DRO1 influences root system architecture in Arabidopsis and Prunus species

Summary Roots provide essential uptake of water and nutrients from the soil, as well as anchorage and stability for the whole plant. Root orientation, or angle, is an important component of the overall architecture and depth of the root system; however, little is known about the genetic control of t...

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Veröffentlicht in:The Plant journal : for cell and molecular biology 2017-03, Vol.89 (6), p.1093-1105
Hauptverfasser: Guseman, Jessica M., Webb, Kevin, Srinivasan, Chinnathambi, Dardick, Chris
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container_issue 6
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container_title The Plant journal : for cell and molecular biology
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creator Guseman, Jessica M.
Webb, Kevin
Srinivasan, Chinnathambi
Dardick, Chris
description Summary Roots provide essential uptake of water and nutrients from the soil, as well as anchorage and stability for the whole plant. Root orientation, or angle, is an important component of the overall architecture and depth of the root system; however, little is known about the genetic control of this trait. Recent reports in Oryza sativa (rice) identified a role for DEEPER ROOTING 1 (DRO1) in influencing the orientation of the root system, leading to positive changes in grain yields under water‐limited conditions. Here we found that DRO1 and DRO1‐related genes are present across diverse plant phyla, and fall within the IGT gene family. The IGT family also includes TAC1 and LAZY1, which are known to affect the orientation of lateral shoots. Consistent with a potential role in root development, DRO1 homologs in Arabidopsis and peach showed root‐specific expression. Promoter–reporter constructs revealed that AtDRO1 is predominantly expressed in both the root vasculature and root tips, in a distinct developmental pattern. Mutation of AtDRO1 led to more horizontal lateral root angles. Overexpression of AtDRO1 under a constitutive promoter resulted in steeper lateral root angles, as well as shoot phenotypes including upward leaf curling, shortened siliques and narrow lateral branch angles. A conserved C‐terminal EAR‐like motif found in IGT genes was required for these ectopic phenotypes. Overexpression of PpeDRO1 in Prunus domestica (plum) led to deeper‐rooting phenotypes. Collectively, these data indicate a potential application for DRO1‐related genes to alter root architecture for drought avoidance and improved resource use. Significance Statement Root orientation is an architectural trait that can greatly influence the overall depth of a root system, but little is known about the genetic control of this trait. Here we demonstrate that expression of DEEPER ROOTING genes is important for lateral root angle in the model plant Arabidopsis and for root system depth in plum. We suggest that manipulating DRO1 expression will be useful for altering root architecture in crops.
doi_str_mv 10.1111/tpj.13470
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Root orientation, or angle, is an important component of the overall architecture and depth of the root system; however, little is known about the genetic control of this trait. Recent reports in Oryza sativa (rice) identified a role for DEEPER ROOTING 1 (DRO1) in influencing the orientation of the root system, leading to positive changes in grain yields under water‐limited conditions. Here we found that DRO1 and DRO1‐related genes are present across diverse plant phyla, and fall within the IGT gene family. The IGT family also includes TAC1 and LAZY1, which are known to affect the orientation of lateral shoots. Consistent with a potential role in root development, DRO1 homologs in Arabidopsis and peach showed root‐specific expression. Promoter–reporter constructs revealed that AtDRO1 is predominantly expressed in both the root vasculature and root tips, in a distinct developmental pattern. Mutation of AtDRO1 led to more horizontal lateral root angles. Overexpression of AtDRO1 under a constitutive promoter resulted in steeper lateral root angles, as well as shoot phenotypes including upward leaf curling, shortened siliques and narrow lateral branch angles. A conserved C‐terminal EAR‐like motif found in IGT genes was required for these ectopic phenotypes. Overexpression of PpeDRO1 in Prunus domestica (plum) led to deeper‐rooting phenotypes. Collectively, these data indicate a potential application for DRO1‐related genes to alter root architecture for drought avoidance and improved resource use. Significance Statement Root orientation is an architectural trait that can greatly influence the overall depth of a root system, but little is known about the genetic control of this trait. Here we demonstrate that expression of DEEPER ROOTING genes is important for lateral root angle in the model plant Arabidopsis and for root system depth in plum. We suggest that manipulating DRO1 expression will be useful for altering root architecture in crops.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.13470</identifier><identifier>PMID: 28029738</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Avoidance ; Botany ; Crop science ; Drought ; fruits ; Gene expression ; gene overexpression ; Genes ; Genetic control ; Genetics ; Grain ; grain yield ; gravitropism ; Gravitropism - genetics ; Gravitropism - physiology ; Homology ; IGT family ; LAZY1 ; leaf curling ; Mutation ; Nutrients ; Orientation ; Oryza sativa ; peaches ; phenotype ; Phenotypes ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Roots - genetics ; Plant Roots - metabolism ; Plant Roots - physiology ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - growth &amp; development ; Plants, Genetically Modified - metabolism ; plums ; promoter regions ; Promoter Regions, Genetic - genetics ; Prunus ; Prunus - genetics ; Prunus - metabolism ; Prunus - physiology ; Prunus domestica ; rice ; Root development ; root orientation ; root system architecture ; root systems ; root tips ; Rooting ; Roots ; Shoots ; soil ; Soil stability ; TAC1</subject><ispartof>The Plant journal : for cell and molecular biology, 2017-03, Vol.89 (6), p.1093-1105</ispartof><rights>Published 2016. This article is a U.S. Government work and is in the public domain in the USA</rights><rights>Published 2016. This article is a U.S. Government work and is in the public domain in the USA.</rights><rights>Copyright © 2017 John Wiley &amp; Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.13470$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.13470$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,778,782,1414,1430,27907,27908,45557,45558,46392,46816</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28029738$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guseman, Jessica M.</creatorcontrib><creatorcontrib>Webb, Kevin</creatorcontrib><creatorcontrib>Srinivasan, Chinnathambi</creatorcontrib><creatorcontrib>Dardick, Chris</creatorcontrib><title>DRO1 influences root system architecture in Arabidopsis and Prunus species</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary Roots provide essential uptake of water and nutrients from the soil, as well as anchorage and stability for the whole plant. Root orientation, or angle, is an important component of the overall architecture and depth of the root system; however, little is known about the genetic control of this trait. Recent reports in Oryza sativa (rice) identified a role for DEEPER ROOTING 1 (DRO1) in influencing the orientation of the root system, leading to positive changes in grain yields under water‐limited conditions. Here we found that DRO1 and DRO1‐related genes are present across diverse plant phyla, and fall within the IGT gene family. The IGT family also includes TAC1 and LAZY1, which are known to affect the orientation of lateral shoots. Consistent with a potential role in root development, DRO1 homologs in Arabidopsis and peach showed root‐specific expression. Promoter–reporter constructs revealed that AtDRO1 is predominantly expressed in both the root vasculature and root tips, in a distinct developmental pattern. Mutation of AtDRO1 led to more horizontal lateral root angles. Overexpression of AtDRO1 under a constitutive promoter resulted in steeper lateral root angles, as well as shoot phenotypes including upward leaf curling, shortened siliques and narrow lateral branch angles. A conserved C‐terminal EAR‐like motif found in IGT genes was required for these ectopic phenotypes. Overexpression of PpeDRO1 in Prunus domestica (plum) led to deeper‐rooting phenotypes. Collectively, these data indicate a potential application for DRO1‐related genes to alter root architecture for drought avoidance and improved resource use. Significance Statement Root orientation is an architectural trait that can greatly influence the overall depth of a root system, but little is known about the genetic control of this trait. Here we demonstrate that expression of DEEPER ROOTING genes is important for lateral root angle in the model plant Arabidopsis and for root system depth in plum. We suggest that manipulating DRO1 expression will be useful for altering root architecture in crops.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Avoidance</subject><subject>Botany</subject><subject>Crop science</subject><subject>Drought</subject><subject>fruits</subject><subject>Gene expression</subject><subject>gene overexpression</subject><subject>Genes</subject><subject>Genetic control</subject><subject>Genetics</subject><subject>Grain</subject><subject>grain yield</subject><subject>gravitropism</subject><subject>Gravitropism - genetics</subject><subject>Gravitropism - physiology</subject><subject>Homology</subject><subject>IGT family</subject><subject>LAZY1</subject><subject>leaf curling</subject><subject>Mutation</subject><subject>Nutrients</subject><subject>Orientation</subject><subject>Oryza sativa</subject><subject>peaches</subject><subject>phenotype</subject><subject>Phenotypes</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - metabolism</subject><subject>Plant Roots - physiology</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - growth &amp; development</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>plums</subject><subject>promoter regions</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Prunus</subject><subject>Prunus - genetics</subject><subject>Prunus - metabolism</subject><subject>Prunus - physiology</subject><subject>Prunus domestica</subject><subject>rice</subject><subject>Root development</subject><subject>root orientation</subject><subject>root system architecture</subject><subject>root systems</subject><subject>root tips</subject><subject>Rooting</subject><subject>Roots</subject><subject>Shoots</subject><subject>soil</subject><subject>Soil stability</subject><subject>TAC1</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqN0c9LwzAUB_AgipvTg_-AFLx46faSlzTNcczfCIooeCtd-4odXVuTFtl_b9ymBw9qLgm8Dy_J-zJ2zGHM_Zp07WLMUWrYYUOOkQqR48suG4KJINSSiwE7cG4BwDVGcp8NRAzCaIyH7Pb88Z4HZV1UPdUZucA2TRe4letoGaQ2ey07yrrekjfB1KbzMm9aV7ogrfPgwfZ17wLXUlaSO2R7RVo5OtruI_Z8efE0uw7v7q9uZtO7cCHRQBgXUs9lkeeYcZqTSk1UFCBzU0SiEIRG-3dSGhmpYsUjykkrpaRE6ZkihSN2tunb2uatJ9cly9JlVFVpTU3vEgEAUoFC-Sflsdaxvwf4P6hCP0rOP7ue_qCLpre1_7NXRkcoBJjflUaDhgvw6mSr-vmS8qS15TK1q-QrIQ8mG_BeVrT6rnNIPqNPfPTJOvrk6eF2fcAPSKudLg</recordid><startdate>201703</startdate><enddate>201703</enddate><creator>Guseman, Jessica M.</creator><creator>Webb, Kevin</creator><creator>Srinivasan, Chinnathambi</creator><creator>Dardick, Chris</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>201703</creationdate><title>DRO1 influences root system architecture in Arabidopsis and Prunus species</title><author>Guseman, Jessica M. ; 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development</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>plums</topic><topic>promoter regions</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Prunus</topic><topic>Prunus - genetics</topic><topic>Prunus - metabolism</topic><topic>Prunus - physiology</topic><topic>Prunus domestica</topic><topic>rice</topic><topic>Root development</topic><topic>root orientation</topic><topic>root system architecture</topic><topic>root systems</topic><topic>root tips</topic><topic>Rooting</topic><topic>Roots</topic><topic>Shoots</topic><topic>soil</topic><topic>Soil stability</topic><topic>TAC1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guseman, Jessica M.</creatorcontrib><creatorcontrib>Webb, Kevin</creatorcontrib><creatorcontrib>Srinivasan, Chinnathambi</creatorcontrib><creatorcontrib>Dardick, Chris</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium &amp; 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Root orientation, or angle, is an important component of the overall architecture and depth of the root system; however, little is known about the genetic control of this trait. Recent reports in Oryza sativa (rice) identified a role for DEEPER ROOTING 1 (DRO1) in influencing the orientation of the root system, leading to positive changes in grain yields under water‐limited conditions. Here we found that DRO1 and DRO1‐related genes are present across diverse plant phyla, and fall within the IGT gene family. The IGT family also includes TAC1 and LAZY1, which are known to affect the orientation of lateral shoots. Consistent with a potential role in root development, DRO1 homologs in Arabidopsis and peach showed root‐specific expression. Promoter–reporter constructs revealed that AtDRO1 is predominantly expressed in both the root vasculature and root tips, in a distinct developmental pattern. Mutation of AtDRO1 led to more horizontal lateral root angles. Overexpression of AtDRO1 under a constitutive promoter resulted in steeper lateral root angles, as well as shoot phenotypes including upward leaf curling, shortened siliques and narrow lateral branch angles. A conserved C‐terminal EAR‐like motif found in IGT genes was required for these ectopic phenotypes. Overexpression of PpeDRO1 in Prunus domestica (plum) led to deeper‐rooting phenotypes. Collectively, these data indicate a potential application for DRO1‐related genes to alter root architecture for drought avoidance and improved resource use. Significance Statement Root orientation is an architectural trait that can greatly influence the overall depth of a root system, but little is known about the genetic control of this trait. Here we demonstrate that expression of DEEPER ROOTING genes is important for lateral root angle in the model plant Arabidopsis and for root system depth in plum. We suggest that manipulating DRO1 expression will be useful for altering root architecture in crops.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>28029738</pmid><doi>10.1111/tpj.13470</doi><tpages>13</tpages></addata></record>
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subjects Arabidopsis
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis - physiology
Avoidance
Botany
Crop science
Drought
fruits
Gene expression
gene overexpression
Genes
Genetic control
Genetics
Grain
grain yield
gravitropism
Gravitropism - genetics
Gravitropism - physiology
Homology
IGT family
LAZY1
leaf curling
Mutation
Nutrients
Orientation
Oryza sativa
peaches
phenotype
Phenotypes
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Roots - genetics
Plant Roots - metabolism
Plant Roots - physiology
Plants, Genetically Modified - genetics
Plants, Genetically Modified - growth & development
Plants, Genetically Modified - metabolism
plums
promoter regions
Promoter Regions, Genetic - genetics
Prunus
Prunus - genetics
Prunus - metabolism
Prunus - physiology
Prunus domestica
rice
Root development
root orientation
root system architecture
root systems
root tips
Rooting
Roots
Shoots
soil
Soil stability
TAC1
title DRO1 influences root system architecture in Arabidopsis and Prunus species
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