator><creator>Roalson, Eric H.</creator><creator>Zheng, Ping</creator><creator>Main, Dorrie</creator><creator>Baskin, Tobias I.</creator><creator>Sanguinet, Karen A.</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><scope>24P</scope><scope>WIN</scope><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>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><orcidid>https://orcid.org/0009-0004-8485-5336</orcidid><orcidid>https://orcid.org/0000-0003-1655-3681</orcidid><orcidid>https://orcid.org/0000-0002-1162-2724</orcidid><orcidid>https://orcid.org/0000-0003-1202-4870</orcidid><orcidid>https://orcid.org/0000-0002-8043-0494</orcidid><orcidid>https://orcid.org/0000-0003-2123-0828</orcidid><orcidid>https://orcid.org/0000-0001-5189-3310</orcidid><orcidid>https://orcid.org/0000-0002-1226-1422</orcidid><orcidid>https://orcid.org/0000-0002-9686-7391</orcidid><orcidid>https://orcid.org/0000000296867391</orcidid><orcidid>https://orcid.org/0000000212261422</orcidid><orcidid>https://orcid.org/0000000316553681</orcidid><orcidid>https://orcid.org/0000000321230828</orcidid><orcidid>https://orcid.org/0000000280430494</orcidid><orcidid>https://orcid.org/0000000312024870</orcidid><orcidid>https://orcid.org/0000000151893310</orcidid><orcidid>https://orcid.org/0009000484855336</orcidid><orcidid>https://orcid.org/0000000211622724</orcidid></search><sort><creationdate>202309</creationdate><title>BUZZ: an essential gene for postinitiation root hair growth and a mediator of root architecture in Brachypodium distachyon</title><author>Lehman, Thiel A. ; Rosas, Miguel A. ; Brew‐Appiah, Rhoda A. T. ; Solanki, Shyam ; York, Zara B. ; Dannay, Rachel ; Wu, Ying ; Roalson, Eric H. ; Zheng, Ping ; Main, Dorrie ; Baskin, Tobias I. ; Sanguinet, Karen A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3759-3211b9b9cb338d4f18aa256c07d6c25fd174c21750eedbd6e9a353b633c4ed043</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Brachypodium</topic><topic>Brachypodium distachyon</topic><topic>BUZZ</topic><topic>Cell walls</topic><topic>Cytoskeleton</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Genes, Essential</topic><topic>Genetic screening</topic><topic>Genomes</topic><topic>Hairless</topic><topic>Hormones</topic><topic>kinase</topic><topic>Kinases</topic><topic>mRNA</topic><topic>Mutants</topic><topic>nitrate</topic><topic>Nitrates</topic><topic>Nitrates - metabolism</topic><topic>Nucleotide sequence</topic><topic>Nucleotides</topic><topic>Phenotypes</topic><topic>Plant Roots - metabolism</topic><topic>Polymorphism</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA processing</topic><topic>root architecture</topic><topic>Root development</topic><topic>root hair</topic><topic>Root hairs</topic><topic>Roots</topic><topic>RSLs</topic><topic>Signal processing</topic><topic>Single-nucleotide polymorphism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lehman, Thiel A.</creatorcontrib><creatorcontrib>Rosas, Miguel A.</creatorcontrib><creatorcontrib>Brew‐Appiah, Rhoda A. 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T.</au><au>Solanki, Shyam</au><au>York, Zara B.</au><au>Dannay, Rachel</au><au>Wu, Ying</au><au>Roalson, Eric H.</au><au>Zheng, Ping</au><au>Main, Dorrie</au><au>Baskin, Tobias I.</au><au>Sanguinet, Karen A.</au><aucorp>Univ. of Massachusetts, Amherst, MA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>BUZZ: an essential gene for postinitiation root hair growth and a mediator of root architecture in Brachypodium distachyon</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2023-09</date><risdate>2023</risdate><volume>239</volume><issue>5</issue><spage>1723</spage><epage>1739</epage><pages>1723-1739</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
Here, we discover a player in root development. Recovered from a forward‐genetic screen in Brachypodium distachyon, the buzz mutant initiates root hairs but they fail to elongate. In addition, buzz roots grow twice as fast as wild‐type roots. Also, lateral roots show increased sensitivity to nitrate, whereas primary roots are less sensitive to nitrate.
Using whole‐genome resequencing, we identified the causal single nucleotide polymorphism as occurring in a conserved but previously uncharacterized cyclin‐dependent kinase (CDK)‐like gene. The buzz mutant phenotypes are rescued by the wild‐type B. distachyon BUZZ coding sequence and by an apparent homolog in Arabidopsis thaliana. Moreover, T‐DNA mutants in A. thaliana BUZZ have shorter root hairs.
BUZZ mRNA localizes to epidermal cells and develops root hairs and, in the latter, partially colocalizes with the NRT1.1A nitrate transporter. Based on qPCR and RNA‐Seq, buzz overexpresses ROOT HAIRLESS LIKE SIX‐1 and ‐2 and misregulates genes related to hormone signaling, RNA processing, cytoskeletal, and cell wall organization, and to the assimilation of nitrate.
Overall, these data demonstrate that BUZZ is required for tip growth after root hair initiation and root architectural responses to nitrate.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37421201</pmid><doi>10.1111/nph.19079</doi><tpages>1739</tpages><orcidid>https://orcid.org/0009-0004-8485-5336</orcidid><orcidid>https://orcid.org/0000-0003-1655-3681</orcidid><orcidid>https://orcid.org/0000-0002-1162-2724</orcidid><orcidid>https://orcid.org/0000-0003-1202-4870</orcidid><orcidid>https://orcid.org/0000-0002-8043-0494</orcidid><orcidid>https://orcid.org/0000-0003-2123-0828</orcidid><orcidid>https://orcid.org/0000-0001-5189-3310</orcidid><orcidid>https://orcid.org/0000-0002-1226-1422</orcidid><orcidid>https://orcid.org/0000-0002-9686-7391</orcidid><orcidid>https://orcid.org/0000000296867391</orcidid><orcidid>https://orcid.org/0000000212261422</orcidid><orcidid>https://orcid.org/0000000316553681</orcidid><orcidid>https://orcid.org/0000000321230828</orcidid><orcidid>https://orcid.org/0000000280430494</orcidid><orcidid>https://orcid.org/0000000312024870</orcidid><orcidid>https://orcid.org/0000000151893310</orcidid><orcidid>https://orcid.org/0009000484855336</orcidid><orcidid>https://orcid.org/0000000211622724</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Arabidopsis Proteins - metabolism BASIC BIOLOGICAL SCIENCES Brachypodium Brachypodium distachyon BUZZ Cell walls Cytoskeleton Deoxyribonucleic acid DNA Gene Expression Regulation, Plant Genes Genes, Essential Genetic screening Genomes Hairless Hormones kinase Kinases mRNA Mutants nitrate Nitrates Nitrates - metabolism Nucleotide sequence Nucleotides Phenotypes Plant Roots - metabolism Polymorphism Ribonucleic acid RNA RNA processing root architecture Root development root hair Root hairs Roots RSLs Signal processing Single-nucleotide polymorphism |
title | BUZZ: an essential gene for postinitiation root hair growth and a mediator of root architecture in Brachypodium distachyon |
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