Genotype-specific rhizospheric microbiome and iron mobilization strategies in wheat revealed by integrated metagenomic and imaging analyses

IF 3.9 3区 生物学 Q1 PLANT SCIENCES
Rhizosphere Pub Date : 2026-06-01 Epub Date: 2026-05-07 DOI:10.1016/j.rhisph.2026.101349
Pragati Srivastava , Jasdeep Chatrath Padaria , Yogesh K. Ahlawat
{"title":"Genotype-specific rhizospheric microbiome and iron mobilization strategies in wheat revealed by integrated metagenomic and imaging analyses","authors":"Pragati Srivastava ,&nbsp;Jasdeep Chatrath Padaria ,&nbsp;Yogesh K. Ahlawat","doi":"10.1016/j.rhisph.2026.101349","DOIUrl":null,"url":null,"abstract":"<div><div>The rhizosphere represents a highly dynamic and biologically active zone surrounding plant roots, where intricate interactions occur between the plant and diverse microbial assemblages. This microenvironment is shaped by root exudates, microbial metabolites and environmental factors that collectively influence nutrient cycling and plant health. Among the essential micronutrients, iron (Fe) plays a pivotal role in plant metabolism, being involved in key processes such as photosynthesis, respiration and chlorophyll biosynthesis thus critically influencing plant nutrition and yield. To explore microbial-mediated Fe acquisition, we performed shotgun metagenomic sequencing of rhizospheric soils from two contrasting wheat genotypes—HD2967 (low Fe accumulator) and DBW303 (high Fe accumulator) Metagenome-assembled genomes (MAGs) were recovered using CONCOCT and MaxBin, yielding four major bins for HD2967 (e.g., concoct.5, concoct.6, maxbin.001 and maxbin.002) and five bins for DBW303 (e.g., concoct.11, concoct.14, concoct.15, maxbin.001 and maxbin.002). Taxonomic classification showed distinct patterns, HD2967 bins were dominated by <em>Myxococcota</em> (concoct.6, maxbin.001), <em>Alphaproteobacteria</em> (concoct.5) and <em>Deltaproteobacteria</em> (maxbin.002). DBW303 bins were enriched in <em>Verrucomicrobiota</em> (concoct.11), <em>Acidobacteriota</em> (concoct.14) and <em>Gammaproteobacteria</em> (maxbin.001, maxbin.002). Functional annotation via FeGenie revealed a richer siderophore transport and regulation machinery in HD2967. HD2967 showed multiple hits for ExbB/ExbD/TonB siderophore transport systems (concoct.6, maxbin.001, concoct.5), PvdS and PchR regulators and iron oxidation (FoxE) genes. DBW303 also displayed iron acquisition genes but in fewer bins and with lower completeness; concoct.11 and maxbin.002 had high siderophore receptor counts but lower gene regulation density. EDX elemental analysis confirmed higher Fe accumulation in HD2967 plant cell, correlating with microbial genomic potential for Fe uptake.</div><div>Transmission Electron Microscopy (TEM) revealed distinct chloroplast ultrastructural differences between wheat genotypes under low iron (Fe) stress. The high Fe accumulator DBW 303 maintained intact thylakoid organization and basal granules, while HD2967 exhibited disorganized thylakoids and impaired chloroplast integrity. These cellular differences corresponded with Energy Dispersive X-ray Spectroscopy (EDX) data, which showed higher Fe and micronutrient deposition within plant cell of DBW 303, highlighting genotype-dependent nutrient uptake and its impact on photosynthetic structure., possibly representing siderophore-bound Fe deposits or ferritin-like storage forms. In conclusion, the integration of taxonomic, functional and elemental data illustrates a strong genotype-driven divergence in rhizospheric microbial communities and Fe mobilization pathways. These insights pave the way for bioinoculant design and targeted microbiome engineering for micronutrient biofortification in crops.</div></div>","PeriodicalId":48589,"journal":{"name":"Rhizosphere","volume":"38 ","pages":"Article 101349"},"PeriodicalIF":3.9000,"publicationDate":"2026-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Rhizosphere","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2452219826000947","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2026/5/7 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

The rhizosphere represents a highly dynamic and biologically active zone surrounding plant roots, where intricate interactions occur between the plant and diverse microbial assemblages. This microenvironment is shaped by root exudates, microbial metabolites and environmental factors that collectively influence nutrient cycling and plant health. Among the essential micronutrients, iron (Fe) plays a pivotal role in plant metabolism, being involved in key processes such as photosynthesis, respiration and chlorophyll biosynthesis thus critically influencing plant nutrition and yield. To explore microbial-mediated Fe acquisition, we performed shotgun metagenomic sequencing of rhizospheric soils from two contrasting wheat genotypes—HD2967 (low Fe accumulator) and DBW303 (high Fe accumulator) Metagenome-assembled genomes (MAGs) were recovered using CONCOCT and MaxBin, yielding four major bins for HD2967 (e.g., concoct.5, concoct.6, maxbin.001 and maxbin.002) and five bins for DBW303 (e.g., concoct.11, concoct.14, concoct.15, maxbin.001 and maxbin.002). Taxonomic classification showed distinct patterns, HD2967 bins were dominated by Myxococcota (concoct.6, maxbin.001), Alphaproteobacteria (concoct.5) and Deltaproteobacteria (maxbin.002). DBW303 bins were enriched in Verrucomicrobiota (concoct.11), Acidobacteriota (concoct.14) and Gammaproteobacteria (maxbin.001, maxbin.002). Functional annotation via FeGenie revealed a richer siderophore transport and regulation machinery in HD2967. HD2967 showed multiple hits for ExbB/ExbD/TonB siderophore transport systems (concoct.6, maxbin.001, concoct.5), PvdS and PchR regulators and iron oxidation (FoxE) genes. DBW303 also displayed iron acquisition genes but in fewer bins and with lower completeness; concoct.11 and maxbin.002 had high siderophore receptor counts but lower gene regulation density. EDX elemental analysis confirmed higher Fe accumulation in HD2967 plant cell, correlating with microbial genomic potential for Fe uptake.
Transmission Electron Microscopy (TEM) revealed distinct chloroplast ultrastructural differences between wheat genotypes under low iron (Fe) stress. The high Fe accumulator DBW 303 maintained intact thylakoid organization and basal granules, while HD2967 exhibited disorganized thylakoids and impaired chloroplast integrity. These cellular differences corresponded with Energy Dispersive X-ray Spectroscopy (EDX) data, which showed higher Fe and micronutrient deposition within plant cell of DBW 303, highlighting genotype-dependent nutrient uptake and its impact on photosynthetic structure., possibly representing siderophore-bound Fe deposits or ferritin-like storage forms. In conclusion, the integration of taxonomic, functional and elemental data illustrates a strong genotype-driven divergence in rhizospheric microbial communities and Fe mobilization pathways. These insights pave the way for bioinoculant design and targeted microbiome engineering for micronutrient biofortification in crops.
综合宏基因组和成像分析揭示了小麦根际微生物组和铁动员策略的基因型特异性
根际是植物根周围高度动态和生物活性的区域,在这里植物和各种微生物组合之间发生复杂的相互作用。这个微环境是由根系分泌物、微生物代谢产物和环境因素共同影响养分循环和植物健康形成的。在必需微量元素中,铁(Fe)在植物代谢中起着举足轻重的作用,参与光合作用、呼吸作用和叶绿素合成等关键过程,对植物的营养和产量具有重要影响。为了探索微生物介导的铁获取,我们对两种不同的小麦基因型——HD2967(低铁积累者)和DBW303(高铁积累者)的根际土壤进行了散枪宏基因组测序,使用CONCOCT和MaxBin回收了宏基因组组装的基因组(MAGs),得到了HD2967(例如CONCOCT)的四个主要bin。5,编造。6, maxbin。001和maxbin。002)和5个箱子存放DBW303(例如,concost。11日,编造。14日,编造。15日,maxbin。001和maxbin.002)。分类模式明显,HD2967箱以粘球菌为主;6, maxbin。α变形菌(炮制.5)和δ变形菌(maxbin.002)。DBW303箱中Verrucomicrobiota (concost)富集;11),酸杆菌门(调和菌门)和γ变形菌门(maxbin.)。001年,maxbin.002)。FeGenie功能注释显示HD2967具有丰富的铁载体转运和调控机制。HD2967显示了ExbB/ExbD/TonB铁载体传输系统的多重击中(conconst)。6, maxbin。001年,编造。5), PvdS和PchR调节因子和铁氧化(FoxE)基因。DBW303也表现出铁获取基因,但数量较少,完整性较低;编造。11和maxbin。002的铁载体受体数量较高,但基因调控密度较低。EDX元素分析证实HD2967在植物细胞中有较高的铁积累,这与微生物基因组对铁吸收的潜力有关。透射电镜(TEM)显示,低铁胁迫下不同小麦基因型叶绿体超微结构存在明显差异。高铁蓄能器DBW 303保持了完整的类囊体组织和基本颗粒,而HD2967则表现出无组织的类囊体和受损的叶绿体完整性。这些细胞差异与能量色散x射线光谱(EDX)数据相一致,表明DBW 303植物细胞内铁和微量营养素沉积量较高,突出了基因型依赖性营养吸收及其对光合结构的影响。,可能代表铁载体结合的铁矿床或类似铁蛋白的储存形式。综上所述,分类、功能和元素数据的整合表明,根际微生物群落和铁动员途径存在强烈的基因型驱动差异。这些见解为作物微量营养素生物强化的生物接种剂设计和靶向微生物组工程铺平了道路。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Rhizosphere
Rhizosphere Agricultural and Biological Sciences-Agronomy and Crop Science
CiteScore
5.70
自引率
8.10%
发文量
155
审稿时长
29 days
期刊介绍: Rhizosphere aims to advance the frontier of our understanding of plant-soil interactions. Rhizosphere is a multidisciplinary journal that publishes research on the interactions between plant roots, soil organisms, nutrients, and water. Except carbon fixation by photosynthesis, plants obtain all other elements primarily from soil through roots. We are beginning to understand how communications at the rhizosphere, with soil organisms and other plant species, affect root exudates and nutrient uptake. This rapidly evolving subject utilizes molecular biology and genomic tools, food web or community structure manipulations, high performance liquid chromatography, isotopic analysis, diverse spectroscopic analytics, tomography and other microscopy, complex statistical and modeling tools.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信
小红书