Rhizosphere & Microbiome

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    A simplified SynCom based on core-helper strain interactions enhances symbiotic nitrogen fixation in soybean
    Yanjun Li, Ruirui Li, Ran Liu, Junhao Shi, Xiaofan Qiu, Jianfeng Lei, Xu Zhao, Cunhu Wang, Minghai Ge, Huan Xu, Pengyao Miao, Zhongwei Li, Keke Yi, Hong Liao, Yongjia Zhong
    J Integr Plant Biol 2025, 67 (6): 1582-1598.  
    DOI: 10.1111/jipb.13881
    Abstract (Browse 807)  |   Save
    Synthetic microbial communities (SynComs) are a promising tool for making full use of the beneficial functions imparted by whole bacterial consortia. However, the complexity of reconstructed SynComs often limits their application in sustainable agriculture. Furthermore, inter-strain interactions are often neglected during SynCom construction. Here, we propose a strategy for constructing a simplified and functional SynCom (sfSynCom) by using elite helper strains that significantly improve the beneficial functions of the core symbiotic strain, here Bradyrhizobium elkanii BXYD3, to sustain the growth of soybean (Glycine max). We first identified helper strains that significantly promote nodulation and nitrogen fixation in soybean mediated by BXYD3. Two of these helper strains assigned to the Pantoea taxon produce acyl homoserine lactones, which significantly enhanced the colonization and infection of soybean by BXYD3. Finally, we constructed a sfSynCom from these core and helper strains. This sfSynCom based on the core-helper strategy was more effective at promoting nodulation than inoculation with BXYD3 alone and achieved effects comparable to those of a complex elite SynCom previously constructed on the basis of potential beneficial functions between microbes and plants alone. Our results suggest that considering interactions between strains as well as those between strains and the host plant might allow construction of sfSynComs.
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    In the simplified and functional synthetic community (sfSynCom), a helper strain induces biofilm formation in the core symbiotic strain, Bradyrhizobium, via production of acyl homoserine lactones. This biofilm formation facilitates colonization of the soybean plant roots by Bradyrhizobium and thus promotes nodulation.
      
    Plant–microbiome interactions and their impacts on plant adaptation to climate change
    Qing Zeng, Hang-Wei Hu, An-Hui Ge, Chao Xiong, Chang-Chun Zhai, Gui-Lan Duan, Li-Li Han, Si-Yun Huang, Li-Mei Zhang
    J Integr Plant Biol 2025, 67 (3): 826-844.  
    doi: 10.1111/jipb.13863
    Abstract (Browse 565)  |   Save
    Plants have co-evolved with a wide range of microbial communities over hundreds of millions of years, this has drastically influenced their adaptation to biotic and abiotic stress. The rapid development of multi-omics approaches has greatly improved our understanding of the diversity, composition, and functions of plant microbiomes, but how global climate change affects the assembly of plant microbiomes and their roles in regulating host plant adaptation to changing environmental conditions is not fully known. In this review, we summarize recent advancements in the community assembly of plant microbiomes, and their responses to climate change factors such as elevated CO2 levels, warming, and drought. We further delineate the research trends and hotspots in plant–microbiome interactions in the context of climate change, and summarize the key mechanisms by which plant microbiomes influence plant adaptation to the changing climate. We propose that future research is urgently needed to unravel the impact of key plant genes and signal molecules modulated by climate change on microbial communities, to elucidate the evolutionary response of plant–microbe interactions at the community level, and to engineer synthetic microbial communities to mitigate the effects of climate change on plant fitness.
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    This review summarizes how climate change factors like elevated CO2, warming, and drought affect plant microbiome assembly and function, thereby influencing plant adaptation. It highlights recent advancements, key mechanisms, and future research needs.
      
    Halotolerant Bacillus sp. strain RA coordinates myo-inositol metabolism to confer salt tolerance to tomato
    Fenghui Wu, Zengting Chen, Xiaotong Xu, Xin Xue, Yanling Zhang, Na Sui
    J Integr Plant Biol 2024, 66 (9): 1871-1885.  
    DOI: 10.1111/jipb.13733
    Abstract (Browse 485)  |   Save
    Soil salinity is a worldwide problem threatening crop yields. Some plant growth-promoting rhizobacteria (PGPR) could survive in high salt environment and assist plant adaptation to stress. Nevertheless, the genomic and metabolic features, as well as the regulatory mechanisms promoting salt tolerance in plants by these bacteria remain largely unknown. In the current work, a novel halotolerant PGPR strain, namely, Bacillus sp. strain RA can enhance tomato tolerance to salt stress. Comparative genomic analysis of strain RA with its closely related species indicated a high level of evolutionary plasticity exhibited by strain-specific genes and evolutionary constraints driven by purifying selection, which facilitated its genomic adaptation to salt-affected soils. The transcriptome further showed that strain RA could tolerate salt stress by balancing energy metabolism via the reprogramming of biosynthetic pathways. Plants exude a plethora of metabolites that can strongly influence plant fitness. The accumulation of myo-inositol in leaves under salt stress was observed, leading to the promotion of plant growth triggered by Bacillus sp. strain RA. Importantly, myo-inositol serves as a selective force in the assembly of the phyllosphere microbiome and the recruitment of plant-beneficial species. It promotes destabilizing properties in phyllosphere bacterial co-occurrence networks, but not in fungal networks. Furthermore, interdomain interactions between bacteria and fungi were strengthened by myo-inositol in response to salt stress. This work highlights the genetic adaptation of RA to salt-affected soils and its ability to impact phyllosphere microorganisms through the adjustment of myo-inositol metabolites, thereby imparting enduring resistance against salt stress in tomato.
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    The halotolerant Bacillus sp. strain RA tolerates saline environments by reprogramming its biosynthetic pathways and mitigate salt stress in tomato by affecting phyllosphere microorganisms through myo-inositol.
      
    Essential roles of nodule cysteine-rich peptides in maintaining the viability of terminally differentiated bacteroids in legume-rhizobia symbiosis
    Jian Yang, Fengzhan Gao, Huairong Pan
    J Integr Plant Biol 2025, 67 (4): 1077-1085.  
    DOI: 10.1111/jipb.13891
    Abstract (Browse 452)  |   Save
    Investigations into the nitrogen-fixing symbiosis between legumes and rhizobia can yield innovative strategies for sustainable agriculture. Legume species of the Inverted Repeat-Lacking Clade (IRLC) and the Dalbergioids, can utilize nodule cysteine-rich (NCR) peptides, a diverse family of peptides characterized by four or six highly conserved cysteine residues, to communicate with their microbial symbionts. These peptides, many of which exhibit antimicrobial properties, induce profound differentiation of bacteroids (semi-autonomous forms of bacteria) within nodule cells. This terminal differentiation endows the bacteroids with the ability to fix nitrogen, at the expense of their reproductive capacity. Notably, a significant number of NCR peptides is expressed in the nodule fixation zone, where the bacteroids have already reached terminal differentiation. Recent discoveries, through forward genetics approaches, have revealed that the functions of NCR peptides extend beyond antimicrobial effects and the promotion of differentiation. They also play a critical role in sustaining the viability of terminally differentiated bacteroids within nodule cells. These findings underscore the multifaceted functions of NCR peptides and highlight the importance of these peptides in mediating communications between host cells and the terminally differentiated bacteroids.
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    Nodule cysteine-rich peptides have antimicrobial effects and promote differentiation. They also play a critical role in sustaining the viability of terminally differentiated bacteroids within nodule cells.
      
    MicroRNA gatekeepers: Orchestrating rhizospheric dynamics
    Muhammad Fahad, Leeza Tariq, Wanchang Li, Liang Wu
    J Integr Plant Biol 2025, 67 (3): 845-876.  
    doi: 10.1111/jipb.13860
    Abstract (Browse 444)  |   Save
    The rhizosphere plays a crucial role in plant growth and resilience to biotic and abiotic stresses, highlighting the complex communication between plants and their dynamic rhizosphere environment. Plants produce a wide range of signaling molecules that facilitate communication with various rhizosphere factors, yet our understanding of these mechanisms remains elusive. In addition to protein-coding genes, increasing evidence underscores the critical role of microRNAs (miRNAs), a class of non-coding single-stranded RNA molecules, in regulating plant growth, development, and responses to rhizosphere stresses under diverse biotic and abiotic factors. In this review, we explore the crosstalk between miRNAs and their target mRNAs, which influence the development of key plant structures shaped by the belowground environment. Moving forward, more focused studies are needed to clarify the functions and expression patterns of miRNAs, to uncover the common regulatory mechanisms that mediate plant tolerance to rhizosphere dynamics. Beyond that, we propose that using artificial miRNAs and manipulating the expression of miRNAs and their targets through overexpression or knockout/knockdown approaches could effectively investigate their roles in plant responses to rhizosphere stresses, offering significant potential for advancing crop engineering.
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    MicroRNAs play a crucial role in plant communication within the rhizosphere, shaping growth, development, and resilience to biotic and abiotic stresses.
      
    Functional genomics dissection of the nodulation autoregulation pathway (AON) in soybean (Glycine max)
    Peter M. Gresshoff, Chao Su, Huanan Su, April Hastwell, Yanyan Cha, Mengbai Zhang, Estelle B. Grundy, Xitong Chu, Brett J. Ferguson, Xia Li
    J Integr Plant Biol 2025, 67 (3): 762-772.  
    doi: 10.1111/jipb.13898
    Abstract (Browse 418)  |   Save
    The combination of mutation-based genetics and functional genomics has allowed a detailed dissection of the nodulation-induction and autoregulation of nodulation (AON) pathways of soybean. Applicable to all legumes, nodulation is induced by Rhizobium/Bradyrhizobium-produced lipopolysaccharides (Nod factors), perceived by Nod factor receptors (NFR1/NFR5 dimers), leading to cortical and pericycle cell divisions. These induce the production of Clavata3-like (CLE) peptides, which travel in the xylem to the shoot, where they are perceived by a receptor complex including a leucine-rich repeat (LRR) receptor kinase, encoded by GmNARK, LjHAR1, MtSUNN and closely related receptors in other legumes like Phaseolus vulgaris (common bean), Pisum sativum (pea), and Glycine soja. The activated receptor complex negatively regulates by phosphorylation of the constitutive synthesis of miR2111 in the shoot. This is normally is translocated via the phloem to the entire plant body, initiating suppression of a root-expressed Kelch repeat-containing F-box protein "Too Much Love (TML)," which in turn suppresses the nodule initiation cascade. Nodulation is therefore permitted during a developmental window between the induction and progress of the nodulation/cell division/infection cascade during the first few days after inoculation and the functional "readiness" of the AON cascade, delayed by the root–shoot–root loop. Loss-of-function mutations in GmNARK and LjTML result in excessive nodulation (supernodulation/hypernodulation/supernummary nodulation) as well as localized tolerance to externally applied nitrate. Recent analyses have indicated an interaction of the AON with lateral root formation as well as with the autoregulation of mycorrhization (AOM). Further details of the parallel functions of key points in this regulatory loop remain to be elucidated.
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    This review explores the history of the discovery of autoregulation of nodulation (AON) in soybean, highlighting recent advances in AON signaling pathway regulation and its interaction with processes like lateral root development, and providing new insights into understanding and further exploring the AON pathway.
      
    NODULATION TRIO in Medicago truncatula:Unveiling the redundant roles of MtLYK2, MtLYK3,and MtLYK2bis
    Yaohua Li, Yanwen Zhao, Ziang Yan, Ru Dong, Haixiang Yu, Hui Zhu, Yangrong Cao
    J Integr Plant Biol 2024, 66 (8): 1553-1556.  
    doi: 10.1111/jipb.13718
    Abstract (Browse 355)  |   Save
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    Three Medicago truncatula LysM domain receptor kinases have redundant functions in nodulation, with multiple specificities mediating both entry and signaling responses and with distinct contributions to nodulation likely resulting from differing transcription patterns.
      
    Sodium butyrate regulates the sulfur respiration of rhizosphere soil to produce hydrogen sulfide modulating histone acetylation dynamics to enhance drought tolerance in rice
    Xu Chen, Jialin Ge, Xingjing Cai, Lei Jin, Huanhe Wei, Xinru Zhao, Haidong Yang, Wen Jiang, Zhukuan Cheng, Chao Xue, Xi Cao, Zhiying Wang, Qigen Dai, Yong Zhou, Zhiyun Gong
    J Integr Plant Biol 2025, 67 (11): 2879-2896.  
    DOI: 10.1111/jipb.70027
    Abstract (Browse 311)  |   Save
    Hydrogen sulfide (H2S), a well-established gaseous signaling molecule, can effectively enhance plant tolerance to various environmental stresses. However, there is still a lack of suitable methods to release H2S in agricultural production, and the mechanism by which H2S improves stress resistance remains poorly understood. Here, we show the novel role of sodium butyrate (NaB) in producing H2S consistently in rice rhizosphere soil and the epigenetic mechanism of H2S to enhance rice drought tolerance. We found that NaB increased sulfate-reducing bacteria (SRB) abundance in the rhizosphere soil, resulting in higher expression of sulfite reductase (SiR), and consequently increased H2S production. Mechanistic investigation showed that H2S enhanced the level of H4K5ac in promoter regions of drought-tolerant genes, facilitating their expression by repressing the histone deacetylase (HDAC) gene OsHDA710. Loss-of-function mutants of OsHDA710 exhibited enhanced drought tolerance compared to wild-type (WT) plants, while OsHDA710 overexpression plants showed drought hypersensitivity. Moreover, we demonstrated that OsHDA710 could bind directly to promoters of drought-tolerance genes by recognizing the TGACC motif. Our findings illustrate an efficient way to produce H2S and a novel mechanism for H2S in improving the drought resistance of plants.
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    Sodium butyrate increases the numbers of sulfate-reducing bacteria in the rice rhizosphere, stimulating hydrogen sulfide (H2S) biosynthesis. H2S represses the histone deacetylase OsHDA710, thereby elevating histone acetylation at drought-tolerance gene promoters and activating transcription in an epigenetic pathway for drought resistance.
      
    CPOP1 is a key enzyme required for nodule microenvironment control and successful symbiotic nitrogen fixation in Lotus japonicus
    Yu-Fang Tian, Yu Luo, Qi-Min Li, Zhi-Qin Zhang, Ya-Long Guo, Wei-Cai Yang
    J Integr Plant Biol 2025, 67 (12): 3167-3181.  
    doi: 10.1111/jipb.70037
    Abstract (Browse 236)  |   Save
    Symbiotic nitrogen fixation in legumes requires the exquisite regulation of the environment within the infected region of the nodule. The microaerobic environment critical for nitrogenase activity is maintained through the physical oxygen diffusion barrier of the cortex and locally the oxygen-binding protein leghemoglobin (Lb). Leghemoglobin binds and releases oxygen with heme moiety to maintain oxygen gradients inside the infected cell (IC) during nitrogen fixation. Heme binds to diverse proteins and plays critical roles in different redox reactions. However, the role and regulation of host-controlled heme production during symbiotic nitrogen fixation are not clear. Here, we identified coproporphyrinogen III oxidase plastid related 1 (CPOP1) as a key regulator of symbiotic heme biosynthesis in Lotus japonicus. CPOP1 is specifically highly expressed in nitrogen-fixing nodules, and knocking out CPOP1 alone causes leaf etiolation and dwarfism which could be recovered by the exogenous application of nitrogen source, indicating nitrogen fixation defect. The IC-specific expression of CPOP1 was directed by the −881 to −740 bp promoter region. The cpop1 mutant shows significantly increased nodule oxygen level and decreased nitrogen fixation activity compared to the wild-type. Intriguingly, bacteria proliferation is inhibited due to the down-regulation of cell division-related gene expression upon CPOP1 knockout. Our data showed that CPOP1 is essential for the microaerobic environment control of ICs and the activation of rhizobial nitrogenase required for symbiotic nitrogen fixation, through host-regulated nodule heme synthesis.
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    The enzyme coproporphyrinogen III oxidase plastid related 1 (CPOP1) creates a low-oxygen nodule environment for nitrogen fixation within nodules of Lotus japonicus. CPOP1 makes heme, which helps control oxygen, and acts in infected cells; its knockout raises oxygen levels, suppresses nitrogen-fixing enzyme activity, and halts nitrogen fixation.
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