Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen‐fixing clade
Summary Nitrogen is one of the most inaccessible plant nutrients, but certain species have overcome this limitation by establishing symbiotic interactions with nitrogen‐fixing bacteria in the root nodule. This root–nodule symbiosis (RNS) is restricted to species within a single clade of angiosperms,...
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Veröffentlicht in: | The New phytologist 2022-04, Vol.234 (2), p.634-649 |
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creator | Pereira, Wendell J. Knaack, Sara Chakraborty, Sanhita Conde, Daniel Folk, Ryan A. Triozzi, Paolo M. Balmant, Kelly M. Dervinis, Christopher Schmidt, Henry W. Ané, Jean‐Michel Roy, Sushmita Kirst, Matias |
description | Summary
Nitrogen is one of the most inaccessible plant nutrients, but certain species have overcome this limitation by establishing symbiotic interactions with nitrogen‐fixing bacteria in the root nodule. This root–nodule symbiosis (RNS) is restricted to species within a single clade of angiosperms, suggesting a critical, but undetermined, evolutionary event at the base of this clade.
To identify putative regulatory sequences implicated in the evolution of RNS, we evaluated the genomes of 25 species capable of nodulation and identified 3091 conserved noncoding sequences (CNS) in the nitrogen‐fixing clade (NFC).
We show that the chromatin accessibility of 452 CNS correlates significantly with the regulation of genes responding to lipochitooligosaccharides in Medicago truncatula. These included 38 CNS in proximity to 19 known genes involved in RNS. Five such regions are upstream of MtCRE1, Cytokinin Response Element 1, required to activate a suite of downstream transcription factors necessary for nodulation in M. truncatula. Genetic complementation of an Mtcre1 mutant showed a significant decrease of nodulation in the absence of the five CNS, when they are driving the expression of a functional copy of MtCRE1.
CNS identified in the NFC may harbor elements required for the regulation of genes controlling RNS in M. truncatula. |
doi_str_mv | 10.1111/nph.18006 |
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Nitrogen is one of the most inaccessible plant nutrients, but certain species have overcome this limitation by establishing symbiotic interactions with nitrogen‐fixing bacteria in the root nodule. This root–nodule symbiosis (RNS) is restricted to species within a single clade of angiosperms, suggesting a critical, but undetermined, evolutionary event at the base of this clade.
To identify putative regulatory sequences implicated in the evolution of RNS, we evaluated the genomes of 25 species capable of nodulation and identified 3091 conserved noncoding sequences (CNS) in the nitrogen‐fixing clade (NFC).
We show that the chromatin accessibility of 452 CNS correlates significantly with the regulation of genes responding to lipochitooligosaccharides in Medicago truncatula. These included 38 CNS in proximity to 19 known genes involved in RNS. Five such regions are upstream of MtCRE1, Cytokinin Response Element 1, required to activate a suite of downstream transcription factors necessary for nodulation in M. truncatula. Genetic complementation of an Mtcre1 mutant showed a significant decrease of nodulation in the absence of the five CNS, when they are driving the expression of a functional copy of MtCRE1.
CNS identified in the NFC may harbor elements required for the regulation of genes controlling RNS in M. truncatula.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.18006</identifier><identifier>PMID: 35092309</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Alfalfa ; Angiosperms ; Chromatin ; comparative genomics ; Complementation ; conserved noncoding sequences (CNS) ; Cytokinins ; Fixing ; Gene Expression Regulation, Plant ; Gene regulation ; Genes ; Genomes ; Genomics ; Identification ; Medicago truncatula ; Medicago truncatula - microbiology ; MtCRE1 ; Nitrogen ; Nitrogen - metabolism ; nitrogen fixation ; Nitrogen Fixation - genetics ; Nitrogen-fixing bacteria ; Nodulation ; Nutrients ; Plant growth substances ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Root Nodulation - genetics ; Plant Sciences ; Regulatory sequences ; Root Nodules, Plant - microbiology ; Sinorhizobium meliloti ; Species ; Symbionts ; Symbiosis ; Symbiosis - genetics ; Transcription ; Transcription factors</subject><ispartof>The New phytologist, 2022-04, Vol.234 (2), p.634-649</ispartof><rights>2022 The Authors © 2022 New Phytologist Foundation</rights><rights>2022 The Authors New Phytologist © 2022 New Phytologist Foundation.</rights><rights>2022. 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><citedby>FETCH-LOGICAL-c4706-996df9d2aada4ae8d2770de45c02b6099887e60d20a4247c71a697a2eb3586783</citedby><cites>FETCH-LOGICAL-c4706-996df9d2aada4ae8d2770de45c02b6099887e60d20a4247c71a697a2eb3586783</cites><orcidid>0000-0002-3128-9439 ; 0000-0003-1019-6281 ; 0000-0002-3694-1705 ; 0000-0002-8186-3945 ; 0000-0003-0192-3336 ; 0000-0002-5333-9273 ; 0000-0001-8362-4190 ; 0000-0001-7991-3977 ; 0000-0002-2176-4232 ; 0000-0002-1178-2517 ; 0000-0003-3917-3219 ; 0000000310196281 ; 0000000221764232 ; 0000000339173219 ; 0000000236941705 ; 0000000183624190 ; 0000000253339273 ; 0000000179913977 ; 0000000211782517 ; 0000000231289439 ; 0000000301923336 ; 0000000281863945</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.18006$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.18006$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35092309$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1904396$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Pereira, Wendell J.</creatorcontrib><creatorcontrib>Knaack, Sara</creatorcontrib><creatorcontrib>Chakraborty, Sanhita</creatorcontrib><creatorcontrib>Conde, Daniel</creatorcontrib><creatorcontrib>Folk, Ryan A.</creatorcontrib><creatorcontrib>Triozzi, Paolo M.</creatorcontrib><creatorcontrib>Balmant, Kelly M.</creatorcontrib><creatorcontrib>Dervinis, Christopher</creatorcontrib><creatorcontrib>Schmidt, Henry W.</creatorcontrib><creatorcontrib>Ané, Jean‐Michel</creatorcontrib><creatorcontrib>Roy, Sushmita</creatorcontrib><creatorcontrib>Kirst, Matias</creatorcontrib><creatorcontrib>Univ. of Florida, Gainesville, FL (United States)</creatorcontrib><title>Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen‐fixing clade</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Nitrogen is one of the most inaccessible plant nutrients, but certain species have overcome this limitation by establishing symbiotic interactions with nitrogen‐fixing bacteria in the root nodule. This root–nodule symbiosis (RNS) is restricted to species within a single clade of angiosperms, suggesting a critical, but undetermined, evolutionary event at the base of this clade.
To identify putative regulatory sequences implicated in the evolution of RNS, we evaluated the genomes of 25 species capable of nodulation and identified 3091 conserved noncoding sequences (CNS) in the nitrogen‐fixing clade (NFC).
We show that the chromatin accessibility of 452 CNS correlates significantly with the regulation of genes responding to lipochitooligosaccharides in Medicago truncatula. These included 38 CNS in proximity to 19 known genes involved in RNS. Five such regions are upstream of MtCRE1, Cytokinin Response Element 1, required to activate a suite of downstream transcription factors necessary for nodulation in M. truncatula. Genetic complementation of an Mtcre1 mutant showed a significant decrease of nodulation in the absence of the five CNS, when they are driving the expression of a functional copy of MtCRE1.
CNS identified in the NFC may harbor elements required for the regulation of genes controlling RNS in M. truncatula.</description><subject>Alfalfa</subject><subject>Angiosperms</subject><subject>Chromatin</subject><subject>comparative genomics</subject><subject>Complementation</subject><subject>conserved noncoding sequences (CNS)</subject><subject>Cytokinins</subject><subject>Fixing</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Identification</subject><subject>Medicago truncatula</subject><subject>Medicago truncatula - microbiology</subject><subject>MtCRE1</subject><subject>Nitrogen</subject><subject>Nitrogen - metabolism</subject><subject>nitrogen fixation</subject><subject>Nitrogen Fixation - genetics</subject><subject>Nitrogen-fixing bacteria</subject><subject>Nodulation</subject><subject>Nutrients</subject><subject>Plant growth substances</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Root Nodulation - genetics</subject><subject>Plant Sciences</subject><subject>Regulatory sequences</subject><subject>Root Nodules, Plant - microbiology</subject><subject>Sinorhizobium meliloti</subject><subject>Species</subject><subject>Symbionts</subject><subject>Symbiosis</subject><subject>Symbiosis - genetics</subject><subject>Transcription</subject><subject>Transcription factors</subject><issn>0028-646X</issn><issn>1469-8137</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kc9u1DAQhy0EokvhwAugCC7lkHbiOP5zqYSqliJVwAEkbpbXnt24ytqLnSz0xiPwjDwJXlIqQMIXH-bzNzP-EfK0geOmnJOw7Y8bCcDvkUXDuKpl04r7ZAFAZc0Z_3RAHuV8DQCq4_QhOWg7ULQFtSD9xRTs6GMwQ2WCq2zcbE0yo99htcYQN97mKuEOzZBLMWRMO3RViMFG58O6yvh5wmAxVz5UY49V8GOK5emPb99X_usesYNx-Jg8WBUHPrm9D8nHi_MPZ5f11bvXb85eXdWWCeC1UtytlKPGOMMMSkeFAIess0CXHJSSUiAHR8EwyoQVjeFKGIrLtpNcyPaQnM7e7bTcoLMYxmQGvU1-Y9KNjsbrvyvB93odd1q1QDkXRfB8FsQ8ep2tH9H2ZfOAdtSNAtYqXqCj2y4plv3zqDc-WxwGEzBOWVNOWylVw9qCvvgHvY5TKv-9pxhQ2jG67_pypmyKOSdc3U3cgN6HrEvI-lfIhX3254p35O9UC3AyA1_8gDf_N-m37y9n5U94m7Nf</recordid><startdate>202204</startdate><enddate>202204</enddate><creator>Pereira, Wendell J.</creator><creator>Knaack, Sara</creator><creator>Chakraborty, Sanhita</creator><creator>Conde, Daniel</creator><creator>Folk, Ryan A.</creator><creator>Triozzi, Paolo M.</creator><creator>Balmant, Kelly M.</creator><creator>Dervinis, Christopher</creator><creator>Schmidt, Henry W.</creator><creator>Ané, Jean‐Michel</creator><creator>Roy, Sushmita</creator><creator>Kirst, Matias</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><general>John Wiley and Sons Inc</general><scope>24P</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><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3128-9439</orcidid><orcidid>https://orcid.org/0000-0003-1019-6281</orcidid><orcidid>https://orcid.org/0000-0002-3694-1705</orcidid><orcidid>https://orcid.org/0000-0002-8186-3945</orcidid><orcidid>https://orcid.org/0000-0003-0192-3336</orcidid><orcidid>https://orcid.org/0000-0002-5333-9273</orcidid><orcidid>https://orcid.org/0000-0001-8362-4190</orcidid><orcidid>https://orcid.org/0000-0001-7991-3977</orcidid><orcidid>https://orcid.org/0000-0002-2176-4232</orcidid><orcidid>https://orcid.org/0000-0002-1178-2517</orcidid><orcidid>https://orcid.org/0000-0003-3917-3219</orcidid><orcidid>https://orcid.org/0000000310196281</orcidid><orcidid>https://orcid.org/0000000221764232</orcidid><orcidid>https://orcid.org/0000000339173219</orcidid><orcidid>https://orcid.org/0000000236941705</orcidid><orcidid>https://orcid.org/0000000183624190</orcidid><orcidid>https://orcid.org/0000000253339273</orcidid><orcidid>https://orcid.org/0000000179913977</orcidid><orcidid>https://orcid.org/0000000211782517</orcidid><orcidid>https://orcid.org/0000000231289439</orcidid><orcidid>https://orcid.org/0000000301923336</orcidid><orcidid>https://orcid.org/0000000281863945</orcidid></search><sort><creationdate>202204</creationdate><title>Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen‐fixing clade</title><author>Pereira, Wendell J. ; Knaack, Sara ; Chakraborty, Sanhita ; Conde, Daniel ; Folk, Ryan A. ; Triozzi, Paolo M. ; Balmant, Kelly M. ; Dervinis, Christopher ; Schmidt, Henry W. ; Ané, Jean‐Michel ; Roy, Sushmita ; Kirst, Matias</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4706-996df9d2aada4ae8d2770de45c02b6099887e60d20a4247c71a697a2eb3586783</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Alfalfa</topic><topic>Angiosperms</topic><topic>Chromatin</topic><topic>comparative genomics</topic><topic>Complementation</topic><topic>conserved noncoding sequences (CNS)</topic><topic>Cytokinins</topic><topic>Fixing</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Identification</topic><topic>Medicago truncatula</topic><topic>Medicago truncatula - microbiology</topic><topic>MtCRE1</topic><topic>Nitrogen</topic><topic>Nitrogen - metabolism</topic><topic>nitrogen fixation</topic><topic>Nitrogen Fixation - genetics</topic><topic>Nitrogen-fixing bacteria</topic><topic>Nodulation</topic><topic>Nutrients</topic><topic>Plant growth substances</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Root Nodulation - genetics</topic><topic>Plant Sciences</topic><topic>Regulatory sequences</topic><topic>Root Nodules, Plant - microbiology</topic><topic>Sinorhizobium meliloti</topic><topic>Species</topic><topic>Symbionts</topic><topic>Symbiosis</topic><topic>Symbiosis - genetics</topic><topic>Transcription</topic><topic>Transcription factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pereira, Wendell J.</creatorcontrib><creatorcontrib>Knaack, Sara</creatorcontrib><creatorcontrib>Chakraborty, Sanhita</creatorcontrib><creatorcontrib>Conde, Daniel</creatorcontrib><creatorcontrib>Folk, Ryan A.</creatorcontrib><creatorcontrib>Triozzi, Paolo M.</creatorcontrib><creatorcontrib>Balmant, Kelly M.</creatorcontrib><creatorcontrib>Dervinis, Christopher</creatorcontrib><creatorcontrib>Schmidt, Henry W.</creatorcontrib><creatorcontrib>Ané, Jean‐Michel</creatorcontrib><creatorcontrib>Roy, Sushmita</creatorcontrib><creatorcontrib>Kirst, Matias</creatorcontrib><creatorcontrib>Univ. of Florida, Gainesville, FL (United States)</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pereira, Wendell J.</au><au>Knaack, Sara</au><au>Chakraborty, Sanhita</au><au>Conde, Daniel</au><au>Folk, Ryan A.</au><au>Triozzi, Paolo M.</au><au>Balmant, Kelly M.</au><au>Dervinis, Christopher</au><au>Schmidt, Henry W.</au><au>Ané, Jean‐Michel</au><au>Roy, Sushmita</au><au>Kirst, Matias</au><aucorp>Univ. of Florida, Gainesville, FL (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen‐fixing clade</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2022-04</date><risdate>2022</risdate><volume>234</volume><issue>2</issue><spage>634</spage><epage>649</epage><pages>634-649</pages><issn>0028-646X</issn><issn>1469-8137</issn><eissn>1469-8137</eissn><abstract>Summary
Nitrogen is one of the most inaccessible plant nutrients, but certain species have overcome this limitation by establishing symbiotic interactions with nitrogen‐fixing bacteria in the root nodule. This root–nodule symbiosis (RNS) is restricted to species within a single clade of angiosperms, suggesting a critical, but undetermined, evolutionary event at the base of this clade.
To identify putative regulatory sequences implicated in the evolution of RNS, we evaluated the genomes of 25 species capable of nodulation and identified 3091 conserved noncoding sequences (CNS) in the nitrogen‐fixing clade (NFC).
We show that the chromatin accessibility of 452 CNS correlates significantly with the regulation of genes responding to lipochitooligosaccharides in Medicago truncatula. These included 38 CNS in proximity to 19 known genes involved in RNS. Five such regions are upstream of MtCRE1, Cytokinin Response Element 1, required to activate a suite of downstream transcription factors necessary for nodulation in M. truncatula. Genetic complementation of an Mtcre1 mutant showed a significant decrease of nodulation in the absence of the five CNS, when they are driving the expression of a functional copy of MtCRE1.
CNS identified in the NFC may harbor elements required for the regulation of genes controlling RNS in M. truncatula.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>35092309</pmid><doi>10.1111/nph.18006</doi><tpages>649</tpages><orcidid>https://orcid.org/0000-0002-3128-9439</orcidid><orcidid>https://orcid.org/0000-0003-1019-6281</orcidid><orcidid>https://orcid.org/0000-0002-3694-1705</orcidid><orcidid>https://orcid.org/0000-0002-8186-3945</orcidid><orcidid>https://orcid.org/0000-0003-0192-3336</orcidid><orcidid>https://orcid.org/0000-0002-5333-9273</orcidid><orcidid>https://orcid.org/0000-0001-8362-4190</orcidid><orcidid>https://orcid.org/0000-0001-7991-3977</orcidid><orcidid>https://orcid.org/0000-0002-2176-4232</orcidid><orcidid>https://orcid.org/0000-0002-1178-2517</orcidid><orcidid>https://orcid.org/0000-0003-3917-3219</orcidid><orcidid>https://orcid.org/0000000310196281</orcidid><orcidid>https://orcid.org/0000000221764232</orcidid><orcidid>https://orcid.org/0000000339173219</orcidid><orcidid>https://orcid.org/0000000236941705</orcidid><orcidid>https://orcid.org/0000000183624190</orcidid><orcidid>https://orcid.org/0000000253339273</orcidid><orcidid>https://orcid.org/0000000179913977</orcidid><orcidid>https://orcid.org/0000000211782517</orcidid><orcidid>https://orcid.org/0000000231289439</orcidid><orcidid>https://orcid.org/0000000301923336</orcidid><orcidid>https://orcid.org/0000000281863945</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alfalfa Angiosperms Chromatin comparative genomics Complementation conserved noncoding sequences (CNS) Cytokinins Fixing Gene Expression Regulation, Plant Gene regulation Genes Genomes Genomics Identification Medicago truncatula Medicago truncatula - microbiology MtCRE1 Nitrogen Nitrogen - metabolism nitrogen fixation Nitrogen Fixation - genetics Nitrogen-fixing bacteria Nodulation Nutrients Plant growth substances Plant Proteins - genetics Plant Proteins - metabolism Plant Root Nodulation - genetics Plant Sciences Regulatory sequences Root Nodules, Plant - microbiology Sinorhizobium meliloti Species Symbionts Symbiosis Symbiosis - genetics Transcription Transcription factors |
title | Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen‐fixing clade |
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