The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilization

Interactions between endophytes (endophytic bacteria and fungi) and plants are crucial in maintaining crop fitness in agricultural systems, particularly in relation to abundant and rare subcommunities involved in community construction. However, the influence of long-term fertilization on heterogene...

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Main Authors: Xiaoxia Li, Muhammad Awais, Shuang Wang, Zhu Zhang, Shuning Zhao, Yufeng Liu, Zhouping Sun, Hongdan Fu, Tianlai Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1487323/full
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author Xiaoxia Li
Xiaoxia Li
Xiaoxia Li
Muhammad Awais
Muhammad Awais
Muhammad Awais
Shuang Wang
Shuang Wang
Shuang Wang
Shuang Wang
Zhu Zhang
Zhu Zhang
Zhu Zhang
Shuning Zhao
Shuning Zhao
Shuning Zhao
Yufeng Liu
Yufeng Liu
Yufeng Liu
Zhouping Sun
Zhouping Sun
Zhouping Sun
Hongdan Fu
Hongdan Fu
Hongdan Fu
Tianlai Li
Tianlai Li
Tianlai Li
author_facet Xiaoxia Li
Xiaoxia Li
Xiaoxia Li
Muhammad Awais
Muhammad Awais
Muhammad Awais
Shuang Wang
Shuang Wang
Shuang Wang
Shuang Wang
Zhu Zhang
Zhu Zhang
Zhu Zhang
Shuning Zhao
Shuning Zhao
Shuning Zhao
Yufeng Liu
Yufeng Liu
Yufeng Liu
Zhouping Sun
Zhouping Sun
Zhouping Sun
Hongdan Fu
Hongdan Fu
Hongdan Fu
Tianlai Li
Tianlai Li
Tianlai Li
author_sort Xiaoxia Li
collection DOAJ
description Interactions between endophytes (endophytic bacteria and fungi) and plants are crucial in maintaining crop fitness in agricultural systems, particularly in relation to abundant and rare subcommunities involved in community construction. However, the influence of long-term fertilization on heterogeneous rhizosphere nitrogen and phosphorus environments and how these conditions affect the key subcommunities of root endophytes and their community assembly mechanisms remain unclear. We studied the 26th year of a field experiment conducted in a greenhouse with varying levels of nitrogen and phosphorus (CKP0, CKP1, CNP0, CNP1, ONP0, and ONP1) to assess the composition of tomato root endophytes and their impact on yield. We employed 16S rRNA and fungal ITS region amplicon sequencing to investigate the assembly mechanisms of abundant and rare endophytic subcommunities, network correlations, core subcommunity structures, and key species that enhance crop yield. The results indicated that organic manure and phosphorus fertilizers significantly increased the rhizosphere soil nitrogen content, phosphorus content, and phosphorus availability (labile P, moderately labile P, and non-labile P). These fertilizers also significantly affected the composition (based on Bray-Curtis distance) and community assembly processes (βNTI) of endophytic microbial subcommunities. The assembly of both bacterial and fungal subcommunities was primarily governed by dispersal limitation, with community structures being significantly regulated by the content of rhizosphere soil available nitrogen (AN) and moderately labile P (MLP). Rare bacterial and fungal subcommunities complemented the ecological niches of abundant subcommunities in the co-occurrence network, supporting community functions and enhancing network stability. Nitrogen-adapting abundant and rare bacterial subcommunities provided a stronger predictive correlation for tomato yield than phosphorus-adapting fungal subcommunities. Additionally, three core genera of rare endophytic bacteria such as Arthrobacter, Microbacterium, and Sphingobium were identified as potentially involved in improving crop yield improvement. These findings revealed the distinct assembly mechanisms of endophytic microbial subcommunities affected by fertilization, enhancing our understanding of better management practices and controlling endophytes to improve crop yield in intensive agricultural ecosystems.
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spelling doaj-art-51f1b5b0f86642dea806a6d3d2478d1c2025-01-17T06:51:10ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.14873231487323The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilizationXiaoxia Li0Xiaoxia Li1Xiaoxia Li2Muhammad Awais3Muhammad Awais4Muhammad Awais5Shuang Wang6Shuang Wang7Shuang Wang8Shuang Wang9Zhu Zhang10Zhu Zhang11Zhu Zhang12Shuning Zhao13Shuning Zhao14Shuning Zhao15Yufeng Liu16Yufeng Liu17Yufeng Liu18Zhouping Sun19Zhouping Sun20Zhouping Sun21Hongdan Fu22Hongdan Fu23Hongdan Fu24Tianlai Li25Tianlai Li26Tianlai Li27College of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Agriculture, Eastern Liaoning University, Dandong, Liaoning, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture of Education Ministry and Liaoning Province, Shenyang, ChinaNational and Local Joint Engineering Research Center of Northern Horticultural Facilities Design and Application Technology, Shenyang, ChinaInteractions between endophytes (endophytic bacteria and fungi) and plants are crucial in maintaining crop fitness in agricultural systems, particularly in relation to abundant and rare subcommunities involved in community construction. However, the influence of long-term fertilization on heterogeneous rhizosphere nitrogen and phosphorus environments and how these conditions affect the key subcommunities of root endophytes and their community assembly mechanisms remain unclear. We studied the 26th year of a field experiment conducted in a greenhouse with varying levels of nitrogen and phosphorus (CKP0, CKP1, CNP0, CNP1, ONP0, and ONP1) to assess the composition of tomato root endophytes and their impact on yield. We employed 16S rRNA and fungal ITS region amplicon sequencing to investigate the assembly mechanisms of abundant and rare endophytic subcommunities, network correlations, core subcommunity structures, and key species that enhance crop yield. The results indicated that organic manure and phosphorus fertilizers significantly increased the rhizosphere soil nitrogen content, phosphorus content, and phosphorus availability (labile P, moderately labile P, and non-labile P). These fertilizers also significantly affected the composition (based on Bray-Curtis distance) and community assembly processes (βNTI) of endophytic microbial subcommunities. The assembly of both bacterial and fungal subcommunities was primarily governed by dispersal limitation, with community structures being significantly regulated by the content of rhizosphere soil available nitrogen (AN) and moderately labile P (MLP). Rare bacterial and fungal subcommunities complemented the ecological niches of abundant subcommunities in the co-occurrence network, supporting community functions and enhancing network stability. Nitrogen-adapting abundant and rare bacterial subcommunities provided a stronger predictive correlation for tomato yield than phosphorus-adapting fungal subcommunities. Additionally, three core genera of rare endophytic bacteria such as Arthrobacter, Microbacterium, and Sphingobium were identified as potentially involved in improving crop yield improvement. These findings revealed the distinct assembly mechanisms of endophytic microbial subcommunities affected by fertilization, enhancing our understanding of better management practices and controlling endophytes to improve crop yield in intensive agricultural ecosystems.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1487323/fullendophytecommunity assemblyabundant microbial taxarare microbial taxasolar greenhouse
spellingShingle Xiaoxia Li
Xiaoxia Li
Xiaoxia Li
Muhammad Awais
Muhammad Awais
Muhammad Awais
Shuang Wang
Shuang Wang
Shuang Wang
Shuang Wang
Zhu Zhang
Zhu Zhang
Zhu Zhang
Shuning Zhao
Shuning Zhao
Shuning Zhao
Yufeng Liu
Yufeng Liu
Yufeng Liu
Zhouping Sun
Zhouping Sun
Zhouping Sun
Hongdan Fu
Hongdan Fu
Hongdan Fu
Tianlai Li
Tianlai Li
Tianlai Li
The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilization
Frontiers in Microbiology
endophyte
community assembly
abundant microbial taxa
rare microbial taxa
solar greenhouse
title The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilization
title_full The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilization
title_fullStr The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilization
title_full_unstemmed The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilization
title_short The process of nitrogen-adaptation root endophytic bacterial rather than phosphorus-adaptation fungal subcommunities construction unveiled the tomato yield improvement under long-term fertilization
title_sort process of nitrogen adaptation root endophytic bacterial rather than phosphorus adaptation fungal subcommunities construction unveiled the tomato yield improvement under long term fertilization
topic endophyte
community assembly
abundant microbial taxa
rare microbial taxa
solar greenhouse
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1487323/full
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