Passion fruit plants alter the soil microbial community with continuous cropping and improve plant disease resistance by recruiting beneficial microorganisms

Passion fruit (Passiflora edulis) is widely grown in tropical and subtropical regions, showing high economic and ornamental value. Microorganisms are indicators for the stability and health of the soil ecosystem, which can affect the yield and quality of passion fruit under continuous cropping. High...

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Veröffentlicht in:PloS one 2023-02, Vol.18 (2), p.e0281854-e0281854
Hauptverfasser: Wang, Ye, Teng, Yao, Zhang, Jianli, Zhang, Zixiong, Wang, Chen, Wu, Xiukun, Long, Xiuqin
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Teng, Yao
Zhang, Jianli
Zhang, Zixiong
Wang, Chen
Wu, Xiukun
Long, Xiuqin
description Passion fruit (Passiflora edulis) is widely grown in tropical and subtropical regions, showing high economic and ornamental value. Microorganisms are indicators for the stability and health of the soil ecosystem, which can affect the yield and quality of passion fruit under continuous cropping. High-throughput sequencing and interactive analysis were used to analyse the variation of microbial communities in the noncultivated soil (NCS), cultivated soil (CS), and the rhizosphere soil of purple passion fruit (Passiflora edulis f. edulis ×Passiflora edulis f. flavicarpa, RP) and yellow passion fruit (Passiflora edulis f. flavicarpa, RY). An average of 98,001 high-quality fungal internal transcribed spacer (ITS) sequences, mainly from Ascomycota, Basidiomycota, Mortierellomycota, Mucoromycota and Glomeromycota, as well as an average of 71,299 high-quality bacterial 16S rRNA sequences, mainly from Proteobacteria, Actinobacteria, Acidobacteria, Firmicutes and Chloroflexi, were obtained per sample. It was found that the continuous cropping of passion fruit increased the richness but reduced the diversity of soil fungi, while it dramatically increased the richness and diversity of soil bacteria. In addition, during the continuous cropping, grafting different scions in the same rootstock contributed to the aggregation of differential rhizosphere microbial communities. Among fungal genera, Trichoderma showed higher abundance in RY than in RP and CS, while the opposite was observed in the pathogen Fusarium. Moreover, the co-occurrence network and potential function analyses also showed that the appearance of Trichoderma was related to Fusarium and its contribution to plant metabolism was significantly greater in RY than in RP and CS. In conclusion, the rhizosphere of yellow passion fruit may be beneficial for the enrichment of disease-resistant microbes, such as Trichoderma, which may be an important factor inducing stronger resistance to stem rot. It will help to form a potential strategy for overcoming the pathogen-mediated obstacles in passion fruit and improve its yield and quality.
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Microorganisms are indicators for the stability and health of the soil ecosystem, which can affect the yield and quality of passion fruit under continuous cropping. High-throughput sequencing and interactive analysis were used to analyse the variation of microbial communities in the noncultivated soil (NCS), cultivated soil (CS), and the rhizosphere soil of purple passion fruit (Passiflora edulis f. edulis ×Passiflora edulis f. flavicarpa, RP) and yellow passion fruit (Passiflora edulis f. flavicarpa, RY). An average of 98,001 high-quality fungal internal transcribed spacer (ITS) sequences, mainly from Ascomycota, Basidiomycota, Mortierellomycota, Mucoromycota and Glomeromycota, as well as an average of 71,299 high-quality bacterial 16S rRNA sequences, mainly from Proteobacteria, Actinobacteria, Acidobacteria, Firmicutes and Chloroflexi, were obtained per sample. It was found that the continuous cropping of passion fruit increased the richness but reduced the diversity of soil fungi, while it dramatically increased the richness and diversity of soil bacteria. In addition, during the continuous cropping, grafting different scions in the same rootstock contributed to the aggregation of differential rhizosphere microbial communities. Among fungal genera, Trichoderma showed higher abundance in RY than in RP and CS, while the opposite was observed in the pathogen Fusarium. Moreover, the co-occurrence network and potential function analyses also showed that the appearance of Trichoderma was related to Fusarium and its contribution to plant metabolism was significantly greater in RY than in RP and CS. In conclusion, the rhizosphere of yellow passion fruit may be beneficial for the enrichment of disease-resistant microbes, such as Trichoderma, which may be an important factor inducing stronger resistance to stem rot. It will help to form a potential strategy for overcoming the pathogen-mediated obstacles in passion fruit and improve its yield and quality.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0281854</identifier><identifier>PMID: 36809377</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Ascomycota - genetics ; Bacteria ; Bar codes ; Biology and Life Sciences ; Continuous cropping ; Cropping systems ; Deoxyribonucleic acid ; Disease Resistance ; Diseases and pests ; DNA ; Drug resistance in microorganisms ; Earth Sciences ; Ecology and Environmental Sciences ; Environmental aspects ; Fruit ; Fruits ; Fungi ; Fusarium ; Fusarium - genetics ; Growth ; Loam soils ; Medicine and Health Sciences ; Methods ; Microbial activity ; Microbiomes ; Microbiota ; Microorganisms ; Next-generation sequencing ; Passiflora - genetics ; Passiflora edulis ; Passion fruit ; Pathogens ; Plant diseases ; Plant immunity ; Plant metabolism ; Prevention ; Probiotics ; Resistance factors ; Rhizosphere ; RNA, Ribosomal, 16S - genetics ; rRNA 16S ; Scions ; Soil ; Soil bacteria ; Soil Microbiology ; Soil microorganisms ; Soil stability ; Soils ; Stem rot ; Trichoderma</subject><ispartof>PloS one, 2023-02, Vol.18 (2), p.e0281854-e0281854</ispartof><rights>Copyright: © 2023 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Wang 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>2023 Wang et al 2023 Wang et al</rights><rights>2023 Wang et al. 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Microorganisms are indicators for the stability and health of the soil ecosystem, which can affect the yield and quality of passion fruit under continuous cropping. High-throughput sequencing and interactive analysis were used to analyse the variation of microbial communities in the noncultivated soil (NCS), cultivated soil (CS), and the rhizosphere soil of purple passion fruit (Passiflora edulis f. edulis ×Passiflora edulis f. flavicarpa, RP) and yellow passion fruit (Passiflora edulis f. flavicarpa, RY). An average of 98,001 high-quality fungal internal transcribed spacer (ITS) sequences, mainly from Ascomycota, Basidiomycota, Mortierellomycota, Mucoromycota and Glomeromycota, as well as an average of 71,299 high-quality bacterial 16S rRNA sequences, mainly from Proteobacteria, Actinobacteria, Acidobacteria, Firmicutes and Chloroflexi, were obtained per sample. 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It will help to form a potential strategy for overcoming the pathogen-mediated obstacles in passion fruit and improve its yield and quality.</description><subject>Analysis</subject><subject>Ascomycota - genetics</subject><subject>Bacteria</subject><subject>Bar codes</subject><subject>Biology and Life Sciences</subject><subject>Continuous cropping</subject><subject>Cropping systems</subject><subject>Deoxyribonucleic acid</subject><subject>Disease Resistance</subject><subject>Diseases and pests</subject><subject>DNA</subject><subject>Drug resistance in microorganisms</subject><subject>Earth Sciences</subject><subject>Ecology and Environmental Sciences</subject><subject>Environmental aspects</subject><subject>Fruit</subject><subject>Fruits</subject><subject>Fungi</subject><subject>Fusarium</subject><subject>Fusarium - genetics</subject><subject>Growth</subject><subject>Loam soils</subject><subject>Medicine and Health Sciences</subject><subject>Methods</subject><subject>Microbial activity</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microorganisms</subject><subject>Next-generation sequencing</subject><subject>Passiflora - genetics</subject><subject>Passiflora edulis</subject><subject>Passion fruit</subject><subject>Pathogens</subject><subject>Plant diseases</subject><subject>Plant immunity</subject><subject>Plant metabolism</subject><subject>Prevention</subject><subject>Probiotics</subject><subject>Resistance factors</subject><subject>Rhizosphere</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>rRNA 16S</subject><subject>Scions</subject><subject>Soil</subject><subject>Soil bacteria</subject><subject>Soil Microbiology</subject><subject>Soil microorganisms</subject><subject>Soil stability</subject><subject>Soils</subject><subject>Stem rot</subject><subject>Trichoderma</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk8tu1DAUhiMEoqXwBggsISFYzGDHdhxvkKqKS6VKRdy2luOczLhK7NR2CvMwvCtOZ1p1UBcoC8f2d_7jcyuK5wQvCRXk3YWfgtP9cvQOlrisSc3Zg-KQSFouqhLTh3f-D4onMV5gzGldVY-LA1rVWFIhDos_X3SM1jvUhckmNPbapYh0nyCgtAYUve3RYE3wjdU9Mn4YJmfTBv2yaZ23Llk3-SmiTIyjdSukXYvsMAZ_BVs51NoIOgIKEG1M2hlAzSbvzOxyNmnAQWfN7ODalQ8r7Wwc4tPiUaf7CM9261Hx4-OH7yefF2fnn05Pjs8WppJlWoCgDdQUaMcYk4wDqYAyQWkJvKxKwQWwpm0w6yTpmgp0VTJSdaWRhEswgh4VL7e6Y--j2mU2qlKImmc9JjNxuiVary_UGOygw0Z5bdX1QX6x0iFZ04PirZCyagiUjWa05ZoA5qwTkhvemrLNWu933qZmgNaAS0H3e6L7N86u1cpfKSkZxZhkgTc7geAvJ4hJDTYa6HO2Idfi-t2yxkzMkb36B70_uh210jkA6zqf_ZpZVB0LWuOasJpnankPlb8Wctn8XMN8vmfwds9gbhf4nVZ6ilGdfvv6_-z5z3329R12Dbld19H3U8qNHPdBtgVzU8UYoLtNMsFqnqKbbKh5itRuirLZi7sFujW6GRv6FwUZG-M</recordid><startdate>20230221</startdate><enddate>20230221</enddate><creator>Wang, Ye</creator><creator>Teng, Yao</creator><creator>Zhang, Jianli</creator><creator>Zhang, Zixiong</creator><creator>Wang, Chen</creator><creator>Wu, Xiukun</creator><creator>Long, Xiuqin</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>IOV</scope><scope>ISR</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>AEUYN</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>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-3167-2542</orcidid></search><sort><creationdate>20230221</creationdate><title>Passion fruit plants alter the soil microbial community with continuous cropping and improve plant disease resistance by recruiting beneficial microorganisms</title><author>Wang, Ye ; Teng, Yao ; Zhang, Jianli ; Zhang, Zixiong ; Wang, Chen ; Wu, Xiukun ; Long, Xiuqin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-e73be83e3f444945e16e347332e5262757e4bdb04f91fb6ea62416f2c9159ec73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Analysis</topic><topic>Ascomycota - 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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>Wang, Ye</au><au>Teng, Yao</au><au>Zhang, Jianli</au><au>Zhang, Zixiong</au><au>Wang, Chen</au><au>Wu, Xiukun</au><au>Long, Xiuqin</au><au>Arif, Muhammad</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Passion fruit plants alter the soil microbial community with continuous cropping and improve plant disease resistance by recruiting beneficial microorganisms</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-02-21</date><risdate>2023</risdate><volume>18</volume><issue>2</issue><spage>e0281854</spage><epage>e0281854</epage><pages>e0281854-e0281854</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Passion fruit (Passiflora edulis) is widely grown in tropical and subtropical regions, showing high economic and ornamental value. Microorganisms are indicators for the stability and health of the soil ecosystem, which can affect the yield and quality of passion fruit under continuous cropping. High-throughput sequencing and interactive analysis were used to analyse the variation of microbial communities in the noncultivated soil (NCS), cultivated soil (CS), and the rhizosphere soil of purple passion fruit (Passiflora edulis f. edulis ×Passiflora edulis f. flavicarpa, RP) and yellow passion fruit (Passiflora edulis f. flavicarpa, RY). An average of 98,001 high-quality fungal internal transcribed spacer (ITS) sequences, mainly from Ascomycota, Basidiomycota, Mortierellomycota, Mucoromycota and Glomeromycota, as well as an average of 71,299 high-quality bacterial 16S rRNA sequences, mainly from Proteobacteria, Actinobacteria, Acidobacteria, Firmicutes and Chloroflexi, were obtained per sample. It was found that the continuous cropping of passion fruit increased the richness but reduced the diversity of soil fungi, while it dramatically increased the richness and diversity of soil bacteria. In addition, during the continuous cropping, grafting different scions in the same rootstock contributed to the aggregation of differential rhizosphere microbial communities. Among fungal genera, Trichoderma showed higher abundance in RY than in RP and CS, while the opposite was observed in the pathogen Fusarium. Moreover, the co-occurrence network and potential function analyses also showed that the appearance of Trichoderma was related to Fusarium and its contribution to plant metabolism was significantly greater in RY than in RP and CS. In conclusion, the rhizosphere of yellow passion fruit may be beneficial for the enrichment of disease-resistant microbes, such as Trichoderma, which may be an important factor inducing stronger resistance to stem rot. It will help to form a potential strategy for overcoming the pathogen-mediated obstacles in passion fruit and improve its yield and quality.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>36809377</pmid><doi>10.1371/journal.pone.0281854</doi><tpages>e0281854</tpages><orcidid>https://orcid.org/0000-0002-3167-2542</orcidid><oa>free_for_read</oa></addata></record>
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ispartof PloS one, 2023-02, Vol.18 (2), p.e0281854-e0281854
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1932-6203
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source MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry
subjects Analysis
Ascomycota - genetics
Bacteria
Bar codes
Biology and Life Sciences
Continuous cropping
Cropping systems
Deoxyribonucleic acid
Disease Resistance
Diseases and pests
DNA
Drug resistance in microorganisms
Earth Sciences
Ecology and Environmental Sciences
Environmental aspects
Fruit
Fruits
Fungi
Fusarium
Fusarium - genetics
Growth
Loam soils
Medicine and Health Sciences
Methods
Microbial activity
Microbiomes
Microbiota
Microorganisms
Next-generation sequencing
Passiflora - genetics
Passiflora edulis
Passion fruit
Pathogens
Plant diseases
Plant immunity
Plant metabolism
Prevention
Probiotics
Resistance factors
Rhizosphere
RNA, Ribosomal, 16S - genetics
rRNA 16S
Scions
Soil
Soil bacteria
Soil Microbiology
Soil microorganisms
Soil stability
Soils
Stem rot
Trichoderma
title Passion fruit plants alter the soil microbial community with continuous cropping and improve plant disease resistance by recruiting beneficial microorganisms
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