Journal Article

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

Zhang, Haoyu, Wang, Yue, Xie, Jianbo, Wu, Jiadong, Tan, Shuxian, Zhang, Deqiang, Chen, Sisi, Liu, Sijia, Jin, Zhelun, Si, Jingna, Du, Yuxin, Liu, Lin

2025

Overview

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. Multi-omics analysis reveals that differential plant performance among Populus species is associated with Pseudomonas in the rhizosphere. Further mechanistic investigation identifies GL3 as a regulator of flavone biosynthesis contributing to Pseudomonas recruitment.

• Publisher: Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio
• Subject: 38 / 38/35 / 38/39 / 38/44 / 38/47 / 38/91 / 42 / 45 / 631/326/2565 / 631/337/2019 / 631/449/1659 / Apigenin - metabolism / Biosynthesis / Chalcone synthase / Data analysis / Flavones / Gene Expression Regulation, Plant / Genetic diversity / Humanities and Social Sciences / Metabolites / Microbiomes / Microbiota / Microorganisms / multidisciplinary / Nitrogen / Nitrogen - metabolism / Plant growth / Plant Proteins - genetics / Plant Proteins - metabolism / Plant Roots - growth & development / Plant Roots - metabolism / Plant Roots - microbiology / Poplar / Populus - genetics / Populus - growth & development / Populus - metabolism / Populus - microbiology / Pseudomonas / Pseudomonas - genetics / Pseudomonas - metabolism / Regulatory mechanisms (biology) / Rhizosphere / Rhizosphere microorganisms / Root development / Roots / Science / Science (multidisciplinary) / Secretion / Soil Microbiology / Transcriptomes