AHLs介导的群体感应和群体淬灭对植物-根际微生物相互作用的影响

张清旭; 李建鹃; 郭玥; 王炎炎; 彭艳晖; 王裕华; 胡明玥; 林文雄; 吴则焰

doi:10.12357/cjea.20230414

AHLs介导的群体感应和群体淬灭对植物-根际微生物相互作用的影响

1.
福建农林大学菌草与生态学院　福州　350002
2.
福建省林业调查规划院　福州　350003

基金项目: 国家自然科学基金项目(31500443)、福建省自然科学基金项目(2022J01139)、福建省财政林业科技研究项目(2023FKJ26)、福建农林大学科技创新专项(KFb22046XA, KJb22019XA)和福建农林大学生态学一流学科建设项目资助

详细信息

作者简介:
张清旭, 主要研究方向为森林生态学和分子生态学。E-mail: zqx19940817@163.com

通讯作者:
吴则焰, 主要研究方向为森林生态学和分子生态学。E-mail: wuzeyan0977@126.com

中图分类号: S154.4
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出版历程
- 收稿日期: 2023-07-29
- 录用日期: 2023-08-24
- 网络出版日期: 2023-09-21
- 刊出日期: 2024-01-15

Effects of quorum sensing and quorum quenching mediated by AHLs on plant-rhizosphere microbial interactions

1.
College of JunCao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou 350002, China
2.
Forest Investigation and Planning Institute of Fujian Province, Fuzhou 350003, China

Funds: This study was supported by the National Natural Science Foundation of China (31500443), Fujian Provincial Natural Science Foundation (2022J01139), Fujian Provincial Finance and Forestry Science and Technology Research Project (2023FKJ26), Fujian Agriculture and Forestry University Science and Technology Innovation Project (KFb22046XA, KJb22019XA), and Fujian Agriculture and Forestry University First-class Ecological Discipline Construction Project.

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Corresponding author:
WU Zeyan: E-mail: wuzeyan0977@126.com

摘要

摘要:
根际是由植物根系和土壤微生物之间相互作用形成的一种特殊环境, 根际微生物群落的宏基因组是植物微生物组的重要组成部分。植物与根际微生物之间的相互作用是一个复杂的过程。在根际环境中, 微生物群落利用复杂的种内和种间信号传导机制招募特定的微生物, 协调并控制混合群落的行为, 从而影响植物的生长发育和健康。根际微生物能够自发产生、释放特定的信号分子, 并能感知其浓度变化, 从而调节微生物的群体行为, 这一调控系统称为群体感应(quorum sensing, QS)。QS系统的特征是合成和释放特定的信号分子。根际土壤细菌中存在多种QS信号分子, 如N-酰基高丝氨酸内酯(AHLs)、二酮哌嗪、扩散信号因子、次生代谢物、植物激素类分子等。AHLs作为细菌中被广泛研究的QS信号分子, 在植物与根际微生物的相互作用中发挥重要作用。本文综述了AHLs介导的群体感应机制, 并讨论了AHLs在植物与根际微生物相互作用中的调节作用, 包括AHLs对植物的生长发育、逆境耐受性和抗病性等方面的有益影响, 以及AHLs介导的QS系统调控导致的根际致病菌对植物的有害影响, 同时还探讨了基于AHLs的群体淬灭对植物-根际微生物相互作用的影响, 以期为植物健康与农业生产提供新的思路和方法, 推动可持续农业的发展。
- 根际微生物 /
- N-酰基高丝氨酸内酯(AHLs) /
- 群体感应 /
- 群体淬灭 /
- 植物健康
Abstract:
The rhizosphere is a unique environment that arises from the interaction between plant roots and soil microorganisms. The metagenome of the microbial community in the rhizosphere plays a crucial role in shaping the plant microbiome. The interaction between plants and rhizosphere microorganisms is a complex process. In the rhizosphere environment, the microbial community recruits specific microorganisms through intricate signaling mechanisms within and between species. This coordination and control of the mixed community ultimately impacts the growth, development and health of plants. From an academic perspective, rhizosphere signaling mechanisms can be categorized into three primary types. Firstly, plants transmit signals to microorganisms by secreting low molecular weight molecules. Secondly, there is inter- and intraspecific microbial signaling. Lastly, microorganisms transmit signals to plants through compounds they produce. Rhizosphere microbes utilize quorum sensing (QS) to autonomously generate and release distinct signaling molecules, enabling them to detect variations in their concentrations and thereby regulate microbial quorum behavior. QS is a bacterial intercellular communication mechanism that regulates the expression of numerous bacterial genes, which are involved in various plant-microbe interactions. These interactions encompass functions such as biofilm formation, nitrogen fixation, hydrolysis, enzyme and extracellular polysaccharide synthesis, toxin production, cell movement, and intercellular connectivity. QS systems are characterized by the synthesis and release of specific signaling molecules. This process is crucial in rhizosphere communication as it enables the transmission of inter- and intraspecific information through the necessary signaling molecules. Due to the high density and diversity of rhizosphere bacteria, the rhizosphere may facilitate the transmission of QS signals. Additionally, these signaling molecules aid in the colonization of plant root surfaces or other rhizosphere-related areas by rhizosphere bacteria through gene expression mediated by QS. Recent research has revealed the presence of N-acyl-homoserine lactones (AHLs), diketopiperazines, diffusible signaling factor, secondary metabolites, phytohormonelike molecules and other QS signaling molecules in rhizosphere soil bacteria. AHLs are the most extensively studied quorum sensing signaling molecules in bacteria. They not only mediate bacterial quorum sensing, but also have a significant impact on the interaction between plants and rhizosphere microorganisms. This includes the colonization of rhizosphere microorganisms, the maintenance of soil ecosystems and the effects on plant growth. An in-depth understanding of the quorum sensing mechanism mediated by AHLs holds significant importance in promoting agricultural production, enhancing plant health, and fostering sustainable development. This article presents a review of the quorum sensing mechanism mediated by AHLs and discusses the regulatory role of AHLs in the interaction between plants and rhizosphere microorganisms. It explores the beneficial effects of AHLs on plant growth and development, stress tolerance and disease resistance, as well as the harmful effects of rhizosphere pathogenic bacteria on plants due to AHLs-mediated regulation of the QS system. Additionally, the article explores the impact of AHLs-based quorum quenching on plant-rhizosphere microbial interactions, aiming to provide valuable insights for plant health and agricultural production. The article also proposes new ideas and methods to promote the development of sustainable agriculture.
- Rhizosphere microorganisms /
- N-acyl-homoserine lactones (AHLs) /
- Quorum sensing /
- Quorum quenching /
- Plant health

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表 1 不同类型N-酰基高丝氨酸内酯(AHLs)和分泌AHLs的根际细菌对植物的影响

Table 1 The effects of different types of N-acyl-homoserine lactones (AHLs) and AHLs-producing rhizosphere bacteria on plants

相关植物 Associated plant	AHLs/分泌AHLs的细菌 AHLs/AHLs-secreting bacteria	主要影响 Major effect	参考文献 Reference
拟南芥 Arabidopsis thaliana	3-oxo-C6-HSL	增强拟南芥的耐盐性 Enhance salt tolerance in A. thaliana	[47]
	3-oxo-C6-HSL, 3-oxo-C8-HSL	激发GCR1/GPA1基因, 促进根系生长 Stimulate the GCR1/GPA1 genes, promote root growth	[48]
	C6-HSL	改变植物激素平衡 Change the balance of phytohormone	[50]
	C4-HSL	诱导根细胞细胞内钙离子升高 Induce intracellular calcium elevation in root cells	[51]
蒺藜苜蓿 Medicago truncatula	3-oxo-C12-HSL, 3-oxo-C16:1-HSL	诱导生长素反应蛋白和类黄酮合成蛋白, 分泌群体感应拟态物质 Induce auxin-responsive and flavonoid synthesis proteins, secrete mimetics of quorum sensing	[52]
	3-oxo-C14-HSL	增加根系结瘤数量 Increase the number of nodules formed on root systems	[53]
番茄 Solanum lycopersicum	AHL/液化沙雷氏菌 MG1和恶臭假单胞菌 IsoF AHL/Serratia liquefaciens MG1 and Pseudomonas putida IsoF	增加植物系统抗性, 增加水杨酸含量, 诱导防御基因的表达发生变化 Increase systemic resistance of plants, increase salicylic acid content, induce changes in the expression of defense genes	[54]
	AHL/恶臭假单胞菌 AHL/P. putida	促进细胞间的有效交流 Promote efficient communication between the cells	[55]
	3-oxo-C12-HSL, 3-oxo-C14-HSL/ 禾谷伯克霍尔德菌 M12和M14 3-oxo-C12-HSL, 3-oxo-C14-HSL/ Burkholderia graminis M12 and M14	促进植物生长, 诱导抗盐胁迫 Promote plant growth, induce protection against salt stress	[56]
	3-oxo-C14-HSL	保护番茄免受晚疫病 Protect S. lycopersicum from late blight disease	[57]
	3-oxo-C6-HSL, 3-oxo-C8-HSL, 3-oxo-C12-HSL, 3-oxo-C14-HSL	促进植物生长, 诱导对植物病原体的抗性 Promote plant growth, induce resistance to plant pathogens	[58]
小麦 Triticum aestivum	3-oxo-C6-HSL	增强小麦的耐盐性 Enhance salt tolerance in T. aestivum	[47]
	AHL/恶臭假单胞菌 AHL/P. putida	促进细胞间的有效交流 Promote efficient communication between the cells	[55]
	AHL/致黄假单胞菌 AHL/Pseudomonas aureofaciens	AHL介导的交流 AHL-mediated communication	[59]
	C4-HSL	提高植物对真菌病原体的防御能力 Improve plant defense against the fungal pathogens	[60]
油菜 Brassica napus	C4-HSL, C6-HSL, 3-oxo-C6-HSL/ 普城沙雷氏菌 HRO-C48 C4-HSL, C6-HSL, 3-oxo-C6-HSL/ Serratia plymuthica HRO-C48	降低大丽轮枝菌对作物的致病性, 保护作物免受黄萎病的危害, 诱导产生抗真菌挥发物和水解酶 Reduce the pathogenicity of Verticillium dahliae to crops, protect crops against Verticillium wilt, and induce the production of antifungal volatiles and hydrolytic enzymes	[61-62]
黄瓜 Cucumis sativus	C6-HSL, 3-oxo-C10-HSL	促进主根伸长, 促进植物生长 Promote primary root elongation, enhance plant growth	[63]
	3-oxo-C14-HSL	增强植株对病原体的防御能力 Enhance the plant’s defense against pathogens	[63]
鹰嘴豆 Cicer arietinum	C4-HSL	提高植物的生长能力和植物对真菌病原体的防御能力 Improve the plant growth and plant defense against the fungal pathogens	[60]
大麦 Hordeum vulgare	3-OH-C10-HSL/食酸菌 N35 3-OH-C10-HSL/Acidovorax radicis N35	诱导有益菌根际定植, 提高幼苗防御能力 Induce beneficial mycorrhizal colonization, improve seedling defense	[64]
燕麦 Avena sativa	AHL/变形菌门 AHL/Proteobacteria	控制细胞外酶活性 Control extracellular enzyme activity	[65]
玉米 Zea mays	C4-HSL, C6-HSL, 3-oxo-C6-HSL/ 绿针假单胞菌 449 C4-HSL, C6-HSL, 3-oxo-C6-HSL/ Pseudomonas chlororaphis 449	对植物病原真菌具有拮抗活性 Antagonistic activity against phytopathogenic fungi	[66]
芝麻 Sesamum indicum	C6-HSL, C8-HSL/沙雷氏菌属 GS2 C6-HSL, C8-HSL/Serratia glossinae GS2	形成生物膜, 促进植物生长 Form biofilms, promote plant growth	[67]
水稻 Oryza sativa	C4-HSL/气单胞菌属, 肠杆菌属, 肺炎克雷伯菌, 考氏科萨克氏菌, 水性鞘氨醇单胞菌, 斯惠假单胞菌和Providentia rettigeri C4-HSL/Aeromonas sp., Enterobacter sp., Klebsiella pneumoniae, Kosakonia cowanii, Sphingomonas aquatilis, Pseudomonas sihuiensis and Providentia rettigeri	形成生物膜 Form biofilms	[68]
千年芋 Xanthosoma sagittifolium	AHL/假单胞菌 CMR12a AHL/Pseudomonas CMR12a	对群结腐霉(Pythium myriotylum)具有拮抗活性 Antagonistic activity against P. myriotylum	[69]
绿豆 Vigna radiata	3-oxo-C10-HSL	促进根系分枝, 改变根系结构 Promote root formation, change the root architecture	[70]
菜豆 Phaseolus vulgaris	3O-C7-HSL, 3OH-C7-HSL/ 苍白杆菌属 Pv2Z2 3O-C7-HSL, 3OH-C7-HSL/ Ochrobactrum sp. Pv2Z2	促进植物生长和生物降解潜力 Promote plant growth and biodegradation potential	[71]
马铃薯 Solanum tuberosum	3-oxo-C6-HSL, 3-oxo-C8-HSL/ 欧文氏菌 3-oxo-C6-HSL, 3-oxo-C8-HSL/ Erwinia carotovora	抑制毒力因子 Inhibit virulence factor	[72]
烟草 Nicotiana tabacum	C4-HSL, C8-HSL, 3-oxo-C6-HSL/ 粘质沙雷氏菌 C4-HSL, C8-HSL, 3-oxo-C6-HSL/ Serratia marcescens	诱导植物系统抗性 Induce systemic resistance (ISR)	[73]
地黄 Rehmannia glutinosa	AHL/假单胞菌属, 肠杆菌属 AHL/Pseudomonas, Enterobacteriaceae	对植物病原体具有拮抗活性, 引起地黄组培苗枯萎病 Antagonistic activity against plant pathogen, cause severe wilt disease in the tissue culture seedlings of R. glutinosa	[74]
人参 Panax ginseng	C8-HSL, C10-HSL, C12-HSL	改变土壤微生物群落结构 Alter the soil microbial community structure	[75]
碱蓬 Suaeda glauca 芦苇 Phragmites australis	C6-HSL, C8-HSL/红细菌目 C6-HSL, C8-HSL/Rhodobacterales	形成生物膜, 降解二甲基巯基丙酸内盐和油 Form bioflms, degrade Dimethylsulfoniopropionate and oil	[76]
洋葱 Allium cepa	C6-HSL, 3-oxo-C6-HSL/菠萝泛菌 SK-1 C6-HSL, 3-oxo-C6-HSL/Pantoea ananatis SK-1	引起洋葱中心腐烂病 Cause center rot disease of A. cepa	[77]
太子参 Pseudostellaria heterophylla	AHL/粘质沙雷氏菌 AHL/S. marcescens	导致太子参枯萎病 Cause P. heterophylla wilt disease	[78]

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表 2 植物根际土壤或土壤中存在的群体淬灭细菌及作用

Table 2 The quorum-quenching bacteria and their effects present in the plant rhizosphere soil or soil

相关植物或土壤来源 Associated plants or soil source	群体淬灭细菌 Quorum quenching bacteria	主要作用 Major effect	参考文献 Reference
烟草 Nicotiana tabacum	芽孢杆菌、变形杆菌、鞘氨醇单胞菌和博斯氏菌 Bacillus, Proteobacteria, Sphingomonas, Bosea	降解 AHLs Degrade AHLs	[37]
地黄 Rehmannia glutinosa	不动杆菌属 Acinetobacter sp.	破坏有益菌的群体感应系统 Disrupt the quorum sensing system of the beneficial bacteria	[74]
太子参 Pseudostellaria heterophylla	苏云金芽孢杆菌 Bacillus thuringiensis	缓解由粘质沙雷氏菌引起的枯萎病 Alleviate wilt disease caused by Serratia marcescens	[78]
马铃薯 Solanum tuberosum	红平红球菌 Rhodococcus erythropolis	保护马铃薯免受果胶杆菌属(Pectobacterium)细菌的侵害 Protect S. tuberosum against the pathogen Pectobacterium	[126]
	短小芽孢杆菌、荧光假单胞菌、假单胞菌属 Bacillus pumilus, Pseudomonas fluorescens, Pseudomonas	对软腐病原体具有生物防治活性 Have a biocontrol activity against soft-rot pathogens	[128]
	芽孢杆菌属 EM84 Bacillus EM84	抑制病原菌生长, 降低马铃薯块茎中黑腐果胶杆菌 SM1 (Pectobacterium atrosepticum SM1)的致病性 Inhibit growth of pathogen, reduce the pathogenicity of P. atrosepticum SM1 in S. tuberosum tubers	[130]
辣椒 Capsicum annuum	苏云金芽孢杆菌 B. thuringiensis	保护植物免受由欧文氏菌(Erwinia carotovora)所造成的根腐病的侵害 Protect the plant from root rot caused by E. carotovora	[131]
黄瓜 Cucumis sativus	不动杆菌属 C1010 Acinetobacter sp. C1010	降解AHLs, 减轻由欧文氏菌引起的软腐病 Degrade AHLs, attenuate soft rot symptom caused by E. carotovora	[132]
生姜 Zingiber officinale	不动杆菌 GG2、克雷伯氏菌 Se14 Acinetobacter GG2, Klebsiella Se14	降低植物病原体中毒力因子的产生 Attenuate virulence factor production in plant pathogens	[133]
胡萝卜、马铃薯和黄瓜 Daucus carota, Solanum tuberosum and Cucumis sativus	蜡样芽孢杆菌 RC1 Bacillus cereus RC1	缓解由河生肠杆菌(Lelliottia amnigena)引起的软腐病 Alleviate soft rot caused by L. amnigena	[134]
印度36种不同植物根际土壤 Rhizosphere soil of 36 different plant species in India	阿氏芽孢杆菌 J1D、蜡样芽孢杆菌 G Priestia aryabhattai J1D, B. cereus G	水解AHL信号分子, 阻断群体感应系统 Hydrolyse AHL signalling molecules, and block the quorum sensing system	[107]
泰国不同省份的根际土壤 Rhizosphere soils in different provinces of Thailand	链霉菌 Streptomyces	抑制马铃薯软腐病 Inhibit soft rot of S. tuberosum	[135]
农业污染土壤 Agricultural contaminated soil	不动杆菌属 XN-10 Acinetobacter sp. XN-10	降低胡萝卜果胶杆菌(Pectobacterium carotovorum)的致病性 Attenuate the pathogenicity of P. carotovorum	[136]

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