Legacy of land use history determines reprogramming of plant physiology by soil microbiome.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
03 2019
03 2019
Historique:
received:
02
04
2018
accepted:
04
10
2018
revised:
25
08
2018
pubmed:
29
10
2018
medline:
7
8
2019
entrez:
29
10
2018
Statut:
ppublish
Résumé
Microorganisms associated with roots are thought to be part of the so-called extended plant phenotypes with roles in the acquisition of nutrients, production of growth hormones, and defense against diseases. Since the crops selectively enrich most rhizosphere microbes out of the bulk soil, we hypothesized that changes in the composition of bulk soil communities caused by agricultural management affect the extended plant phenotype. In the current study, we performed shotgun metagenome sequencing of the rhizosphere microbiome of the peanut (Arachis hypogaea) and metatranscriptome analysis of the roots of peanut plants grown in the soil with different management histories, peanut monocropping and crop rotation. We found that the past planting record had a significant effect on the assembly of the microbial community in the peanut rhizosphere, indicating a soil memory effect. Monocropping resulted in a reduction of the rhizosphere microbial diversity, an enrichment of several rare species, and a reduced representation of traits related to plant performance, such as nutrients metabolism and phytohormone biosynthesis. Furthermore, peanut plants in monocropped soil exhibited a significant reduction in growth coinciding with a down-regulation of genes related to hormone production, mainly auxin and cytokinin, and up-regulation of genes related to the abscisic acid, salicylic acid, jasmonic acid, and ethylene pathways. These findings suggest that land use history affects crop rhizosphere microbiomes and plant physiology.
Identifiants
pubmed: 30368524
doi: 10.1038/s41396-018-0300-0
pii: 10.1038/s41396-018-0300-0
pmc: PMC6461838
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Pagination
738-751Références
Castrillo G, Teixeira P, Paredes SH, Law TF, De Lorenzo L, Feltcher ME, et al. Root microbiota drive direct integration of phosphate stress and immunity. Nature. 2017;543:513–8.
pubmed: 28297714
pmcid: 5364063
Fitzpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MTJ. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc Natl Acad Sci USA. 2018;22:E1157–65.
Raaijmakers JM, Mazzola M. Soil immune responses. Science. 2016;352:1392–3.
pubmed: 27313024
Wagg C, Jansa J, Schmid B, van der Heijden MG. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett. 2011;14:1001–9.
pubmed: 21790936
Garbeva P, Van Elsas JD, Van Veen JA. Rhizosphere microbial community and its response to plant species and soil history. Plant Soil. 2008;302:19–32.
Griffiths BS, Caul S, Thompson J, Birch ANE, Cortet J, Andersen MN, et al. Microbial and microfaunal community structure in cropping systems with genetically modified plants. Pedobiologia. 2007;51:195–206.
Lin Q, Zhao HM, Chen YX. Effects of 2,4-dichlorophenol, pentachlorophenol and vegetation on microbial characteristics in a heavy metal polluted soil. J Environ Sci Health B. 2007;42:551–7.
pubmed: 17562463
Schlemper TR, Leite MFA, Lucheta AR, Shimels M, Bouwmeester HJ, van Veen JA, et al. Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol Ecol. 2017;93:1–11.
Sessitsch A, Gyamfi S, Tscherko D, Gerzabek MH, Kandeler E. Activity of microorganisms in the rhizosphere of herbicide treated and untreated transgenic glufosinate-tolerant and wildtype oilseed rape grown in containment. Plant Soil. 2005;266:105–16.
Lau JA, Lennon JT. Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytol. 2011;192:215–24.
pubmed: 21658184
Smith CR, Blair PL, Boyd C, Cody B, Hazel A, Hedrick A, et al. Microbial community responses to soil tillage and crop rotation in a corn/soybean agroecosystem. Ecol Evol. 2016;6:8075–84.
pubmed: 27878079
pmcid: 5108259
Zuppinger-Dingley D, Schmid B, Petermann JS, Yadav V, Deyn GBD, Dan FBF. Selection for niche differentiation in plant communities increases biodiversity effects. Nature. 2014;515:108–11.
pubmed: 25317555
Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT. Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci USA. 2015;112:E5013–20.
pubmed: 26305938
Expósito RG, Bruijn ID, Postma J, Raaijmakers JM. Current insights into the role of rhizosphere bacteria in disease suppressive soils. Front Microbiol. 2017;8:2529.
Janvier C, Villeneuve F, Alabouvette C, Edelhermann V, Mateille T, Steinberg C. Soil health through soil disease suppression: which strategy from descriptors to indicators? Soil Biol Biochem. 2007;39:1–23.
Marschner H (eds). Mineral nutrition of higher plants, 2nd edn. Academic Press: London, UK, 1995.
Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM. Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil. 2012;360:1–13.
Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.
pubmed: 22564542
Chaparro JM, Badri DV, Vivanco JM. Rhizosphere microbiome assemblage is affected by plant development. ISME J. 2014;8:790–803.
pubmed: 24196324
Niu B, Paulson JN, Zheng X, Kolter R. Simplified and representative bacterial community of maize roots. Proc Natl Acad Sci USA. 2017;114:E2450–59.
pubmed: 28275097
Bulgarelli D, Garridooter R, Münch PC, Weiman A, Dröge J, Pan Y, et al. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe. 2015;17:392–403.
pubmed: 25732064
pmcid: 4362959
Dawson W, Hör J, Egert M, Kleunen MV, Pester M. A small number of low-abundance bacteria dominate plant species-specific responses during rhizosphere colonization. Front Microbiol. 2017;8:975.
pubmed: 28611765
pmcid: 5447024
Zhou X, Wu F. p-coumaric acid influenced cucumber rhizosphere soil microbial communities and the growth of Fusarium oxysporum f.sp. cucumerinum owen. PLoS One. 2012;7:e48288.
pubmed: 23118972
pmcid: 3484048
Hernández M, Dumont MG, Yuan Q, Conrad R. Different bacterial populations associated with the roots and rhizosphere of rice incorporate plant-derived carbon. Appl Environ Microbiol. 2015; 81, 2244–2253.
pubmed: 25616793
pmcid: 4345361
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA. 2015;112:911–20.
Vandenkoornhuyse P, Quaiser A, Duhamel M, Van AL, Dufresne A. The importance of the microbiome of the plant holobiont. New Phytol. 2015;206:1196–206.
pubmed: 25655016
Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM. How plants communicate using the underground information superhighway. Trends Plant Sci. 2004;9:26–32.
pubmed: 14729216
van Loon LC. Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol. 2007;119:243–54.
Bordiec S, Paquis S, Lacroix H, Dhondt S, Ait BE, Kauffmann S, et al. Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain psjn and the non-host bacterium pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot. 2011;62:595–603.
pubmed: 20881012
Poupin MJ, Timmermann T, Vega A, Zuñiga A, González B. Effects of the plant growth-promoting bacterium Burkholderia phytofirmans psjn throughout the life cycle of Arabidopsis thaliana. PLoS One. 2013;8:e69435.
pubmed: 23869243
pmcid: 3711820
Armada E, Leite MFA, Medina A, Azcón R, Kuramae EE. Native bacteria promote plant growth under drought stress condition without impacting the rhizomicrobiome. FEMS Microbiol Ecol. 2018;94:fiy092.
Li XG, Ding CF, Hua K, Zhang TL, Zhang YN, Zhao L, et al. Soil sickness of peanuts is attributable to modifications in soil microbes induced by peanut root exudates rather than to direct allelopathy. Soil Biol Biochem. 2014;78:149–59.
FAO. World reference base for soil resources (WRB). World Soil Resources Reports. 1998; 84.
Hol WHG, Garbeva P, Hordijk CA, Hundscheid MPJ, Klein Gunnewiek PJA, van Agtmaal M, et al. Non-random species loss in bacterial communities reduces antifungal volatile production. Ecology. 2015;96:2042–8.
pubmed: 26405729
de Boer W, Hundscheid MP, Klein Gunnewiek PJA, de Ridder-Duine AS, Thion C, van Veen JA, et al. Antifungal rhizosphere bacteria can increase as response to the presence of saprotrophic fungi. PLoS One. 2015;10:e0137988.
pubmed: 26393509
pmcid: 4578881
Li XG, Liu B, Sondre H, Liu DD, Han ZM, Zhou KX, et al. The effect of root exudates from two transgenic insect-resistant cotton lines on the growth of Fusarium oxysporum. Transgenic Res. 2009;18:757–67.
pubmed: 19396562
Luo C, Rodriguezr LM, Johnston ER, Wu L, Cheng L, Xue K, et al. Soil microbial community responses to a decade of warming as revealed by comparative metagenomics. Appl Environ Microbiol. 2014;80:1777–86.
pubmed: 24375144
pmcid: 3957593
Rho M, Tang H, Ye Y. FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res. 2010;38:e191.
pubmed: 20805240
pmcid: 2978382
Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, et al. The metagenomics rast server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics. 2008;9:386.
pubmed: 18803844
pmcid: 2563014
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5:621–8.
pubmed: 18516045
Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123–4.
pubmed: 25061070
pmcid: 4609014
Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14:927–30.
Hammer Ø, Harper DAT, Ryan PD. Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001;4:9.
Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.
Lynch MD, Neufeld JD. Ecology and exploration of the rare biosphere. Nat Rev Microbiol. 2015;13:217–29.
pubmed: 25730701
Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev. 2007;31:425–48.
pubmed: 17509086
Alazem M, Lin NS. Roles of plant hormones in the regulation of host–virus interactions. Mol Plant Pathol. 2015;16:529–40.
pubmed: 25220680
Vleesschauwer DD, Gheysen G, Höfte M. Hormone defense networking in rice: tales from a different world. Trends Plant Sci. 2013;18:555–65.
pubmed: 23910453
Mendes R, Raaijmakers JM. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science. 2011;332:1097–100.
pubmed: 21551032
Philippot L, Raaijmakers JM, Lemanceau P, Putten WHVD. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol. 2013;11:789–99.
pubmed: 24056930
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM. Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils. 2012;48:489–99.
Hartmann M, Frey B, Mayer J, Mäder P, Widmer F. Distinct soil microbial diversity under long-term organic and conventional farming. ISME J. 2015;9:1177–94.
pubmed: 25350160
Sugiyama A, Vivanco JM, Jayanty SS, Manter DK. Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms. Plant Dis. 2010;94:1329–35.
pubmed: 30743621
Xu L, Ravnskov S, Larsen J, Nilsson RH, Nicolaisen M. Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Biol Biochem. 2012;46:26–32.
Lennon JT, Jones SE. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol. 2011;9:119–30.
pubmed: 21233850
van Passel MW, Kant R, Palva A, Copeland A, Lucas S, Lapidus A, et al. Genome sequence of the verrucomicrobium Opitutus terrae PB90-1, an abundant inhabitant of rice paddy soil ecosystems. J Bacteriol. 2011;193:2367–8.
pubmed: 21398538
pmcid: 3133072
Zuñiga A, Poupin MJ, Donoso R, Ledger T, Guiliani N, Gutierrez RA, et al. Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans psjn. Mol Plant Microbe Interact. 2013;26:546–53.
pubmed: 23301615
Cottee-Jones HEW, Whittaker RJ. The keystone species concept: a critical appraisal. Front Biogeogr. 2012;4:117–27.
Wei Z, Yang T, Friman VP, Xu Y, Shen Q, Jousset A. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun. 2015;6:8413.
pubmed: 26400552
pmcid: 4598729
Jousset A, Becker J, Chatterjee S, Karlovsky P, Scheu S, Eisenhauer N. Biodiversity and species identity shape the antifungal activity of bacterial communities. Ecology. 2016;95:1184–1190.
pubmed: 25000750
Centler F, Thullner M. Chemotactic preferences govern competition and pattern formation in simulated two-strain microbial communities. Front Microbiol. 2015;6:40.
pubmed: 25699031
pmcid: 4313714
Fibachpaldi S, Burdman S, Okon Y. Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense. FEMS Microbiol Lett. 2012;326:99–108.
Taghavi S, Lelie DVD, Hoffman A, Zhang YB, Walla MD, Vangronsveld J, et al. Genome sequence of the plant growth promoting endophytic bacterium, Enterobacter sp. 638. PLoS Genet. 2010;6:e1000943.
pubmed: 20485560
pmcid: 2869309
Mendes LW, Kuramae EE, Navarrete AA, Van Veen JA, Tsai SM. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J. 2014;8:1577–87.
pubmed: 24553468
pmcid: 4817605
Ofek-Lalzar M, Sela N, Goldmanvoronov M, Green SJ, Hadar Y, Minz D. Niche and host-associated functional signatures of the root surface microbiome. Nat Commun. 2014;5:4950.
pubmed: 25232638
Pankebuisse K, Poole AC, Goodrich JK, Ley RE, Kaokniffin J. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J. 2014;9:980.
Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, Smet ID, et al. Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 2013;18:450–8.
pubmed: 23701908
Overvoorde P, Fukaki H, Beeckman T. Auxin control of root development. Cold Spring Harb Perspect Biol. 2010;2:a001537.
pubmed: 20516130
pmcid: 2869515
Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, et al. Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA. 2003;100:4927–32.
pubmed: 12684534
Huang LF, Song LX, Xia XJ, Mao WH, Shi K, Zhou YH, et al. Plant-soil feedbacks and soil sickness: from mechanisms to application in agriculture. J Chem Ecol. 2013;39:232–42.
pubmed: 23385367
Perry LG, Thelen GC, Ridenour WM, Callaway RM, Paschke MW, Vivanco JM. Concentrations of the allelochemical (±)-catechin in Centaurea maculosa soils. J Chem Ecol. 2007;12:2337–44.
Blair AC, Nissen SJ, Brunk GR, Hufbauer RA. A lack of evidence for an ecological role of the putative allelochemical (6)-catechin in spotted knap weed invasion success. J Chem Ecol. 2006;32:2327–31.
pubmed: 16955253
Deng Y, Yao J, Wang X, Guo H, Duan D. Transcriptome sequencing and comparative analysis of Saccharina japonica (Laminariales, Phaeophyceae) under blue light induction. PLoS One. 2012;7:e39704.
pubmed: 22761876
pmcid: 3384632
Son KH, Oh MM. Leaf shape, growth, and antioxidant phenolic compounds of two lettuce cultivars grown under various combinations of blue and red light-emitting diodes. HortScience. 2013;48:988–95.
Ferreyra FML, Rius SP, Paula C. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci. 2012;3:1–15.
Yadav V, Mallappa C, Gangappa SN, Bhatia S, Chattopadhyay S. A basic helix-loop-helix transcription factor in Arabidopsis, myc2, acts as a repressor of blue light-mediated photomorphogenic growth. Plant Cell. 2005;17:1953–66.
pubmed: 15923349
pmcid: 1167544
Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR. Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci. 2017;8:475.
pubmed: 28421102
pmcid: 5378820
Vicente MRS, Plasencia J. Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot. 2011;62:3321–3338.
Peng Z, Liu F, Wang L, Zhou H, Paudel D, Tan L, et al. Transcriptome profiles reveal gene regulation of peanut (Arachis hypogaea L.) nodulation. Sci Rep. 2017;7:40066.
pubmed: 28059169
pmcid: 5216375
de Billy F, Grosjean C, May S, Bennett M, Cullimore JV. Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Interact. 2001;14:267–77.
Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J. 1998;14:23–34.
pubmed: 15494052
Takanashi K, Sugiyama A, Yazaki K. Auxin distribution and lenticel formation in determinate nodule of Lotus japonicus. Plant Signal Behav. 2011;6:1405–7.
pubmed: 22019641
pmcid: 3258077
Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, et al. The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell. 2014;26:4680–701.
pubmed: 25527707
pmcid: 4311213
Penmetsa RV, Uribe P, Anderson J, Lichtenzveig J, Gish JC, Nam YW, et al. The Medicago truncatula of the Arabidopsis EIN2 gene, sickle, is a negative regulator of symbiotic and pathogenic microbial interactions. Plant J. 2008;55:580–95.
pubmed: 18435823
Stacey MG, Osawa H, Patel A, Gassmann W, Stacey G. Expression analyses of Arabidopsis oligopeptide transporters during seed germination, vegetative growth and reproduction. Planta. 2006;223:291–305.
pubmed: 16151844
Sun J, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM. Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J. 2006;46:961–70.
pubmed: 16805730
van Spronsen PC, Tak T, Rood AM, van Brussel AA, Kijne JW, Boot KJ. Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation. Mol Plant Microbe Interact. 2003;16:83–91.
pubmed: 12580285
Zhang W, Sun K, Shi RH, Yuan J, Wang XJ, Dai CC. Auxin signalling of Arachis hypogaea activated by colonization of mutualistic fungus Phomopsis liquidambari enhances nodulation and N
Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, et al. Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol. 2008;179:209–23.
pubmed: 18422893
Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, et al. Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol. 2012;12:3.
pubmed: 22235902
pmcid: 3268082
Baier MC, Barsch A, Küster H, Hohnjec N. Antisense repression of the Medicago truncatula nodule‐enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol. 2007;145:1600–18.
pubmed: 17951459
pmcid: 2151687
Martin F, Kamoun S, editors. Effectors in plant–microbe interactions. Wiley-Blackwell: Oxford, UK, 2012.
Newman MA, Sundelin T, Nielsen JT, Erbs G. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci. 2013;4:139.
pubmed: 23720666
pmcid: 3655273
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature. 2012;488:91–5.
pubmed: 22859207