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Intra and Inter-Spore Variability in Rhizophagus irregularis AOX Gene
Arbuscular mycorrhizal fungi (AMF) are root-inhabiting fungi that form mutualistic symbioses with their host plants. AMF symbiosis improves nutrient uptake and buffers the plant against a diversity of stresses. Rhizophagus irregularis is one of the most widespread AMF species in the world, and its a...
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Published in: | PloS one 2015-11, Vol.10 (11), p.e0142339-e0142339 |
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description | Arbuscular mycorrhizal fungi (AMF) are root-inhabiting fungi that form mutualistic symbioses with their host plants. AMF symbiosis improves nutrient uptake and buffers the plant against a diversity of stresses. Rhizophagus irregularis is one of the most widespread AMF species in the world, and its application in agricultural systems for yield improvement has increased over the last years. Still, from the inoculum production perspective, a lack of consistency of inoculum quality is referred to, which partially may be due to a high genetic variability of the fungus. The alternative oxidase (AOX) is an enzyme of the alternative respiratory chain already described in different taxa, including various fungi, which decreases the damage caused by oxidative stress. Nevertheless, virtually nothing is known on the involvement of AMF AOX on symbiosis establishment, as well on the existence of AOX variability that could affect AMF effectiveness and consequently plant performance. Here, we report the isolation and characterisation of the AOX gene of R. irregularis (RiAOX), and show that it is highly expressed during early phases of the symbiosis with plant roots. Phylogenetic analysis clustered RiAOX sequence with ancient fungi, and multiple sequence alignment revealed the lack of several regulatory motifs which are present in plant AOX. The analysis of RiAOX polymorphisms in single spores of three different isolates showed a reduced variability in one spore relatively to a group of spores. A high number of polymorphisms occurred in introns; nevertheless, some putative amino acid changes resulting from non-synonymous variants were found, offering a basis for selective pressure to occur within the populations. Given the AOX relatedness with stress responses, differences in gene variants amongst R. irregularis isolates are likely to be related with its origin and environmental constraints and might have a potential impact on inoculum production. |
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AMF symbiosis improves nutrient uptake and buffers the plant against a diversity of stresses. Rhizophagus irregularis is one of the most widespread AMF species in the world, and its application in agricultural systems for yield improvement has increased over the last years. Still, from the inoculum production perspective, a lack of consistency of inoculum quality is referred to, which partially may be due to a high genetic variability of the fungus. The alternative oxidase (AOX) is an enzyme of the alternative respiratory chain already described in different taxa, including various fungi, which decreases the damage caused by oxidative stress. Nevertheless, virtually nothing is known on the involvement of AMF AOX on symbiosis establishment, as well on the existence of AOX variability that could affect AMF effectiveness and consequently plant performance. Here, we report the isolation and characterisation of the AOX gene of R. irregularis (RiAOX), and show that it is highly expressed during early phases of the symbiosis with plant roots. Phylogenetic analysis clustered RiAOX sequence with ancient fungi, and multiple sequence alignment revealed the lack of several regulatory motifs which are present in plant AOX. The analysis of RiAOX polymorphisms in single spores of three different isolates showed a reduced variability in one spore relatively to a group of spores. A high number of polymorphisms occurred in introns; nevertheless, some putative amino acid changes resulting from non-synonymous variants were found, offering a basis for selective pressure to occur within the populations. Given the AOX relatedness with stress responses, differences in gene variants amongst R. irregularis isolates are likely to be related with its origin and environmental constraints and might have a potential impact on inoculum production.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0142339</identifier><identifier>PMID: 26540237</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Alternative oxidase ; Amino acid sequence ; Arbuscular mycorrhizas ; Crop yield ; Curie, Marie (1867-1934) ; Electron transport ; Enzymes ; Fungi ; Gene expression ; Genetic diversity ; Genetic variability ; Genomics ; Glomeromycota ; Host plants ; Hypotheses ; Inoculum ; Introns ; Mitochondrial Proteins - genetics ; Mycorrhizae - genetics ; Nucleotide sequence ; Nutrient uptake ; Oxidative stress ; Oxidoreductases - genetics ; Phylogeny ; Plant diversity ; Plant Proteins - genetics ; Plant roots ; Plant Roots - genetics ; Plant Roots - microbiology ; Plants - genetics ; Plants - microbiology ; Quality ; Regulatory sequences ; Respiration ; Rhizophagus irregularis ; Spores ; Spores, Fungal - genetics ; Symbiosis ; Symbiosis - genetics ; Taxa ; Variability</subject><ispartof>PloS one, 2015-11, Vol.10 (11), p.e0142339-e0142339</ispartof><rights>2015 Campos et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Campos et al 2015 Campos et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-bcd1aa3628a0797d09b7262fad1f347b078af908fcbadaf56dd294949a264ba13</citedby><cites>FETCH-LOGICAL-c526t-bcd1aa3628a0797d09b7262fad1f347b078af908fcbadaf56dd294949a264ba13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1730683549/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1730683549?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26540237$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Yu, Jae-Hyuk</contributor><creatorcontrib>Campos, Catarina</creatorcontrib><creatorcontrib>Cardoso, Hélia</creatorcontrib><creatorcontrib>Nogales, Amaia</creatorcontrib><creatorcontrib>Svensson, Jan</creatorcontrib><creatorcontrib>Lopez-Ráez, Juan Antonio</creatorcontrib><creatorcontrib>Pozo, María José</creatorcontrib><creatorcontrib>Nobre, Tânia</creatorcontrib><creatorcontrib>Schneider, Carolin</creatorcontrib><creatorcontrib>Arnholdt-Schmitt, Birgit</creatorcontrib><title>Intra and Inter-Spore Variability in Rhizophagus irregularis AOX Gene</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Arbuscular mycorrhizal fungi (AMF) are root-inhabiting fungi that form mutualistic symbioses with their host plants. AMF symbiosis improves nutrient uptake and buffers the plant against a diversity of stresses. Rhizophagus irregularis is one of the most widespread AMF species in the world, and its application in agricultural systems for yield improvement has increased over the last years. Still, from the inoculum production perspective, a lack of consistency of inoculum quality is referred to, which partially may be due to a high genetic variability of the fungus. The alternative oxidase (AOX) is an enzyme of the alternative respiratory chain already described in different taxa, including various fungi, which decreases the damage caused by oxidative stress. Nevertheless, virtually nothing is known on the involvement of AMF AOX on symbiosis establishment, as well on the existence of AOX variability that could affect AMF effectiveness and consequently plant performance. Here, we report the isolation and characterisation of the AOX gene of R. irregularis (RiAOX), and show that it is highly expressed during early phases of the symbiosis with plant roots. Phylogenetic analysis clustered RiAOX sequence with ancient fungi, and multiple sequence alignment revealed the lack of several regulatory motifs which are present in plant AOX. The analysis of RiAOX polymorphisms in single spores of three different isolates showed a reduced variability in one spore relatively to a group of spores. A high number of polymorphisms occurred in introns; nevertheless, some putative amino acid changes resulting from non-synonymous variants were found, offering a basis for selective pressure to occur within the populations. Given the AOX relatedness with stress responses, differences in gene variants amongst R. irregularis isolates are likely to be related with its origin and environmental constraints and might have a potential impact on inoculum production.</description><subject>Alternative oxidase</subject><subject>Amino acid sequence</subject><subject>Arbuscular mycorrhizas</subject><subject>Crop yield</subject><subject>Curie, Marie (1867-1934)</subject><subject>Electron transport</subject><subject>Enzymes</subject><subject>Fungi</subject><subject>Gene expression</subject><subject>Genetic diversity</subject><subject>Genetic variability</subject><subject>Genomics</subject><subject>Glomeromycota</subject><subject>Host plants</subject><subject>Hypotheses</subject><subject>Inoculum</subject><subject>Introns</subject><subject>Mitochondrial Proteins - genetics</subject><subject>Mycorrhizae - genetics</subject><subject>Nucleotide sequence</subject><subject>Nutrient uptake</subject><subject>Oxidative stress</subject><subject>Oxidoreductases - genetics</subject><subject>Phylogeny</subject><subject>Plant diversity</subject><subject>Plant Proteins - genetics</subject><subject>Plant roots</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - microbiology</subject><subject>Plants - genetics</subject><subject>Plants - microbiology</subject><subject>Quality</subject><subject>Regulatory sequences</subject><subject>Respiration</subject><subject>Rhizophagus irregularis</subject><subject>Spores</subject><subject>Spores, Fungal - genetics</subject><subject>Symbiosis</subject><subject>Symbiosis - genetics</subject><subject>Taxa</subject><subject>Variability</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkstq3DAUhk1padKkb1BaQzfZeKqbJWtTCCFJBwKBtgnZiWNdZjR4LFeyC-nTV5NxQlKKFjpI3_nPhb8oPmC0wFTgL5swxR66xRB6u0CYEUrlq-IQS0oqThB9_Sw-KN6ltEGopg3nb4sDwmuGCBWHxfmyHyOU0JsyRzZWP4YQbXkL0UPrOz_el74vv6_9nzCsYTWl0sdoV1OXgVSeXt-Vl7a3x8UbB12y7-f7qLi5OP959q26ur5cnp1eVbomfKxabTAA5aQBJKQwSLaCcOLAYEeZaJFowEnUON2CAVdzY4hk-QDhrAVMj4pPe92hC0nNG0gKC4p4Q2smM7HcEybARg3RbyHeqwBePTyEuFIQR687q8BxiV3WdYywRvLGWAnYaUFqSrXjWevrXG1qt9Zou1tV90L05U_v12oVfivGKZMNygIns0AMvyabRrX1Sduug96G6aFvLJqaMpbRz_-g_5-O7SkdQ0rRuqdmMFI7VzxmqZ0r1OyKnPbx-SBPSY82oH8BbQi1kg</recordid><startdate>20151105</startdate><enddate>20151105</enddate><creator>Campos, Catarina</creator><creator>Cardoso, Hélia</creator><creator>Nogales, Amaia</creator><creator>Svensson, Jan</creator><creator>Lopez-Ráez, Juan Antonio</creator><creator>Pozo, María José</creator><creator>Nobre, Tânia</creator><creator>Schneider, Carolin</creator><creator>Arnholdt-Schmitt, Birgit</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20151105</creationdate><title>Intra and Inter-Spore Variability in Rhizophagus irregularis AOX Gene</title><author>Campos, Catarina ; Cardoso, Hélia ; Nogales, Amaia ; Svensson, Jan ; Lopez-Ráez, Juan Antonio ; Pozo, María José ; Nobre, Tânia ; Schneider, Carolin ; Arnholdt-Schmitt, Birgit</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-bcd1aa3628a0797d09b7262fad1f347b078af908fcbadaf56dd294949a264ba13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Alternative oxidase</topic><topic>Amino acid sequence</topic><topic>Arbuscular mycorrhizas</topic><topic>Crop yield</topic><topic>Curie, Marie (1867-1934)</topic><topic>Electron transport</topic><topic>Enzymes</topic><topic>Fungi</topic><topic>Gene expression</topic><topic>Genetic diversity</topic><topic>Genetic variability</topic><topic>Genomics</topic><topic>Glomeromycota</topic><topic>Host plants</topic><topic>Hypotheses</topic><topic>Inoculum</topic><topic>Introns</topic><topic>Mitochondrial Proteins - genetics</topic><topic>Mycorrhizae - genetics</topic><topic>Nucleotide sequence</topic><topic>Nutrient uptake</topic><topic>Oxidative stress</topic><topic>Oxidoreductases - genetics</topic><topic>Phylogeny</topic><topic>Plant diversity</topic><topic>Plant Proteins - genetics</topic><topic>Plant roots</topic><topic>Plant Roots - genetics</topic><topic>Plant Roots - microbiology</topic><topic>Plants - genetics</topic><topic>Plants - microbiology</topic><topic>Quality</topic><topic>Regulatory sequences</topic><topic>Respiration</topic><topic>Rhizophagus irregularis</topic><topic>Spores</topic><topic>Spores, Fungal - genetics</topic><topic>Symbiosis</topic><topic>Symbiosis - genetics</topic><topic>Taxa</topic><topic>Variability</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Campos, Catarina</creatorcontrib><creatorcontrib>Cardoso, Hélia</creatorcontrib><creatorcontrib>Nogales, Amaia</creatorcontrib><creatorcontrib>Svensson, Jan</creatorcontrib><creatorcontrib>Lopez-Ráez, Juan Antonio</creatorcontrib><creatorcontrib>Pozo, María José</creatorcontrib><creatorcontrib>Nobre, Tânia</creatorcontrib><creatorcontrib>Schneider, Carolin</creatorcontrib><creatorcontrib>Arnholdt-Schmitt, Birgit</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database (ProQuest)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database (Proquest)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Campos, Catarina</au><au>Cardoso, Hélia</au><au>Nogales, Amaia</au><au>Svensson, Jan</au><au>Lopez-Ráez, Juan Antonio</au><au>Pozo, María José</au><au>Nobre, Tânia</au><au>Schneider, Carolin</au><au>Arnholdt-Schmitt, Birgit</au><au>Yu, Jae-Hyuk</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Intra and Inter-Spore Variability in Rhizophagus irregularis AOX Gene</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-11-05</date><risdate>2015</risdate><volume>10</volume><issue>11</issue><spage>e0142339</spage><epage>e0142339</epage><pages>e0142339-e0142339</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Arbuscular mycorrhizal fungi (AMF) are root-inhabiting fungi that form mutualistic symbioses with their host plants. AMF symbiosis improves nutrient uptake and buffers the plant against a diversity of stresses. Rhizophagus irregularis is one of the most widespread AMF species in the world, and its application in agricultural systems for yield improvement has increased over the last years. Still, from the inoculum production perspective, a lack of consistency of inoculum quality is referred to, which partially may be due to a high genetic variability of the fungus. The alternative oxidase (AOX) is an enzyme of the alternative respiratory chain already described in different taxa, including various fungi, which decreases the damage caused by oxidative stress. Nevertheless, virtually nothing is known on the involvement of AMF AOX on symbiosis establishment, as well on the existence of AOX variability that could affect AMF effectiveness and consequently plant performance. Here, we report the isolation and characterisation of the AOX gene of R. irregularis (RiAOX), and show that it is highly expressed during early phases of the symbiosis with plant roots. Phylogenetic analysis clustered RiAOX sequence with ancient fungi, and multiple sequence alignment revealed the lack of several regulatory motifs which are present in plant AOX. The analysis of RiAOX polymorphisms in single spores of three different isolates showed a reduced variability in one spore relatively to a group of spores. A high number of polymorphisms occurred in introns; nevertheless, some putative amino acid changes resulting from non-synonymous variants were found, offering a basis for selective pressure to occur within the populations. Given the AOX relatedness with stress responses, differences in gene variants amongst R. irregularis isolates are likely to be related with its origin and environmental constraints and might have a potential impact on inoculum production.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26540237</pmid><doi>10.1371/journal.pone.0142339</doi><oa>free_for_read</oa></addata></record> |
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subjects | Alternative oxidase Amino acid sequence Arbuscular mycorrhizas Crop yield Curie, Marie (1867-1934) Electron transport Enzymes Fungi Gene expression Genetic diversity Genetic variability Genomics Glomeromycota Host plants Hypotheses Inoculum Introns Mitochondrial Proteins - genetics Mycorrhizae - genetics Nucleotide sequence Nutrient uptake Oxidative stress Oxidoreductases - genetics Phylogeny Plant diversity Plant Proteins - genetics Plant roots Plant Roots - genetics Plant Roots - microbiology Plants - genetics Plants - microbiology Quality Regulatory sequences Respiration Rhizophagus irregularis Spores Spores, Fungal - genetics Symbiosis Symbiosis - genetics Taxa Variability |
title | Intra and Inter-Spore Variability in Rhizophagus irregularis AOX Gene |
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