Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in Populus

Abstract Plant growth behavior is a function of genetic network architecture. The importance of root microbiome variation driving plant functional traits is increasingly recognized, but the genetic mechanisms governing this variation are less studied. Here, we collect roots and rhizosphere soils fro...

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Main Authors: Jiadong Wu, Sijia Liu, Haoyu Zhang, Sisi Chen, Jingna Si, Lin Liu, Yue Wang, Shuxian Tan, Yuxin Du, Zhelun Jin, Jianbo Xie, Deqiang Zhang
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56226-w
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author Jiadong Wu
Sijia Liu
Haoyu Zhang
Sisi Chen
Jingna Si
Lin Liu
Yue Wang
Shuxian Tan
Yuxin Du
Zhelun Jin
Jianbo Xie
Deqiang Zhang
author_facet Jiadong Wu
Sijia Liu
Haoyu Zhang
Sisi Chen
Jingna Si
Lin Liu
Yue Wang
Shuxian Tan
Yuxin Du
Zhelun Jin
Jianbo Xie
Deqiang Zhang
author_sort Jiadong Wu
collection DOAJ
description Abstract Plant growth behavior is a function of genetic network architecture. The importance of root microbiome variation driving plant functional traits is increasingly recognized, but the genetic mechanisms governing this variation are less studied. Here, we collect roots and rhizosphere soils from nine Populus species belonging to four sections (Leuce, Aigeiros, Tacamahaca, and Turanga), generate metabolite and transcription data for roots and microbiota data for rhizospheres, and conduct comprehensive multi-omics analyses. We demonstrate that the roots of vigorous Leuce poplar enrich more Pseudomonas, compared with the poorly performing poplar. Moreover, we confirm that Pseudomonas is strongly associated with tricin and apigenin biosynthesis and identify that gene GLABRA3 (GL3) is critical for tricin secretion. The elevated tricin secretion via constitutive transcription of PopGL3 and Chalcone synthase (PopCHS4) can drive Pseudomonas colonization in the rhizosphere and further enhance poplar growth, nitrogen acquisition, and secondary root development in nitrogen-poor soil. This study reveals that plant-metabolite-microbe regulation patterns contribute to the poplar fitness and thoroughly decodes the key regulatory mechanisms of tricin, and provides insights into the interactions of the plant’s key metabolites with its transcriptome and rhizosphere microbes.
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institution Kabale University
issn 2041-1723
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publishDate 2025-02-01
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spelling doaj-art-e5a80c6cd5f54f068c279c196e28fdc62025-02-09T12:45:44ZengNature PortfolioNature Communications2041-17232025-02-0116111510.1038/s41467-025-56226-wFlavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in PopulusJiadong Wu0Sijia Liu1Haoyu Zhang2Sisi Chen3Jingna Si4Lin Liu5Yue Wang6Shuxian Tan7Yuxin Du8Zhelun Jin9Jianbo Xie10Deqiang Zhang11State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry UniversityAbstract Plant growth behavior is a function of genetic network architecture. The importance of root microbiome variation driving plant functional traits is increasingly recognized, but the genetic mechanisms governing this variation are less studied. Here, we collect roots and rhizosphere soils from nine Populus species belonging to four sections (Leuce, Aigeiros, Tacamahaca, and Turanga), generate metabolite and transcription data for roots and microbiota data for rhizospheres, and conduct comprehensive multi-omics analyses. We demonstrate that the roots of vigorous Leuce poplar enrich more Pseudomonas, compared with the poorly performing poplar. Moreover, we confirm that Pseudomonas is strongly associated with tricin and apigenin biosynthesis and identify that gene GLABRA3 (GL3) is critical for tricin secretion. The elevated tricin secretion via constitutive transcription of PopGL3 and Chalcone synthase (PopCHS4) can drive Pseudomonas colonization in the rhizosphere and further enhance poplar growth, nitrogen acquisition, and secondary root development in nitrogen-poor soil. This study reveals that plant-metabolite-microbe regulation patterns contribute to the poplar fitness and thoroughly decodes the key regulatory mechanisms of tricin, and provides insights into the interactions of the plant’s key metabolites with its transcriptome and rhizosphere microbes.https://doi.org/10.1038/s41467-025-56226-w
spellingShingle Jiadong Wu
Sijia Liu
Haoyu Zhang
Sisi Chen
Jingna Si
Lin Liu
Yue Wang
Shuxian Tan
Yuxin Du
Zhelun Jin
Jianbo Xie
Deqiang Zhang
Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in Populus
Nature Communications
title Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in Populus
title_full Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in Populus
title_fullStr Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in Populus
title_full_unstemmed Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in Populus
title_short Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and secondary root growth in Populus
title_sort flavones enrich rhizosphere pseudomonas to enhance nitrogen utilization and secondary root growth in populus
url https://doi.org/10.1038/s41467-025-56226-w
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