Full Text:   <486>

Summary:  <83>

CLC number: 

On-line Access: 2025-10-21

Received: 2025-03-02

Revision Accepted: 2025-08-03

Crosschecked: 2025-10-21

Cited: 0

Clicked: 1387

Citations:  Bibtex RefMan EndNote GB/T7714

 ORCID:

Mengcen WANG

https://ORCID:orcid.org/0000-0001-7169-6779

Xiaoyu LIU

https://ORCID:orcid.org/0000-0002-6054-8858

-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2025 Vol.26 No.10 P.923-934

http://doi.org/10.1631/jzus.B2500099


Harnessing chemical communication in plant–microbiome and intra-microbiome interactions


Author(s):  Hongfu LI, Yaxin HU, Siqi CHEN, Yusufjon GAFFOROV, Mengcen WANG, Xiaoyu LIU

Affiliation(s):  College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China; more

Corresponding email(s):   wmctz@zju.edu.cn, Xiaoyu.liu@research.uwa.edu.au

Key Words:  Plant-microbiome interaction, Intra-microbiome interaction, Chemical communication, Click chemistry, Genome editing, Artificial intelligence (AI)


Share this article to: More |Next Article >>>

Hongfu LI, Yaxin HU, Siqi CHEN, Yusufjon GAFFOROV, Mengcen WANG, Xiaoyu LIU. Harnessing chemical communication in plant–microbiome and intra-microbiome interactions[J]. Journal of Zhejiang University Science B, 2025, 26(10): 923-934.

@article{title="Harnessing chemical communication in plant–microbiome and intra-microbiome interactions",
author="Hongfu LI, Yaxin HU, Siqi CHEN, Yusufjon GAFFOROV, Mengcen WANG, Xiaoyu LIU",
journal="Journal of Zhejiang University Science B",
volume="26",
number="10",
pages="923-934",
year="2025",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2500099"
}

%0 Journal Article
%T Harnessing chemical communication in plant–microbiome and intra-microbiome interactions
%A Hongfu LI
%A Yaxin HU
%A Siqi CHEN
%A Yusufjon GAFFOROV
%A Mengcen WANG
%A Xiaoyu LIU
%J Journal of Zhejiang University SCIENCE B
%V 26
%N 10
%P 923-934
%@ 1673-1581
%D 2025
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2500099

TY - JOUR
T1 - Harnessing chemical communication in plant–microbiome and intra-microbiome interactions
A1 - Hongfu LI
A1 - Yaxin HU
A1 - Siqi CHEN
A1 - Yusufjon GAFFOROV
A1 - Mengcen WANG
A1 - Xiaoyu LIU
J0 - Journal of Zhejiang University Science B
VL - 26
IS - 10
SP - 923
EP - 934
%@ 1673-1581
Y1 - 2025
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2500099


Abstract: 
chemical communication in plant-microbiome and intra-microbiome interactions weaves a complex network, critically shaping ecosystem stability and agricultural productivity. This non-contact interaction is driven by small-molecule signals that orchestrate crosstalk dynamics and beneficial association. Plants leverage these signals to distinguish between pathogens and beneficial microbes, dynamically modulate immune responses, and secrete exudates to recruit a beneficial microbiome, while microbes in turn influence plant nutrient acquisition and stress resilience. Such bidirectional chemical dialogues underpin nutrient cycling, co-evolution, microbiome assembly, and plant resistance. However, knowledge gaps persist regarding validating the key molecules involved in plant-microbe interactions. Interpreting chemical communication requires multi-omics integration to predict key information, genome editing and click chemistry to verify the function of biomolecules, and artificial intelligence (AI) models to improve resolution and accuracy. This review helps advance the understanding of chemical communication and provides theoretical support for agriculture to cope with food insecurity and climate challenges.

植物-微生物组和微生物组内相互作用中化学通讯的应用

李泓甫1,2,3,胡雅馨1,2,3,陈思齐1,2,3,Yusufjon GAFFOROV4,王蒙岑1,2,3,5,刘晓玉6
1浙江大学农业与生物技术学院,中国杭州市,310058
2水稻生物育种全国重点实验室,农业农村部作物病虫分子生物学重点实验室,浙江大学,中国杭州市,310058
3浙江省作物病虫生物学重点实验室,浙江省作物病虫绿色防控技术工程研究中心,浙江大学农药与环境毒理研究所,中国杭州市,310058
4新乌兹别克斯坦大学中亚发展研究中心,塔什干市,100007,乌兹别克斯坦
5北海道大学农学研究院农业科学前沿全球教育项目,札幌市,060-0808,日本
6澳大利亚植物能量生物学卓越研究中心,西澳大利亚大学,珀斯市,西澳大利亚州6430,澳大利亚
摘要:植物-微生物群以及微生物群内的化学通讯编织出一个复杂的网络,对生态系统稳定性和农业生产力具有重要影响。这种非接触式的相互作用由小分子信号驱动,这些信号协调交互对话的动态并促进有益的互作关系。植物利用这些信号来区分病原体与有益微生物,动态调节免疫反应,并分泌根系外泌物以招募有益微生物群;而微生物则反过来影响植物的养分获取和抗逆能力。这种双向化学对话支撑着养分循环、共同进化、微生物群组装以及植物的抗性。然而,目前在验证参与植物-微生物互作的关键分子方面仍存在知识空白。解析化学通讯需要整合多组学预测关键信息,利用基因组编辑和点击化学来验证生物分子的功能,并借助人工智能(AI)模型来提升解析的分辨率和准确性。本综述旨在推动对化学通讯的理解,并为农业应对粮食安全与气候挑战提供理论支持。

关键词:植物-微生物组相互作用;微生物组内相互作用;化学通讯;点击化学;基因组编辑;人工智能

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]AshrafiR, BruneauxM, SundbergLR, et al., 2017. Application of high resolution melting assay (HRM) to study temperature-dependent intraspecific competition in a pathogenic bacterium. Sci Rep, 7:980.

[2]AtkinsonNJ, LilleyCJ, UrwinPE, 2013. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol, 162(4):2028-2041.

[3]BaiWH, LiC, LiW, et al., 2024. Machine learning assists prediction of genes responsible for plant specialized metabolite biosynthesis by integrating multi-omics data. BMC Genomics, 25:418.

[4]BerrocalA, NavarreteJ, OviedoC, et al., 2012. Quorum sensing activity in Ophiostoma ulmi: effects of fusel oils and branched chain amino acids on yeast-mycelial dimorphism. J Appl Microbiol, 113(1):126-134.

[5]BishnoiP, SarohaB, KumarS, et al., 2025. Click Chemistry: an overview and recent updates in the medicinal attributes of click-derived heterocycles. Mol Divers, in press.

[6]BordensteinSR, TheisKR, 2015. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol, 13(8):e1002226.

[7]BrackmanG, CoenyeT, 2015. Quorum sensing inhibitors as anti-biofilm agents. Curr Pharm Des, 21(1):5-11.

[8]CallawayE, 2024. ‘ChatGPT for CRISPR’ creates new gene-editing tools. Nature, 629(8011):272-272.

[9]CallawayE, 2025. Biggest-ever AI biology model writes DNA on demand. Nature, 638(8052):868-869.

[10]Cembrowska-LechD, KrzemińskaA, MillerT, et al., 2023. An integrated multi-omics and artificial intelligence framework for advance plant phenotyping in horticulture. Biology, 12(10):1298.

[11]ChenDM, LiRN, ShaoQ, et al., 2023. Design and synthesis of novel near-infrared fluorescence probes based on an open conformation of a cytochrome P450 1B1 complex for molecular imaging of colorectal tumors. J Med Chem, 66(23):16032-16050.

[12]ChenMM, KopittkePM, ZhaoFJ, et al., 2024. Applications and opportunities of click chemistry in plant science. Trends Plant Sci, 29(2):167-178.

[13]ChenSS, LuXQ, FangHD, et al., 2024. Early surveillance of rice bakanae disease using deep learning and hyperspectral imaging. aBIOTECH, 5(3):281-297.

[14]ChenY, WangJ, YangN, et al., 2018. Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation. Nat Commun, 9:3429.

[15]ChengR, KeTL, GuiFZ, et al., 2025. drSMALL: database for disease resistance-shaping small molecules derived from the plant microbiome. Crop Health, 3:2.

[16]DullahS, HazarikaDJ, ParveenA, et al., 2021. Fungal interactions induce changes in hyphal morphology and enzyme production. Mycology, 12(4):279-295.

[17]FanXY, MatsumotoH, XuHR, et al., 2024. Aspergillus cvjetkovicii protects against phytopathogens through interspecies chemical signalling in the phyllosphere. Nat Microbiol, 9(11):2862-2876.

[18]GandomiAH, ChenF, AbualigahL, 2023. Big data analytics using artificial intelligence. Electronics, 12(4):957.

[19]GaoCX, 2021. Genome engineering for crop improvement and future agriculture. Cell, 184(6):1621-1635.

[20]GigerGH, ErnstC, RichterI, et al., 2024. Inducing novel endosymbioses by implanting bacteria in fungi. Nature, 635(8038):415-422.

[21]GongAD, WuNN, KongXW, et al., 2019. Inhibitory effect of volatiles emitted from Alcaligenes faecalis N1-4 on Aspergillus flavus and aflatoxins in storage. Front Microbiol, 10:1419.

[22]GuY, TianJJ, ZhangY, et al., 2021. Dissecting signal molecule AI-2 mediated biofilm formation and environmental tolerance in Lactobacillus plantarum. J Biosci Bioeng, 131(2):153-160.

[23]HacquardS, MartinFM, 2024. The chemical language of plant–microbe–microbe associations: an introduction to a virtual issue. New Phytol, 244(3):739-742.

[24]HanifMS, TayyabM, BailloEH, et al., 2024. Plant microbiome technology for sustainable agriculture. Front Microbiol, 15:1500260.

[25]HibbingME, FuquaC, ParsekMR, et al., 2010. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol, 8(1):15-25.

[26]HoganDA, VikÅ, KolterR, 2004. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol, 54(5):1212-1223.

[27]HuTT, FangHD, PanQQ, et al., 2024. Seed microbiome-mediated herbicide resistance evolution in weeds. New Phytol, 242(2):333-343.

[28]HussainM, ZahraN, LangT, et al., 2023. Integrating nanotechnology with plant microbiome for next-generation crop health. Plant Physiol Biochem, 196:703-711.

[29]JinPF, WangY, TanZ, et al., 2020. Antibacterial activity and rice-induced resistance, mediated by C15 surfactin A, in controlling rice disease caused by Xanthomonas oryzae pv. oryzae. Pestic Biochem Physiol, 169:104669.

[30]JonesJDG, StaskawiczBJ, DanglJL, 2024. The plant immune system: from discovery to deployment. Cell, 187(9):2095-2116.

[31]JumperJ, EvansR, PritzelA, et al., 2021. Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873):583-589.

[32]KatoH, NemotoK, ShimizuM, et al., 2022. Recognition of pathogen-derived sphingolipids in Arabidopsis. Science, 376(6595):857-860.

[33]KimothoRN, MainaS, 2024. Unraveling plant–microbe interactions: can integrated omics approaches offer concrete answers? J Exp Bot, 75(5):1289-1313.

[34]KolbHC, FinnMG, SharplessKB, 2001. Click chemistry: diverse chemical function from a few good reactions. Angew Chem Int Ed, 40(11):2004-2021.

[35]KuYS, LiaoYJ, ChiouSP, et al., 2024. From trade-off to synergy: microbial insights into enhancing plant growth and immunity. Plant Biotechnol J, 22(9):2461-2471.

[36]LaschP, BeyerW, BoschA, et al., 2025. A MALDI-ToF mass spectrometry database for identification and classification of highly pathogenic bacteria. Sci Data, 12:187.

[37]LeachJE, TriplettLR, ArguesoCT, et al., 2017. Communication in the phytobiome. Cell, 169(4):587-596.

[38]LiBS, SunC, LiJY, et al., 2024. Targeted genome-modification tools and their advanced applications in crop breeding. Nat Rev Genet, 25(9):603-622.

[39]LiJB, WuPF, CaoZT, et al., 2024. Machine learning-based prediction models to guide the selection of Cas9 variants for efficient gene editing. Cell Rep, 43(2):113765.

[40]LiJC, JiangXF, 2021. Mol-BERT: an effective molecular representation with BERT for molecular property prediction. Wireless Commun Mobile Comput, 2021:7181815.

[41]LiRY, ChenSS, MatsumotoH, et al., 2023. Predicting rice diseases using advanced technologies at different scales: present status and future perspectives. aBIOTECH, 4(4):359-371.

[42]LiuXY, MatsumotoH, LvTX, et al., 2023. Phyllosphere microbiome induces host metabolic defence against rice false-smut disease. Nat Microbiol, 8(8):1419-1433.

[43]LotterhosKE, 2024. Principles in experimental design for evaluating genomic forecasts. Methods Ecol Evol, 15(9):1466-1482.

[44]LuoCH, HeYJ, ChenYP, 2025. Rhizosphere microbiome regulation: unlocking the potential for plant growth. Curr Res Microb Sci, 8:100322.

[45]LuoF, YuZJ, ZhouQ, et al., 2022. Multi-omics-based discovery of plant signaling molecules. Metabolites, 12(1):76.

[46]LvTX, ZhanCF, PanQQ, et al., 2023. Plant pathogenesis: toward multidimensional understanding of the microbiome. iMeta, 2(3):e129.

[47]MaierhabaY, MomjianC, MankelD, et al., 2024. Dual-BONCAT reveals distinct day- and night-active microbial populations in salt marsh sediments. bioRxiv, preprint.

[48]MatsumotoH, FanXY, WangY, et al., 2021. Bacterial seed endophyte shapes disease resistance in rice. Nat Plants, 7(1):60-72.

[49]MatsumotoH, QianY, FanXY, et al., 2022. Reprogramming of phytopathogen transcriptome by a non-bactericidal pesticide residue alleviates its virulence in rice. Fundam Res, 2(2):198-207.

[50]MidziJ, JefferyDW, BaumannU, et al., 2022. Stress-induced volatile emissions and signalling in inter-plant communication. Plants, 11(19):2566.

[51]MorimotoK, KrahnD, KaschaniF, et al., 2022. Broad-range metalloprotease profiling in plants uncovers immunity provided by defence-related metalloenzyme. New Phytol, 235(3):1287-1301.

[52]MullerE, ShiryanI, BorensteinE, 2024. Multi-omic integration of microbiome data for identifying disease-associated modules. Nat Commun, 15:2621.

[53]PanQQ, LvTX, XuHR, et al., 2024. Gut pathobiome mediates behavioral and developmental disorders in biotoxin-exposed amphibians. Environ Sci Ecotechnol, 21:100415.

[54]PantigosoHA, NewbergerD, VivancoJM, 2022. The rhizosphere microbiome: plant–microbial interactions for resource acquisition. J Appl Microbiol, 133(5):2864-2876.

[55]PaquetteSJ, ZaheerR, StanfordK, et al., 2018. Competition among Escherichia coli strains for space and resources. Vet Sci, 5(4):93.

[56]ReesHA, MinellaAC, BurnettCA, et al., 2021. CRISPR-derived genome editing therapies: progress from bench to bedside. Mol Ther, 29(11):3125-3139.

[57]RooneyLM, AmosWB, HoskissonPA, et al., 2020. Intra-colony channels in E. coli function as a nutrient uptake system. ISME J, 14(10):2461-2473.

[58]SharmaM, SudheerS, UsmaniZ, et al., 2020. Deciphering the omics of plant–microbe interaction: perspectives and new insights. Curr Genomics, 21(5):343-362.

[59]SlettenEM, BertozziCR, 2011. From mechanism to mouse: a tale of two bioorthogonal reactions. Acc Chem Res, 44(9):666-676.

[60]SrivastavaAK, SinghRD, PandeyGK, et al., 2025. Unravelling the molecular dialogue of beneficial microbe–plant interactions. Plant Cell Environ, 48(4):2534-2548.

[61]StukenbrockE, GurrS, 2023. Address the growing urgency of fungal disease in crops. Nature, 617(7959):31-34.

[62]SuP, KangHX, PengQZ, et al., 2024. Microbiome homeostasis on rice leaves is regulated by a precursor molecule of lignin biosynthesis. Nat Commun, 15:23.

[63]TanXH, WangDP, ZhangXW, et al., 2025. A pair of LysM receptors mediates symbiosis and immunity discrimination in Marchantia. Cell, 188(5):1330-1348.e27.

[64]TariqA, GuoSZ, FarhatF, et al., 2025. Engineering synthetic microbial communities: diversity and applications in soil for plant resilience. Agronomy, 15(3):513.

[65]TrivediP, LeachJE, TringeSG, et al., 2020. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol, 18(11):607-621.

[66]UgaldeU, 2006. Autoregulatory signals in mycelial fungi. In: Kües U, Fischer R (Eds.), Growth, Differentiation and Sexuality, 2nd Ed. Springer, Berlin, Heidelberg, p.203-213.

[67]WangBY, ZhaoAS, NovickRP, et al., 2015. Key driving forces in the biosynthesis of autoinducing peptides required for staphylococcal virulence. Proc Natl Acad Sci USA, 112(34):10679-10684.

[68]WangG, RanHM, FanJ, et al., 2022. Fungal-fungal cocultivation leads to widespread secondary metabolite alteration requiring the partial loss-of-function VeA1 protein. Sci Adv, 8(17):eabo6094.

[69]WangMC, CernavaT, 2020. Overhauling the assessment of agrochemical-driven interferences with microbial communities for improved global ecosystem integrity. Environ Sci Ecotechnol, 4:100061.

[70]WangMC, CernavaT, 2023. Soterobionts: disease-preventing microorganisms and proposed strategies to facilitate their discovery. Curr Opin Microbiol, 75:102349.

[71]WangPP, Lehti-ShiuMD, LotreckS, et al., 2024. Prediction of plant complex traits via integration of multi-omics data. Nat Commun, 15:6856.

[72]Weiland-BräuerN, 2021. Friends or foes—microbial interactions in nature. Biology, 10(6):496.

[73]WeiningerD, 1988. SMILES, a chemical language and information system. 1. Introduction to methodology and encoding rules. J Chem Inf Comput Sci, 28(1):31-36.

[74]WhidbeyC, 2025. The right tool for the job: chemical biology and microbiome science. Cell Chem Biol, 32(1):83-97.

[75]WuL, LuoYB, 2021. Bacterial quorum-sensing systems and their role in intestinal bacteria-host crosstalk. Front Microbiol, 12:611413.

[76]XuP, FanXY, MaoYX, et al., 2022. Temporal metabolite responsiveness of microbiota in the tea plant phyllosphere promotes continuous suppression of fungal pathogens. J Adv Res, 39:49-60.

[77]XuP, StirlingE, XieHT, et al., 2023. Continental scale deciphering of microbiome networks untangles the phyllosphere homeostasis in tea plant. J Adv Res, 44:13-22.

[78]ZhanCF, WangMC, 2024. Disease resistance through M genes. Nat Plants, 10(3):352-353.

[79]ZhanCF, MatsumotoH, LiuYF, et al., 2022. Pathways to engineering the phyllosphere microbiome for sustainable crop production. Nat Food, 3(12):997-1004.

[80]ZhangGS, ZhangF, DingG, et al., 2012. Acyl homoserine lactone-based quorum sensing in a methanogenic archaeon. ISME J, 6(7):1336-1344.

[81]ZhangSB, MukherjiR, ChowdhuryS, et al., 2021. Lipopeptide-mediated bacterial interaction enables cooperative predator defense. Proc Natl Acad Sci USA, 118(6):e2013759118.

[82]ZhangXK, LiGJ, ZhangZQ, et al., 2023. 3-Octanol controls gray mold on postharvest fruit by inducing autophagy of Botrytis cinerea. Postharvest Biol Technol, 205:112525.

[83]ZhaoL, WalkowiakS, FernandoWGD, 2023. Artificial intelligence: a promising tool in exploring the phytomicrobiome in managing disease and promoting plant health. Plants, 12(9):1852.

[84]ZhouYQ, WangHK, XuSD, et al., 2022. Bacterial-fungal interactions under agricultural settings: from physical to chemical interactions. Stress Biol, 2:22.

[85]ZhuYL, FangYP, HuangWZ, et al., 2024. AI-driven precision subcellular navigation with fluorescent probes. J Mater Chem B, 12(43):11054-11062.

Open peer comments: Debate/Discuss/Question/Opinion

<1>

Please provide your name, email address and a comment





Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2025 Journal of Zhejiang University-SCIENCE