根系分泌物介导的植物对土传病害的抗性机制

doi:10.13560/j.cnki.biotech.bull.1985.2023-0924

摘要/Abstract

摘要：

根系分泌物作为地下防御物质越来越受到关注。近年来，研究逐渐揭示了植物在病原胁迫下根系分泌物的表达特征及其在植物抗病性中的作用，一些由根分泌物介导的抗性调节机制也已被模拟。鉴于土传病害造成的损失日益增加，了解根系分泌物如何抵抗各种病原菌已成为研究热点。本文全面综述了土壤病原胁迫下根系分泌物介导的植物抗性机制，研究病原胁迫下根系分泌物的表达特征，根系分泌物在植物抗病过程中的作用，以及抗性根介导的分泌物和植物抗性的功能。讨论了当前植物病害条件下根系分泌物对植物抗性的影响，旨在为今后土传病害抗性机制的研究提供思路。

关键词: 根系分泌物, 土传病害, 植物抗性

Abstract:

Root exudates have gained increasing attention as underground defense substances. In recent years, studies have gradually revealed the expression characteristics of root exudates in plants under pathogenic stress, as well as their roles in plant disease resistance. Some resistance regulatory mechanisms mediated by root exudates have also been simulated. Given the growing losses caused by soil-borne diseases, understanding how root exudates resist various pathogenic bacteria has become a research focus. This article comprehensively reviews the plant resistance mechanism mediated by root exudates under soil pathogen stress. It examines the expression characteristics of root exudates under pathogen stress, the role of root exudates in the process of plant disease resistance, and the functions of secretions and plant resistance mediated by resistant roots. The article also discussed the impact of root secretions on plant resistance under current plant disease conditions, aiming to provide future insights into the study of resistance mechanisms of soil-borne diseases.

Key words: root exudates, soil-borne diseases, plant resistance

方天一, 岳艳玲. 根系分泌物介导的植物对土传病害的抗性机制[J]. 生物技术通报, 2024, 40(3): 52-61.

FANG Tian-yi, YUE Yan-ling. Mechanisms of Root Exudates-mediated Plant Resistance to Soil-borne Diseases[J]. Biotechnology Bulletin, 2024, 40(3): 52-61.

图/表 4

参考文献 67

[1]	Curl EA, Truelove B. The rhizosphere[M]. Springer Science & Business Media, 2012.
[2]	Walker TS, Bais HP, Grotewold E, et al. Root exudation and rhizosphere biology[J]. Plant Physiol, 2003, 132(1): 44-51. doi: 10.1104/pp.102.019661 pmid: 12746510
[3]	Chai YN, Schachtman DP. Root exudates impact plant performance under abiotic stress[J]. Trends Plant Sci, 2022, 27(1): 80-91. doi: 10.1016/j.tplants.2021.08.003 URL
[4]	毛梦雪, 朱峰. 根系分泌物介导植物抗逆性研究进展与展望[J]. 中国生态农业学报: 中英文, 2021, 29(10): 1649-1657.
	Mao MX, Zhu F. Progress and perspective in research on plant resistance mediated by root exudates[J]. Chin J Eco Agric, 2021, 29(10): 1649-1657.
[5]	陈龙池, 廖利平, 汪思龙, 等. 根系分泌物生态学研究[J]. 生态学杂志, 2002, 21(6):57-62.
	Chen LC, Liao LP, Wang SL, et al. Ecology of root secretion[J]. Chinese Journal of Ecology, 2002, 21(6):57-62.
[6]	Rovira AD. Plant root exudates[J]. Bot Rev, 1969, 35(1): 35-57. doi: 10.1007/BF02859887 URL
[7]	Dessaux Y, Grandclément C, Faure D. Engineering the rhizosphere[J]. Trends Plant Sci, 2016, 21(3): 266-278. doi: S1360-1385(16)00003-0 pmid: 26818718
[8]	肖蓉, 张春芬, 邓舒, 等. 病害胁迫下植物根系分泌物的响应及作用研究进展[J]. 山西农业科学, 2021, 49(1): 110-114.
	Xiao R, Zhang CF, Deng S, et al. Research progress on response and function of plant root exudates under disease stress[J]. J Shanxi Agric Sci, 2021, 49(1): 110-114.
[9]	Vives-Peris V, de Ollas C, Gómez-Cadenas A, et al. Root exudates: from plant to rhizosphere and beyond[J]. Plant Cell Rep, 2020, 39(1): 3-17. doi: 10.1007/s00299-019-02447-5 pmid: 31346716
[10]	Lanoue A, Burlat V, Henkes GJ, et al. De novo biosynthesis of defense root exudates in response to Fusarium attack in barley[J]. New Phytol, 2010, 185(2): 577-588. doi: 10.1111/nph.2009.185.issue-2 URL
[11]	Neal AL, Ahmad S, Gordon-Weeks R, et al. Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere[J]. PLoS One, 2012, 7(4): e35498. doi: 10.1371/journal.pone.0035498 URL
[12]	Strehmel N, Mönchgesang S, Herklotz S, et al. Piriformospora indica stimulates root metabolism of Arabidopsis thaliana[J]. Int J Mol Sci, 2016, 17(7): 1091. doi: 10.3390/ijms17071091 URL
[13]	Ma JQ, Wang WQ, Yang J, et al. Mycorrhizal symbiosis promotes the nutrient content accumulation and affects the root exudates in maize[J]. BMC Plant Biol, 2022, 22(1): 64. doi: 10.1186/s12870-021-03370-2 pmid: 35123400
[14]	Hu LF, Robert CAM, Cadot S, et al. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota[J]. Nat Commun, 2018, 9(1): 2738. doi: 10.1038/s41467-018-05122-7 pmid: 30013066
[15]	Korenblum E, Dong YH, Szymanski J, et al. Rhizosphere microbiome mediates systemic root metabolite exudation by root-to-root signaling[J]. Proc Natl Acad Sci USA, 2020, 117(7): 3874-3883. doi: 10.1073/pnas.1912130117 pmid: 32015118
[16]	甘林, 代玉立, 杨秀娟, 等. 香蕉抗( 感) 病品种根系分泌物对枯萎病菌和枯草芽孢杆菌的生物效应[J]. 应用生态学报, 2020, 31(7): 2279-2286. doi: 10.13287/j.1001-9332.202007.039
	Gan L, Dai YL, Yang XJ, et al. Biological effects of root exudates from resistant and susceptible banana varieties on Fusaiurm oxysporum f. sp. cubense and Bacillus subtilis[J]. Chinese Journal of Applied Ecology, 2020, 31(7): 2279-2286.
[17]	Zhang CS, Feng C, Zheng YF, et al. Root exudates metabolic profiling suggests distinct defense mechanisms between resistant and susceptible tobacco cultivars against black shank disease[J]. Front Plant Sci, 2020, 11: 559775. doi: 10.3389/fpls.2020.559775 URL
[18]	Li XG, Zhang TL, Wang XX, et al. The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen[J]. Int J Biol Sci, 2013, 9(2): 164-173. doi: 10.7150/ijbs.5579 URL
[19]	赵媛媛. 四川辣椒疫霉菌分离、鉴定及辣椒根系分泌物与辣椒疫病抗性的关系[D]. 雅安: 四川农业大学, 2017.
	Zhao YY. Isolation and identification of phytophthorc capsici in Sichuan Province;the relationship of root exudates with resistance to Phytophthora capsici in peppers[D]. Ya'an: Sichuan Agricultural University, 2017.
[20]	王宏乐. 黄瓜不同抗性品种根分泌物及其对枯萎病病菌的影响[D]. 北京: 中国农业科学院, 2009.
	Wang HL. Root exudates from different cucumber disease-resistant cultivars and its effects on the pathogen of cucumber Fusarium wilt[D]. Beijing: Chinese Academy of Agricultural Sciences, 2009.
[21]	周文丽. 西瓜根系分泌物与枯萎病菌之间的相互作用研究[D]. 保定: 河北农业大学, 2014.
	Zhou WL. Interaction analysis between watermelon root exudates and Fusarium oxysporum sp. niveum[D]. Baoding: Hebei Agricultural University, 2014.
[22]	刘畅. 甜瓜不同抗性品种根系分泌物对枯萎病菌的化感作用研究[D]. 沈阳: 沈阳农业大学, 2018.
	Liu C. Allelopathy of root exudates of different resistant muskmelon cultivars on Fusarium wilt[D]. Shenyang: Shenyang Agricultural University, 2018.
[23]	刘晓燕, 金继运, 何萍, 等. 氯化钾抑制玉米茎腐病发生与土壤微生物关系初探[J]. 植物营养与肥料学报, 2007, 13(2): 279-285.
	Liu XY, Jin JY, He P, et al. Preliminary study on the relation between potassium chloride suppressing corn stalk rot and soil microorganism characteristics[J]. Plant Nutr Fertil Sci, 2007, 13(2): 279-285.
[24]	Ipcho S, Sundelin T, Erbs G, et al. Fungal innate immunity induced by bacterial microbe-associated molecular patterns(MAMPs)[J]. G3, 2016, 6(6): 1585-1595. doi: 10.1534/g3.116.027987 URL
[25]	Lee MW, Huffaker A, Crippen D, et al. Plant elicitor peptides promote plant defences against nematodes in soybean[J]. Mol Plant Pathol, 2018, 19(4): 858-869. doi: 10.1111/mpp.12570 pmid: 28600875
[26]	张成省. 烟草根系分泌物介导的黑胫病抗性机制研究[D]. 北京: 中国农业科学院, 2020.
	Zhang CS. Mechanisms of tobacco resistance agaisnt black shank mediated by root exudates[D]. Beijing: Chinese Academy of Agricultural Sciences, 2020.
[27]	Rosier A, Medeiros FHV, Bais HP. Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions[J]. Plant Soil, 2018, 428(1): 35-55. doi: 10.1007/s11104-018-3679-5
[28]	Sasse J, Martinoia E, Northen T. Feed your friends: do plant exudates shape the root microbiome?[J]. Trends Plant Sci, 2018, 23(1): 25-41. doi: S1360-1385(17)30199-1 pmid: 29050989
[29]	Canarini A, Kaiser C, Merchant A, et al. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli[J]. Front Plant Sci, 2019, 10: 157. doi: 10.3389/fpls.2019.00157 pmid: 30881364
[30]	Yuan MH, Ngou BPM, Ding PT, et al. PTI-ETI crosstalk: an integrative view of plant immunity[J]. Curr Opin Plant Biol, 2021, 62: 102030. doi: 10.1016/j.pbi.2021.102030 URL
[31]	Yuan MH, Jiang ZY, Bi GZ, et al. Pattern-recognition receptors are required for NLR-mediated plant immunity[J]. Nature, 2021, 592(7852): 105-109. doi: 10.1038/s41586-021-03316-6
[32]	Bi GZ, Zhou ZY, Wang WB, et al. Receptor-like cytoplasmic kinases directly link diverse pattern recognition receptors to the activation of mitogen-activated protein kinase cascades in Arabidopsis[J]. Plant Cell, 2018, 30(7): 1543-1561. doi: 10.1105/tpc.17.00981 URL
[33]	Philippot L, Raaijmakers JM, Lemanceau P, et al. Going back to the roots: the microbial ecology of the rhizosphere[J]. Nat Rev Microbiol, 2013, 11(11): 789-799. doi: 10.1038/nrmicro3109 pmid: 24056930
[34]	Li XG, Wei Q, Liu B, et al. Root exudates of transgenic cotton and their effects on Fusarium oxysporum[J]. Front Biosci(Landmark Ed), 2013, 18(2): 725-733.
[35]	Yang GD, Zhou BL, Zhang XY, et al. Effects of tomato root exudates on Meloidogyne incognita[J]. PLoS One, 2016, 11(4): e0154675. doi: 10.1371/journal.pone.0154675 URL
[36]	杨莉, 于俐, 孙卓, 等. 人参根系分泌物中有机酸及皂苷对人参病原菌与生防菌的化感差异研究[J]. 中国农业科技导报, 2022, 24(6): 145-155. doi: 10.13304/j.nykjdb.2021.0303
	Yang L, Yu L, Sun Z, et al. Allelopathic effects of organic acids and saponins in ginseng root exudates on pathogenic and biocontrol bacteria[J]. J Agric Sci Technol, 2022, 24(6): 145-155.
[37]	张敏. 光果甘草连作对土壤微生物群落结构及根腐病病原菌影响的研究[D]. 石河子: 石河子大学, 2021.
	Zhang M. Effects of continuous cropping of Glycyrrhiza glabra L. on soil microbial community structure and root rot pathogens[D]. Shihezi: Shihezi University, 2021.
[38]	陈娜, 高翔, 涂攀峰, 等. 施钾调控烟草根系酚酸的释放及其防控青枯病的研究[J]. 热带农业工程, 2018, 42(2): 1-6.
	Chen N, Gao X, Tu PF, et al. Analysis on the release of phenolic acids from tobacco and control of tobacco bacterial wilt by potassium fertilizer[J]. Trop Agric Eng, 2018, 42(2): 1-6.
[39]	Yang WH, Guo YT, Li Y, et al. Benzoic acid promotes Fusarium wilt incidence by enhancing susceptibility and reducing photosynthesis of faba bean[J]. Ann Appl Biol, 2023.
[40]	Li ZF, He CL, Wang Y, et al. Enhancement of trichothecene mycotoxins of Fusarium oxysporum by ferulic acid aggravates oxidative damage in Rehmannia glutinosa Libosch[J]. Sci Rep, 2016, 6: 33962. doi: 10.1038/srep33962
[41]	程培军, 翟文汇, 张翔, 等. 不同氮形态和施用空间分布对烤烟效应及土壤氮素的影响[J]. 江西农业学报, 2020, 32(9): 97-101.
	Cheng PJ, Zhai WH, Zhang X, et al. Effect of different nitrogen forms and application spatial distribution on flue-cured tobacco and soil nitrogen[J]. Acta Agric Jiangxi, 2020, 32(9): 97-101.
[42]	Li SL, Xu C, Wang J, et al. Cinnamic, myristic and fumaric acids in tobacco root exudates induce the infection of plants by Ralstonia solanacearum[J]. Plant Soil, 2017, 412(1): 381-395. doi: 10.1007/s11104-016-3060-5 URL
[43]	Tang BZ, Liu CY, Li ZQ, et al. Multilayer regulatory landscape during pattern-triggered immunity in rice[J]. Plant Biotechnol J, 2021, 19(12): 2629-2645. doi: 10.1111/pbi.13688 pmid: 34437761
[44]	Tena G. PTI and ETI are one[J]. Nat Plants, 2021, 7(12): 1527. doi: 10.1038/s41477-021-01057-y pmid: 34907297
[45]	Ponce De León I, Schmelz EA, Gaggero C, et al. Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection[J]. Mol Plant Pathol, 2012, 13(8): 960-974. doi: 10.1111/j.1364-3703.2012.00806.x pmid: 22551417
[46]	Venus Y, Oelmüller R. Arabidopsis ROP1 and ROP6 influence germination time, root morphology, the formation of F-actin bundles, and symbiotic fungal interactions[J]. Mol Plant, 2013, 6(3): 872-886. doi: 10.1093/mp/sss101 URL
[47]	Zhang WC, Gao WD, Whalley WR, et al. Physical properties of a sandy soil as affected by incubation with a synthetic root exudate: strength, thermal and hydraulic conductivity, and evaporation[J]. Eur J Soil Sci, 2021, 72(2): 782-792. doi: 10.1111/ejss.13007 pmid: 33776539
[48]	Zhao ML, Zhao J, Yuan J, et al. Root exudates drive soil-microbe-nutrient feedbacks in response to plant growth[J]. Plant Cell Environ, 2021, 44(2): 613-628. doi: 10.1111/pce.v44.2 URL
[49]	张海龙, 武润琴, 李佳佳, 等. 根系分泌物C∶N对刺槐林地土壤理化特征和土壤呼吸的影响[J]. 应用生态学报, 2022, 33(4): 949-956. doi: 10.13287/j.1001-9332.202204.013
	Zhang HL, Wu RQ, Li JJ, et al. Effects of root exudates C: N on soil physical and chemical characteristics and soil respiration in Robinia pseudoacacia plantation[J]. Chin J Appl Ecol, 2022, 33(4): 949-956.
[50]	任改弟, 王光飞, 马艳. 根系分泌物与土传病害的关系研究进展[J]. 土壤, 2021, 53(2): 229-235.
	Ren GD, Wang GF, Ma Y. Research progresses on relationship between plant root exudates and soil-borne diseases[J]. Soils, 2021, 53(2): 229-235.
[51]	Olanrewaju OS, Ayangbenro AS, Glick BR, et al. Plant health: feedback effect of root exudates-rhizobiome interactions[J]. Appl Microbiol Biotechnol, 2019, 103(3): 1155-1166. doi: 10.1007/s00253-018-9556-6 pmid: 30570692
[52]	García-Contreras R, Maeda T, Wood TK. Can resistance against quorum-sensing interference be selected?[J]. ISME J, 2016, 10(1): 4-10. doi: 10.1038/ismej.2015.84 pmid: 26023871
[53]	Liu YP, Feng HC, Fu RX, et al. Induced root-secreted D-galactose functions as a chemoattractant and enhances the biofilm formation of Bacillus velezensis SQR9 in an McpA-dependent manner[J]. Appl Microbiol Biotechnol, 2020, 104(2): 785-797. doi: 10.1007/s00253-019-10265-8
[54]	Zhuang W, Yu XL, Hu RW, et al. Diversity, function and assembly of mangrove root-associated microbial communities at a continuous fine-scale[J]. NPJ Biofilms Microbiomes, 2020, 6(1): 52. doi: 10.1038/s41522-020-00164-6
[55]	Tong XN, Wang XZ, He XJ, et al. Effects of antibiotics on microbial community structure and microbial functions in constructed wetlands treated with artificial root exudates[J]. Environ Sci Process Impacts, 2020, 22(1): 217-226. doi: 10.1039/C9EM00458K URL
[56]	Feng HC, Fu RX, Hou XQ, et al. Chemotaxis of beneficial rhizobacteria to root exudates: the first step towards root-microbe rhizosphere interactions[J]. Int J Mol Sci, 2021, 22(13): 6655. doi: 10.3390/ijms22136655 URL
[57]	Mauchline TH, Malone JG. Life in earth - the root microbiome to the rescue?[J]. Curr Opin Microbiol, 2017, 37: 23-28. doi: S1369-5274(16)30225-9 pmid: 28437662
[58]	Zhao J, Wu YX, Ho HH, et al. PBT1, a novel antimicrobial protein from the biocontrol agent Bacillus subtilis XF-1 against Plasmodiophora brassicae[J]. Eur J Plant Pathol, 2016, 145(3): 583-590. doi: 10.1007/s10658-016-0905-y URL
[59]	徐世荣, 陈骧, 吴云鹏. 细菌芽孢形成机制在微生态制剂生产中的应用[J]. 食品与生物技术学报, 2007, 26(4): 121-126.
	Xu SR, Chen X, Wu YP. Application of the mechanism of sporulation in production of pharmaceutical probiotics[J]. J Food Sci Biotechnol, 2007, 26(4): 121-126.
[60]	Ren GD, Meng TZ, Ma Y. Sugars altered fungal community composition and caused high network complexity in a Fusarium wilt pathogen-infested soil[J]. Biol Fertil Soils, 2020, 56(3): 395-409. doi: 10.1007/s00374-019-01424-0
[61]	Rudrappa T, Czymmek KJ, Paré PW, et al. Root-secreted malic acid recruits beneficial soil bacteria[J]. Plant Physiol, 2008, 148(3): 1547-1556. doi: 10.1104/pp.108.127613 pmid: 18820082
[62]	Gulati S, Ballhausen MB, Kulkarni P, et al. A non-invasive soil-based setup to study tomato root volatiles released by healthy and infected roots[J]. Sci Rep, 2020, 10(1): 12704. doi: 10.1038/s41598-020-69468-z pmid: 32728091
[63]	Sun HS, Jiang SX, Jiang CC, et al. A review of root exudates and rhizosphere microbiome for crop production[J]. Environ Sci Pollut Res Int, 2021, 28(39): 54497-54510. doi: 10.1007/s11356-021-15838-7
[64]	杨帆. 伴生植物根系分泌物对根结线虫及番茄抗性的影响[D]. 哈尔滨: 东北农业大学, 2020.
	Yang F. Effects of root exudates from companion cropping plants on root knot nematode and resistance of tomato[D]. Harbin:Northeast Agricultural University, 2020.
[65]	吕慧芳. 小麦—西瓜间作体系中根系分泌物的变化及其对西瓜枯萎病抗性的影响机制[D]. 武汉: 华中农业大学, 2019.
	Lyu HF. Changes of root exudates in the wheat-watermelon intercropping system and its mechanism of resistance to watermelon Fusarium wilt[D]. Wuhan: Huazhong Agricultural University, 2019.
[66]	李春霞. 伴生小麦对西瓜枯萎病抗性调控的机理研究[D]. 哈尔滨: 东北农业大学, 2019.
	Li CX. The mechanism of enhancement the suppression of Fusarium wilt in watermelon by wheat as companion crop[D]. Harbin: Northeast Agricultural University, 2019.
[67]	肖靖秀. 小麦//蚕豆的根系分泌物特征及其对蚕豆枯萎病菌的响应研究[D]. 昆明: 云南农业大学, 2014.
	Xiao JX. Characterization of root secretion of wheat//fava bean and its response to Fiba bean wilt fungus[D]. Kunming: Yunnan Agricultural University, 2014.