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Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal
Symbioses between the root nodule‐forming, nitrogen‐fixing actinomycete Frankia and its angiospermous host plants are important in the nitrogen economies of numerous terrestrial ecosystems. Molecular characterization of Frankia strains using polymerase chain reaction/restriction fragment length poly...
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Published in: | Environmental microbiology 1999-12, Vol.1 (6), p.525-533 |
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creator | Simonet, Pascal Navarro, Elisabeth Rouvier, Carole Reddell, Paul Zimpfer, Jeff Dommergues, Yvon Bardin, René Combarro, Pilar Hamelin, Jérôme Domenach, Anne-Marie Gourbière, François Prin, Yves Dawson, Jeffrey O. Normand, Philippe |
description | Symbioses between the root nodule‐forming, nitrogen‐fixing actinomycete Frankia and its angiospermous host plants are important in the nitrogen economies of numerous terrestrial ecosystems. Molecular characterization of Frankia strains using polymerase chain reaction/restriction fragment length polymorphism (PCR/RFLP) analyses of the 16S rRNA‐ITS gene and of the nifD–nifK spacer was conducted directly on root nodules collected worldwide from Casuarina and Allocasuarina trees. In their native habitats in Australia, host species contained seven distinctive sets of Frankia in seven different molecular phylogenetic groups. Where Casuarina and Allocasuarina trees are newly planted outside Australia, they do not normally nodulate unless Frankia is introduced with the host seedling. Nodules from Casuarina trees introduced outside Australia over the last two centuries were found to contain Frankia from only one of the seven phylogenetic groups associated with the host genus Casuarina in Australia. The phylogenetic group of Frankia found in Casuarina and Allocasuarina trees introduced outside Australia is the only group that has yielded isolates in pure culture, suggesting a greater ability to survive independently of a host. Furthermore, the Frankia species in this group are able to nodulate a wider range of host species than those in the other six groups. In baiting studies, Casuarina spp. are compatible with more Frankia microsymbiont groups than Allocasuarina host spp. adapted to drier soil conditions, and C. equisetifolia has broader microsymbiont compatibility than other Casuarina spp. Some Frankia associated with the nodular rhizosphere and rhizoplan, but not with the nodular tissue, of Australian hosts were able to nodulate cosmopolitan Myrica plants that have broad microsymbiont compatibility and, hence, are a potential host of Casuarinaceae‐infective Frankia outside the hosts' native range. The results are consistent with the idea that Frankia symbiotic promiscuity and ease of isolation on organic substrates, suggesting saprophytic potential, are associated with increased microsymbiont ability to disperse and adapt to diverse new environments, and that both genetics and environment determine a host's nodular microsymbiont. |
doi_str_mv | 10.1046/j.1462-2920.1999.00068.x |
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Molecular characterization of Frankia strains using polymerase chain reaction/restriction fragment length polymorphism (PCR/RFLP) analyses of the 16S rRNA‐ITS gene and of the nifD–nifK spacer was conducted directly on root nodules collected worldwide from Casuarina and Allocasuarina trees. In their native habitats in Australia, host species contained seven distinctive sets of Frankia in seven different molecular phylogenetic groups. Where Casuarina and Allocasuarina trees are newly planted outside Australia, they do not normally nodulate unless Frankia is introduced with the host seedling. Nodules from Casuarina trees introduced outside Australia over the last two centuries were found to contain Frankia from only one of the seven phylogenetic groups associated with the host genus Casuarina in Australia. The phylogenetic group of Frankia found in Casuarina and Allocasuarina trees introduced outside Australia is the only group that has yielded isolates in pure culture, suggesting a greater ability to survive independently of a host. Furthermore, the Frankia species in this group are able to nodulate a wider range of host species than those in the other six groups. In baiting studies, Casuarina spp. are compatible with more Frankia microsymbiont groups than Allocasuarina host spp. adapted to drier soil conditions, and C. equisetifolia has broader microsymbiont compatibility than other Casuarina spp. Some Frankia associated with the nodular rhizosphere and rhizoplan, but not with the nodular tissue, of Australian hosts were able to nodulate cosmopolitan Myrica plants that have broad microsymbiont compatibility and, hence, are a potential host of Casuarinaceae‐infective Frankia outside the hosts' native range. The results are consistent with the idea that Frankia symbiotic promiscuity and ease of isolation on organic substrates, suggesting saprophytic potential, are associated with increased microsymbiont ability to disperse and adapt to diverse new environments, and that both genetics and environment determine a host's nodular microsymbiont.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1046/j.1462-2920.1999.00068.x</identifier><identifier>PMID: 11207774</identifier><language>eng</language><publisher>Oxford BSL: Blackwell Science Ltd</publisher><subject>Actinomycetales - genetics ; Actinomycetales - physiology ; Biological Evolution ; DNA, Ribosomal Spacer - analysis ; Life Sciences ; Nitrogen Fixation ; Plant Roots - microbiology ; Polymerase Chain Reaction ; Polymorphism, Restriction Fragment Length ; RNA, Ribosomal, 16S - genetics ; Rosales - genetics ; Rosales - microbiology</subject><ispartof>Environmental microbiology, 1999-12, Vol.1 (6), p.525-533</ispartof><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4358-f5c5fe6e9741b5e0f92cc99804bab5cd2f3c57ad4101acc018eb2663511954c53</citedby><cites>FETCH-LOGICAL-c4358-f5c5fe6e9741b5e0f92cc99804bab5cd2f3c57ad4101acc018eb2663511954c53</cites><orcidid>0000-0002-2139-2141</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11207774$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://univ-lyon1.hal.science/hal-02868612$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Simonet, Pascal</creatorcontrib><creatorcontrib>Navarro, Elisabeth</creatorcontrib><creatorcontrib>Rouvier, Carole</creatorcontrib><creatorcontrib>Reddell, Paul</creatorcontrib><creatorcontrib>Zimpfer, Jeff</creatorcontrib><creatorcontrib>Dommergues, Yvon</creatorcontrib><creatorcontrib>Bardin, René</creatorcontrib><creatorcontrib>Combarro, Pilar</creatorcontrib><creatorcontrib>Hamelin, Jérôme</creatorcontrib><creatorcontrib>Domenach, Anne-Marie</creatorcontrib><creatorcontrib>Gourbière, François</creatorcontrib><creatorcontrib>Prin, Yves</creatorcontrib><creatorcontrib>Dawson, Jeffrey O.</creatorcontrib><creatorcontrib>Normand, Philippe</creatorcontrib><title>Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal</title><title>Environmental microbiology</title><addtitle>Environmental Microbiology</addtitle><description>Symbioses between the root nodule‐forming, nitrogen‐fixing actinomycete Frankia and its angiospermous host plants are important in the nitrogen economies of numerous terrestrial ecosystems. Molecular characterization of Frankia strains using polymerase chain reaction/restriction fragment length polymorphism (PCR/RFLP) analyses of the 16S rRNA‐ITS gene and of the nifD–nifK spacer was conducted directly on root nodules collected worldwide from Casuarina and Allocasuarina trees. In their native habitats in Australia, host species contained seven distinctive sets of Frankia in seven different molecular phylogenetic groups. Where Casuarina and Allocasuarina trees are newly planted outside Australia, they do not normally nodulate unless Frankia is introduced with the host seedling. Nodules from Casuarina trees introduced outside Australia over the last two centuries were found to contain Frankia from only one of the seven phylogenetic groups associated with the host genus Casuarina in Australia. The phylogenetic group of Frankia found in Casuarina and Allocasuarina trees introduced outside Australia is the only group that has yielded isolates in pure culture, suggesting a greater ability to survive independently of a host. Furthermore, the Frankia species in this group are able to nodulate a wider range of host species than those in the other six groups. In baiting studies, Casuarina spp. are compatible with more Frankia microsymbiont groups than Allocasuarina host spp. adapted to drier soil conditions, and C. equisetifolia has broader microsymbiont compatibility than other Casuarina spp. Some Frankia associated with the nodular rhizosphere and rhizoplan, but not with the nodular tissue, of Australian hosts were able to nodulate cosmopolitan Myrica plants that have broad microsymbiont compatibility and, hence, are a potential host of Casuarinaceae‐infective Frankia outside the hosts' native range. The results are consistent with the idea that Frankia symbiotic promiscuity and ease of isolation on organic substrates, suggesting saprophytic potential, are associated with increased microsymbiont ability to disperse and adapt to diverse new environments, and that both genetics and environment determine a host's nodular microsymbiont.</description><subject>Actinomycetales - genetics</subject><subject>Actinomycetales - physiology</subject><subject>Biological Evolution</subject><subject>DNA, Ribosomal Spacer - analysis</subject><subject>Life Sciences</subject><subject>Nitrogen Fixation</subject><subject>Plant Roots - microbiology</subject><subject>Polymerase Chain Reaction</subject><subject>Polymorphism, Restriction Fragment Length</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Rosales - genetics</subject><subject>Rosales - microbiology</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1999</creationdate><recordtype>article</recordtype><recordid>eNqNkk1v1DAQhiMEoqXwF5BPSByy2E7sJOJULf0SW5AQXzdr4kxYb71xsJN298ZPx2lWy5WTrZnnGWv0OkkIowtGc_lus2C55CmveCxUVbWglMpysXuSnB4bT493xk-SFyFsKGVFVtDnyQljnBZFkZ8mf5YuxXtnx8G4jtQ4PCB25NJDd2eA9K4fLUytQKBryNqFgfQWuiEQ05FhjaSFrbF7soQwgjcdaAR8ZHWU8PeIXTRgGNDHGa4lv6yrwZLGhB59APsyedaCDfjqcJ4l3y4vvi6v09Xnq5vl-SrVeSbKtBVatCixKnJWC6RtxbWuqpLmNdRCN7zNtCigyRlloDVlJdZcykwwVolci-wseTvPXYNVvTdb8HvlwKjr85WaapSXspSM37PIvpnZ3ru4QRjU1gSNNi6ObgxKVoKWBc8jWM6g9i4Ej-1xMqNqSkpt1BSCmgJRU1LqMSm1i-rrwxtjvcXmn3iIJgLvZ-DBWNz_92B1cXsjy2ins23CgLujDf5OyfgJhPrx6Up9FB9uv9OfUn3J_gIqxrJx</recordid><startdate>199912</startdate><enddate>199912</enddate><creator>Simonet, Pascal</creator><creator>Navarro, Elisabeth</creator><creator>Rouvier, Carole</creator><creator>Reddell, Paul</creator><creator>Zimpfer, Jeff</creator><creator>Dommergues, Yvon</creator><creator>Bardin, René</creator><creator>Combarro, Pilar</creator><creator>Hamelin, Jérôme</creator><creator>Domenach, Anne-Marie</creator><creator>Gourbière, François</creator><creator>Prin, Yves</creator><creator>Dawson, Jeffrey O.</creator><creator>Normand, Philippe</creator><general>Blackwell Science Ltd</general><general>Society for Applied Microbiology and Wiley-Blackwell</general><scope>BSCLL</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>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-2139-2141</orcidid></search><sort><creationdate>199912</creationdate><title>Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal</title><author>Simonet, Pascal ; 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Molecular characterization of Frankia strains using polymerase chain reaction/restriction fragment length polymorphism (PCR/RFLP) analyses of the 16S rRNA‐ITS gene and of the nifD–nifK spacer was conducted directly on root nodules collected worldwide from Casuarina and Allocasuarina trees. In their native habitats in Australia, host species contained seven distinctive sets of Frankia in seven different molecular phylogenetic groups. Where Casuarina and Allocasuarina trees are newly planted outside Australia, they do not normally nodulate unless Frankia is introduced with the host seedling. Nodules from Casuarina trees introduced outside Australia over the last two centuries were found to contain Frankia from only one of the seven phylogenetic groups associated with the host genus Casuarina in Australia. The phylogenetic group of Frankia found in Casuarina and Allocasuarina trees introduced outside Australia is the only group that has yielded isolates in pure culture, suggesting a greater ability to survive independently of a host. Furthermore, the Frankia species in this group are able to nodulate a wider range of host species than those in the other six groups. In baiting studies, Casuarina spp. are compatible with more Frankia microsymbiont groups than Allocasuarina host spp. adapted to drier soil conditions, and C. equisetifolia has broader microsymbiont compatibility than other Casuarina spp. Some Frankia associated with the nodular rhizosphere and rhizoplan, but not with the nodular tissue, of Australian hosts were able to nodulate cosmopolitan Myrica plants that have broad microsymbiont compatibility and, hence, are a potential host of Casuarinaceae‐infective Frankia outside the hosts' native range. The results are consistent with the idea that Frankia symbiotic promiscuity and ease of isolation on organic substrates, suggesting saprophytic potential, are associated with increased microsymbiont ability to disperse and adapt to diverse new environments, and that both genetics and environment determine a host's nodular microsymbiont.</abstract><cop>Oxford BSL</cop><pub>Blackwell Science Ltd</pub><pmid>11207774</pmid><doi>10.1046/j.1462-2920.1999.00068.x</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-2139-2141</orcidid></addata></record> |
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subjects | Actinomycetales - genetics Actinomycetales - physiology Biological Evolution DNA, Ribosomal Spacer - analysis Life Sciences Nitrogen Fixation Plant Roots - microbiology Polymerase Chain Reaction Polymorphism, Restriction Fragment Length RNA, Ribosomal, 16S - genetics Rosales - genetics Rosales - microbiology |
title | Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal |
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