Rhizosphere immunity: targeting the underground for sustainable plant health management
Zhong WEI, Ville-Petri FRIMAN, Thomas POMMIER, Stefan GEISEN, Alexandre JOUSSET, Qirong SHEN
Rhizosphere immunity: targeting the underground for sustainable plant health management
Managing plant health is a great challenge for modern food production and is further complicated by the lack of common ground between the many disciplines involved in disease control. Here we present the concept of rhizosphere immunity, in which plant health is considered as an ecosystem level property emerging from networks of interactions between plants, microbiota and the surrounding soil matrix. These interactions can potentially extend the innate plant immune system to a point where the rhizosphere immunity can fulfil all four core functions of a full immune system: pathogen prevention, recognition, response and homeostasis. We suggest that considering plant health from a meta-organism perspective will help in developing multidisciplinary pathogen management strategies that focus on steering the whole plant-microbe-soil networks instead of individual components. This might be achieved by bringing together the latest discoveries in phytopathology, microbiome research, soil science and agronomy to pave the way toward more sustainable and productive agriculture.
rhizosphere / soil microbiome / plant immunity / microbial ecology / plant health / soilborne pathogens
[1] |
Savary S, Willocquet L, Pethybridge S J, Esker P, McRoberts N, Nelson A. The global burden of pathogens and pests on major food crops. Nature Ecology & Evolution, 2019, 3(3): 430–439
CrossRef
Pubmed
Google scholar
|
[2] |
Göhre V, Robatzek S. Breaking the barriers: microbial effector molecules subvert plant immunity. Annual Review of Phytopathology, 2008, 46(1): 189–215
CrossRef
Pubmed
Google scholar
|
[3] |
War A R, Paulraj M G, Ahmad T, Buhroo A A, Hussain B, Ignacimuthu S, Sharma H C. Mechanisms of plant defense against insect herbivores. Plant Signaling & Behavior, 2012, 7(10): 1306–1320
CrossRef
Pubmed
Google scholar
|
[4] |
Kumar H, Kawai T, Akira S. Pathogen recognition by the innate immune system. International Reviews of Immunology, 2011, 30(1): 16–34
CrossRef
Pubmed
Google scholar
|
[5] |
Sharrock J, Sun J C. Innate immunological memory: from plants to animals. Current Opinion in Immunology, 2020, 62: 69–78
CrossRef
Pubmed
Google scholar
|
[6] |
Dong O X, Ronald P C. Genetic engineering for disease resistance in plants: recent progress and future perspectives. Plant Physiology, 2019, 180(1): 26–38
CrossRef
Pubmed
Google scholar
|
[7] |
Raman R. The impact of Genetically Modified (GM) crops in modern agriculture: a review. GM Crops and Food: Biotechnology in Agriculture and the Food Chain, 2017, 8(4): 195–208
CrossRef
Pubmed
Google scholar
|
[8] |
Hawkins N J, Bass C, Dixon A, Neve P. The evolutionary origins of pesticide resistance. Biological Reviews of the Cambridge Philosophical Society, 2018, 94(1): 135–155
CrossRef
Pubmed
Google scholar
|
[9] |
Zhang W, Cao G, Li X, Zhang H, Wang C, Liu Q, Chen X, Cui Z, Shen J, Jiang R, Mi G, Miao Y, Zhang F, Dou Z. Closing yield gaps in China by empowering smallholder farmers. Nature, 2016, 537(7622): 671–674
CrossRef
Pubmed
Google scholar
|
[10] |
Chen X P, Cui Z L, Vitousek P M, Cassman K G, Matson P A, Bai J S, Meng Q F, Hou P, Yue S C, Rmheld V, Zhang F S. Integrated soil-crop system management for food security. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(16): 6399–6404
CrossRef
Pubmed
Google scholar
|
[11] |
Teixeira P J P, Colaianni N R, Fitzpatrick C R, Dangl J L. Beyond pathogens: microbiota interactions with the plant immune system. Current Opinion in Microbiology, 2019, 49: 7–17
CrossRef
Pubmed
Google scholar
|
[12] |
Sánchez-Cañizares C, Jorrín B, Poole P S, Tkacz A. Understanding the holobiont: the interdependence of plants and their microbiome. Current Opinion in Microbiology, 2017, 38: 188–196
CrossRef
Pubmed
Google scholar
|
[13] |
McNear J, David H. The rhizosphere— roots, soil and everything in between. Nature Education Knowledge, 2013, 4(3): 1
|
[14] |
Hartmann A, Rothballer M, Schmid M. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant and Soil, 2008, 312(1–2): 7–14
CrossRef
Google scholar
|
[15] |
Jones D L, Hinsinger P. The rhizosphere: complex by design. Plant and Soil, 2008, 312(1–2): 1–6
CrossRef
Google scholar
|
[16] |
Brink S C. Unlocking the secrets of the rhizosphere. Trends in Plant Science, 2016, 21(3): 169–170
CrossRef
Pubmed
Google scholar
|
[17] |
Neutra M R, Kozlowski P A. Mucosal vaccines: the promise and the challenge. Nature Reviews: Immunology, 2006, 6(2): 148–158
CrossRef
Pubmed
Google scholar
|
[18] |
Jones J D G, Dangl J L. The plant immune system. Nature, 2006, 444(7117): 323–329
CrossRef
Pubmed
Google scholar
|
[19] |
Dangl J L, Jones J D G. Plant pathogens and integrated defence responses to infection. Nature, 2001, 411(6839): 826–833
CrossRef
Pubmed
Google scholar
|
[20] |
Chisholm S T, Coaker G, Day B, Staskawicz B J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 2006, 124(4): 803–814
CrossRef
Pubmed
Google scholar
|
[21] |
Bittel P, Robatzek S. Microbe-associated molecular patterns (MAMPs) probe plant immunity. Current Opinion in Plant Biology, 2007, 10(4): 335–341
CrossRef
Pubmed
Google scholar
|
[22] |
Newman M A, Sundelin T, Nielsen J T, Erbs G. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Frontiers of Plant Science, 2013, 4: 139
CrossRef
Pubmed
Google scholar
|
[23] |
Carstens M, Katherine J. Plant-pathogen arms race. Science, 2007, 318(5850): 529
CrossRef
Google scholar
|
[24] |
Anderson J P, Gleason C A, Foley R C, Thrall P H, Burdon J B, Singh K B. Plants versus pathogens: an evolutionary arms race. Functional Plant Biology, 2010, 37(6): 499–512
CrossRef
Pubmed
Google scholar
|
[25] |
Gururani M A, Venkatesh J, Upadhyaya C P, Nookaraju A, Pandey S K, Park S W. Plant disease resistance genes: current status and future directions. Physiological and Molecular Plant Pathology, 2012, 78: 51–65
CrossRef
Google scholar
|
[26] |
Ma L J, van der Does H C, Borkovich K A, Coleman J J, Daboussi M J, Pietro A D, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman P M, Kang S, Shim W B, Woloshuk C, Xie X H, Xu J R, Antoniw J, Baker S E, Bluhm B H, Breakspear A, Brown D W, Butchko R A EChapman S, Coulson R, Coutinho P M, Danchin E G J, Diener A, Gale L R, Gardiner D M, Goff S, Hammond-Kosack K E, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira C D, Koehrsen M, Kumar L, Lee Y-H, Li L, Manners J M, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park S Y, Proctor R H, Regev A, Ruiz-Roldan M C, Sain D, Sakthikumar S, Sykes S, Schwartz D C, Turgeon B G, Wapinski I, Yoder O, Young S, Zeng Q D, Zhou S G, Galagan J, Cuomo C A, Kistler H C, Rep M. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium.Nature,2010, 464(7287): 367–373
|
[27] |
Litman G W, Rast J P, Fugmann S D. The origins of vertebrate adaptive immunity. Nature Reviews: Immunology, 2010, 10(8): 543–553
CrossRef
Pubmed
Google scholar
|
[28] |
Marraffini L A, Sontheimer E J. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nature Reviews: Genetics, 2010, 11(3): 181–190
CrossRef
Pubmed
Google scholar
|
[29] |
Danhorn T, Fuqua C. Biofilm formation by plant-associated bacteria. Annual Review of Microbiology, 2007, 61(1): 401–422
CrossRef
Pubmed
Google scholar
|
[30] |
Berendsen R L, Pieterse C M J, Bakker P A H M. The rhizosphere microbiome and plant health. Trends in Plant Science, 2012, 17(8): 478–486
CrossRef
Pubmed
Google scholar
|
[31] |
Lozupone C A, Stombaugh J I, Gordon J I, Jansson J K, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature, 2012, 489(7415): 220–230
CrossRef
Pubmed
Google scholar
|
[32] |
Meade K G, O’Farrelly C. b-Defensins: farming the microbiome for homeostasis and health. Frontiers in Immunology, 2019, 9: 3072
CrossRef
Pubmed
Google scholar
|
[33] |
Wei Z, Yang T, Friman V P, Xu Y, Shen Q, Jousset A. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nature Communications, 2015, 6(1): 8413
CrossRef
Pubmed
Google scholar
|
[34] |
Mallon C A, Poly F, Le Roux X, Marring I, van Elsas J D, Salles J F. Resource pulses can alleviate the biodiversity-invasion relationship in soil microbial communities. Ecology, 2015, 96(4): 915–926
CrossRef
Pubmed
Google scholar
|
[35] |
Mazurier S, Corberand T, Lemanceau P, Raaijmakers J M. Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME Journal, 2009, 3(8): 977–991
CrossRef
Pubmed
Google scholar
|
[36] |
Hu J, Wei Z, Friman V P, Gu S H, Wang X F, Eisenhauer N, Yang T J, Ma J, Shen Q R, Xu Y C, Jousset A. Probiotic diversity enhances rhizosphere microbiome function and plant disease Suppression. mBio, 2016, 7(6): e01790–16
CrossRef
Pubmed
Google scholar
|
[37] |
Raaijmakers J M, Mazzola M. Soil immune responses. Science, 2016, 352(6292): 1392–1393
CrossRef
Pubmed
Google scholar
|
[38] |
Gu Y, Hou Y G, Huang D P, Hao Z X, Wang X F, Wei Z, Jousset A, Tan S Y, Xu D B, Shen Q R, Xu Y C, Friman V P. Application of biochar reduces Ralstonia solanacearum infection via effects on pathogen chemotaxis, swarming motility, and root exudate adsorption. Plant and Soil, 2017, 415(1–2): 269–281
CrossRef
Google scholar
|
[39] |
Abawi G S, Widmer T L. Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops. Applied Soil Ecology, 2000, 15(1): 37–47
CrossRef
Google scholar
|
[40] |
Ngeno D C, Murungi L K, Fundi D I, Wekesa V, Haukeland S, Mbaka J. Soil chemical properties influence abundance of nematode trophic groups and Ralstonia solanacearum in high tunnel tomato production. AAS Open Research, 2019, 2: 3
CrossRef
Google scholar
|
[41] |
Rezanezhad F, Price J S, Quinton W L, Lennartz B, Milojevic T, Van Cappellen P. Structure of peat soils and implications for water storage, flow and solute transport: a review update for geochemists. Chemical Geology, 2016, 429: 75–84
CrossRef
Google scholar
|
[42] |
Narisawa K, Shimura M, Usuki F, Fukuhara S, Hashiba T. Effects of pathogen density, soil moisture, and soil pH on biological control of clubroot in Chinese cabbage by Heteroconium chaetospira. Plant Disease, 2005, 89(3): 285–290
CrossRef
Pubmed
Google scholar
|
[43] |
Xun W, Zhao J, Xue C, Zhang G, Ran W, Wang B, Shen Q, Zhang R. Significant alteration of soil bacterial communities and organic carbon decomposition by different long-term fertilization management conditions of extremely low-productivity arable soil in South China. Environmental Microbiology, 2016, 18(6): 1907–1917
CrossRef
Pubmed
Google scholar
|
[44] |
Venturi V, Keel C. Signaling in the Rhizosphere. Trends in Plant Science, 2016, 21(3): 187–198
CrossRef
Pubmed
Google scholar
|
[45] |
Carvalhais L C, Dennis P G, Badri D V, Kidd B N, Vivanco J M, Schenk P M. Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Molecular Plant-Microbe Interactions, 2015, 28(9): 1049–1058
CrossRef
Pubmed
Google scholar
|
[46] |
Sasse J, Martinoia E, Northen T. Feed your friends: do plant exudates shape the root microbiome. Trends in Plant Science, 2018, 23(1): 25–41
CrossRef
Pubmed
Google scholar
|
[47] |
Lebeis S L, Paredes S H, Lundberg D S, Breakfield N, Gehring J, McDonald M, Malfatti S, Glavina del Rio T, Jones C D, Tringe S G, Dangl J L. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science, 2015, 349(6250): 860–864
CrossRef
Pubmed
Google scholar
|
[48] |
Downie J A. Calcium signals in plant immunity: a spiky issue. New Phytologist, 2014, 204(4): 733–735
CrossRef
Pubmed
Google scholar
|
[49] |
Aznar A, Chen N W G, Thomine S, Dellagi A. Immunity to plant pathogens and iron homeostasis. Plant Science, 2015, 240: 90–97
CrossRef
Pubmed
Google scholar
|
[50] |
Castrillo G, Teixeira P J P L, Paredes S H, Law T F, de Lorenzo L, Feltcher M E, Finkel O M, Breakfield N W, Mieczkowski P, Jones C D, Paz-Ares J, Dangl J L. Root microbiota drive direct integration of phosphate stress and immunity. Nature, 2017, 543(7646): 513–518
CrossRef
Pubmed
Google scholar
|
[51] |
Wolf A B, Vos M, de Boer W, Kowalchuk G A. Impact of matric potential and pore size distribution on growth dynamics of filamentous and non-filamentous soil bacteria. PLoS One, 2013, 8(12): e83661
CrossRef
Pubmed
Google scholar
|
[52] |
Vos M, Wolf A B, Jennings S J, Kowalchuk G A. Micro-scale determinants of bacterial diversity in soil. FEMS Microbiology Reviews, 2013, 37(6): 936–954
CrossRef
Pubmed
Google scholar
|
[53] |
Serna-Chavez H M, Fierer N, van Bodegom P M. Global drivers and patterns of microbial abundance in soil. Global Ecology and Biogeography, 2013, 22(10): 1162–1172
CrossRef
Google scholar
|
[54] |
Wei Z, Gu Y A, Friman V P, Kowalchuk G A, Xu Y C, Shen Q R, Jousset A. Initial soil microbiome composition and functioning predetermine future plant health. Science Advances,2019, 5(9): eaaw0759
|
[55] |
Bakker P A H M, Pieterse C M J, de Jonge R, Berendsen R L. The soil-borne legacy. Cell, 2018, 172(6): 1178–1180
CrossRef
Pubmed
Google scholar
|
[56] |
Rashid M I, Mujawar L H, Shahzad T, Almeelbi T, Ismail I M I, Oves M. Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiological Research, 2016, 183: 26–41
CrossRef
Pubmed
Google scholar
|
[57] |
Mazor G, Kidron G J, Vonshak A, Abeliovich A. The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiology Ecology, 1996, 21(2): 121–130
CrossRef
Google scholar
|
[58] |
Loper J E, Henkels M D. Utilization of heterologous siderophores enhances levels of iron available to Pseudomonas putida in the rhizosphere. Applied and Environmental Microbiology, 1999, 65(12): 5357–5363
CrossRef
Pubmed
Google scholar
|
[59] |
Chovatiya R, Medzhitov R. Stress, inflammation, and defense of homeostasis. Molecular Cell, 2014, 54(2): 281–288
CrossRef
Pubmed
Google scholar
|
[60] |
Lee M H, Jeon H S, Kim S H, Chung J H, Roppolo D, Lee H J, Cho H J, Tobimatsu Y, Ralph J, Park O K. Lignin-based barrier restricts pathogens to the infection site and confers resistance in plants. EMBO Journal, 2019, 38(23): e101948
CrossRef
Pubmed
Google scholar
|
[61] |
Pollard M, Beisson F, Li Y, Ohlrogge J B. Building lipid barriers: biosynthesis of cutin and suberin. Trends in Plant Science, 2008, 13(5): 236–246
CrossRef
Pubmed
Google scholar
|
[62] |
Hose E, Clarkson D T, Steudle E, Schreiber L, Hartung W. The exodermis: a variable apoplastic barrier. Journal of Experimental Botany, 2001, 52(365): 2245–2264
CrossRef
Pubmed
Google scholar
|
[63] |
Beauregard P B, Chai Y, Vlamakis H, Losick R, Kolter R. Bacillus subtilis biofilm induction by plant polysaccharides. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(17): E1621–E1630
CrossRef
Pubmed
Google scholar
|
[64] |
Choi H W, Klessig D F. DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biology, 2016, 16(1): 232
CrossRef
Pubmed
Google scholar
|
[65] |
De Lorenzo G, Ferrari S, Cervone F, Okun E. Extracellular DAMPs in plants and mammals: immunity, tissue damage and repair. Trends in Immunology, 2018, 39(11): 937–950
CrossRef
Pubmed
Google scholar
|
[66] |
de Weert S, Kuiper I, Lagendijk E L, Lamers G E M, Lugtenberg B J J. Role of chemotaxis toward fusaric acid in colonization of hyphae of Fusarium oxysporum f. sp. radicis-lycopersici by Pseudomonas fluorescens WCS365. Molecular Plant-Microbe Interactions, 2004, 17(11): 1185–1191
CrossRef
Pubmed
Google scholar
|
[67] |
López-Díaz C, Rahjoo V, Sulyok M, Ghionna V, Martín-Vicente A, Capilla J, Di Pietro A, López-Berges M S. Fusaric acid contributes to virulence of Fusarium oxysporum on plant and mammalian hosts. Molecular Plant Pathology, 2018, 19(2): 440–453
CrossRef
Pubmed
Google scholar
|
[68] |
Notz R, Maurhofer M, Dubach H, Haas D, Défago G. Fusaric acid-producing strains of Fusarium oxysporum alter 2,4-diacetylphloroglucinol biosynthetic gene expression in Pseudomonas fluorescens CHA0 in vitro and in the rhizosphere of wheat. Applied and Environmental Microbiology, 2002, 68(5): 2229–2235
CrossRef
Pubmed
Google scholar
|
[69] |
Chapelle E, Mendes R, Bakker P A H, Raaijmakers J M. Fungal invasion of the rhizosphere microbiome. ISME Journal, 2016, 10(1): 265–268
CrossRef
Pubmed
Google scholar
|
[70] |
Fujiwara A, Fujisawa M, Hamasaki R, Kawasaki T, Fujie M, Yamada T. Biocontrol of Ralstonia solanacearum by treatment with lytic bacteriophages. Applied and Environmental Microbiology, 2011, 77(12): 4155–4162
CrossRef
Pubmed
Google scholar
|
[71] |
Ye X, Li Z, Luo X, Wang W, Li Y, Li R, Zhang B, Qiao Y, Zhou J, Fan J, Wang H, Huang Y, Cao H, Cui Z, Zhang R. A predatory myxobacterium controls cucumber Fusarium wilt by regulating the soil microbial community. Microbiome, 2020, 8(1): 49
CrossRef
Pubmed
Google scholar
|
[72] |
Xiong W, Song Y, Yang K, Gu Y, Wei Z, Kowalchuk G A, Xu Y, Jousset A, Shen Q, Geisen S. Rhizosphere protists are key determinants of plant health. Microbiome, 2020, 8(1): 27
CrossRef
Pubmed
Google scholar
|
[73] |
Dickman M, Williams B, Li Y, de Figueiredo P, Wolpert T. Reassessing apoptosis in plants. Nature Plants, 2017, 3(10): 773–779
CrossRef
Pubmed
Google scholar
|
[74] |
Voigt C A. Callose-mediated resistance to pathogenic intruders in plant defense-related papillae. Frontiers of Plant Science, 2014, 5: 168
CrossRef
Pubmed
Google scholar
|
[75] |
Wang X, Wei Z, Li M, Wang X, Shan A, Mei X, Jousset A, Shen Q, Xu Y, Friman V P. Parasites and competitors suppress bacterial pathogen synergistically due to evolutionary trade-offs. Evolution, 2017, 71(3): 733–746
CrossRef
Pubmed
Google scholar
|
[76] |
Bais H P, Weir T L, Perry L G, Gilroy S, Vivanco J M. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 2006, 57(1): 233–266
CrossRef
Pubmed
Google scholar
|
[77] |
Ji C, Fan Y, Zhao L. Review on biological degradation of mycotoxins. Animal Nutrition, 2016, 2(3): 127–133
CrossRef
Pubmed
Google scholar
|
[78] |
Radl V, Winkler J B, Kublik S, Yang L H, Winkelmann T, Vestergaard G, Schröder P, Schloter M. Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease. Environmental Microbiology, 2019, 14(1): 9
CrossRef
Google scholar
|
[79] |
Komy Z R, Shaker A M, Heggy S E M, El-Sayed M E A. Kinetic study for copper adsorption onto soil minerals in the absence and presence of humic acid. Chemosphere, 2014, 99: 117–124
CrossRef
Pubmed
Google scholar
|
[80] |
Ye S J, Zeng G M, Wu H P, Zhang C, Liang J, Dai J, Liu Z F, Xiong W P, Wan J, Xu P, Cheng M. Co-occurrence and interactions of pollutants, and their impacts on soil remediation—a review. Critical Reviews in Environmental Science and Technology, 2017, 47(16): 1528–1553
CrossRef
Google scholar
|
[81] |
Weller D M, Raaijmakers J M, Gardener B B M, Thomashow L S. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 2002, 40(1): 309–348
CrossRef
Pubmed
Google scholar
|
[82] |
Ren L X, Su S M, Yang X M, Xu Y C, Huang Q W, Shen Q R. Intercropping with aerobic rice suppressed Fusarium wilt in watermelon. Soil Biology & Biochemistry, 2008, 40(3): 834–844
CrossRef
Google scholar
|
[83] |
Bonanomi G, Lorito M, Vinale F, Woo S L. Organic amendments, beneficial microbes, and soil microbiota: toward a unified framework for disease suppression. Annual Review of Phytopathology, 2018, 56(1): 1–20
CrossRef
Pubmed
Google scholar
|
[84] |
Garbeva P, van Veen J A, van Elsas J D. Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annual Review of Phytopathology, 2004, 42(1): 243–270
CrossRef
Pubmed
Google scholar
|
[85] |
Conrath U. Systemic acquired resistance. Plant Signaling & Behavior, 2006, 1(4): 179–184
CrossRef
Pubmed
Google scholar
|
[86] |
Pieterse C M J, Zamioudis C, Berendsen R L, Weller D M, Van Wees S C M, Bakker P A H M. Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology, 2014, 52(1): 347–375
CrossRef
Pubmed
Google scholar
|
[87] |
Van der Ent S, Van Wees S C M, Pieterse C M J. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry, 2009, 70(13–14): 1581–1588
CrossRef
Pubmed
Google scholar
|
[88] |
Yuan J, Zhao J, Wen T, Zhao M, Li R, Goossens P, Huang Q, Bai Y, Vivanco J M, Kowalchuk G A, Berendsen R L, Shen Q. Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome, 2018, 6(1): 156
CrossRef
Pubmed
Google scholar
|
[89] |
Berendsen R L, Vismans G, Yu K, Song Y, de Jonge R, Burgman W P, Burmølle M, Herschend J, Bakker P A H M, Pieterse C M J. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME Journal, 2018, 12(6): 1496–1507
CrossRef
Pubmed
Google scholar
|
[90] |
Sanguin H, Sarniguet A, Gazengel K, Moënne-Loccoz Y, Grundmann G L. Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytologist, 2009, 184(3): 694–707
CrossRef
Pubmed
Google scholar
|
[91] |
Cha J Y, Han S, Hong H J, Cho H, Kim D, Kwon Y, Kwon S K, Crüsemann M, Bok Lee Y, Kim J F, Giaever G, Nislow C, Moore B S, Thomashow L S, Weller D M, Kwak Y S. Microbial and biochemical basis of a Fusarium wilt-suppressive soil. ISME Journal, 2016, 10(1): 119–129
CrossRef
Pubmed
Google scholar
|
[92] |
Lapsansky E R, Milroy A M, Andales M J, Vivanco J M. Soil memory as a potential mechanism for encouraging sustainable plant health and productivity. Current Opinion in Biotechnology, 2016, 38: 137–142
CrossRef
Pubmed
Google scholar
|
[93] |
Hartmann M, Frey B, Mayer J, Mäder P, Widmer F. Distinct soil microbial diversity under long-term organic and conventional farming. ISME Journal, 2015, 9(5): 1177–1194
CrossRef
Pubmed
Google scholar
|
[94] |
Jiao S, Chen W, Wang J, Du N, Li Q, Wei G. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome, 2018, 6(1): 146
CrossRef
Pubmed
Google scholar
|
[95] |
Teng Y, Chen W. Soil microbiomes: a promising strategy for contaminated soil remediation: a review. Pedosphere, 2019, 29(3): 283–297
CrossRef
Google scholar
|
[96] |
Wang X, Wei Z, Yang K, Wang J, Jousset A, Xu Y, Shen Q, Friman V P. Phage combination therapies for bacterial wilt disease in tomato. Nature Biotechnology, 2019, 37(12): 1513–1520
CrossRef
Pubmed
Google scholar
|
[97] |
Witek K, Jupe F, Witek A I, Baker D, Clark M D, Jones J D G. Accelerated cloning of a potato late blight-resistance gene using RenSeq and SMRT sequencing. Nature Biotechnology, 2016, 34(6): 656–660
CrossRef
Pubmed
Google scholar
|
[98] |
Kwak M J, Kong H G, Choi K, Kwon S K, Song J Y, Lee J, Lee P A, Choi S Y, Seo M, Lee H J, Jung E J, Park H, Roy N, Kim H, Lee M M, Rubin E M, Lee S W, Kim J F. Author Correction: rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nature Biotechnology, 2018, 36(11): 1117
CrossRef
Pubmed
Google scholar
|
[99] |
Wei Z, Jousset A. Plant breeding goes microbial. Trends in Plant Science, 2017, 22(7): 555–558
CrossRef
Pubmed
Google scholar
|
[100] |
Mendes L W, Raaijmakers J M, de Hollander M, Mendes R, Tsai S M. Influence of resistance breeding in common bean on rhizosphere microbiome composition and function. ISME Journal, 2018, 12(1): 212–224
CrossRef
Pubmed
Google scholar
|
[101] |
Mendes L W, Mendes R, Raaijmakers J M, Tsai S M. Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean. ISME Journal, 2018, 12(12): 3038–3042
CrossRef
Pubmed
Google scholar
|
[102] |
Xue C, Shen Z Z, Hao Y W, Yu S T, Li Y C, Huang W J, Chong Y, Ran W, Li R, Shen Q R. Fumigation coupled with bio-organic fertilizer for the suppression of watermelon Fusarium wilt disease re-shapes the soil microbiome. Applied Soil Ecology, 2019, 140: 49–56
CrossRef
Google scholar
|
[103] |
Larkin R P, Griffin T S. Control of soilborne potato diseases using Brassica green manures. Crop Protection, 2007, 26(7): 1067–1077
CrossRef
Google scholar
|
[104] |
Shen G, Zhang S, Liu X, Jiang Q, Ding W. Soil acidification amendments change the rhizosphere bacterial community of tobacco in a bacterial wilt affected field. Applied Microbiology and Biotechnology, 2018, 102(22): 9781–9791
CrossRef
Pubmed
Google scholar
|
[105] |
Adam E, Groenenboom A E, Kurm V, Rajewska M, Schmidt R, Tyc O, Weidner S, Berg G, de Boer W, Falcão Salles J. Controlling the microbiome: microhabitat adjustments for successful biocontrol strategies in soil and human gut. Frontiers in Microbiology, 2016, 7: 1079
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |