Abstract
Aims
Wheat (Triticum aestivum L.) cultivars vary in their resistance to Fusarium head blight (FHB), while it is poorly understood how different cultivars influence FHB-causing Fusarium graminearum abundance in rhizosphere soil.
Methods
A field experiment was conducted to investigate the influence of three wheat cultivars on FHB index, rhizosphere soil F. graminearum abundance, chemical properties, and microbial community composition and metabolic profiles. The cultivars were Sumai3 (SM), Yangmai13 (YM), and Annong8455 (AN), representing high, intermediate, and low resistance to FHB, respectively.
Results
Both wheat FHB index and rhizosphere F. graminearum abundance were ranked as SM < YM < AN (p < 0.05). Wheat cultivar influenced community composition with a higher fungal Shannon index in the SM and YM rhizosphere than in the AN rhizosphere. The relative abundances of Arthrobacter, Pseudomonas, Acremonium and Guehomyces that contain microbes with potential to have beneficial effects on pathogen suppression were higher in the rhizosphere soil of SM, relative to AN. Microorganisms in the SM rhizosphere used less carboxylic acids and phenolic acids but more amino acids than those in the AN rhizosphere. Rhizosphere F. graminearum abundance was positively correlated to utilization of carboxylic acids, but negatively correlated with NH4+-N content, fungal Shannon index, and relative abundance of Arthrobacter, Pseudomonas, Acremonium and Guehomyces.
Conclusions
The different F. graminearum abundance in rhizosphere soil of wheat cultivars with different resistance to FHB may be associated with the changes in rhizosphere soil chemical properties and microbial community composition and function.
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References
An MJ, Zhou XG, Wu FZ, Ma YF, Yang P (2011) Rhizosphere soil microorganism populations and community structures of different watermelon cultivars with differing resistance to Fusarium oxysporum f. sp niveum. Can J Microbiol 57:355–365. https://doi.org/10.1139/W11-015
Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98. https://doi.org/10.1016/j.tplants.2013.11.006
Bai GH, Shaner G (2004) Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol 42:135–161. https://doi.org/10.1146/annurev.phyto.42.040803.140340
Bani M, Cimmino A, Evidente A, Rubiales D, Rispail N (2018) Pisatin involvement in the variation of inhibition of Fusarium oxysporum f. sp pisi spore germination by root exudates of Pisum spp. germplasm. Plant Pathol 67:1046–1054. https://doi.org/10.1111/ppa.12813
Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru margin subseafloor biosphere show a genetically distinct environment. P Natl Acad Sci USA 105:10583–10588. https://doi.org/10.1073/pnas.0709942105
Cao ZQ, Fan TF, Bi YM, Tian GL, Zhang LS (2016) Potassium deficiency and root exudates reduce root growth and increase Fusarium oxysporum growth and disease incidence in continuously cultivated strawberry. New Zeal J Crop Hort 44:58–68. https://doi.org/10.1080/01140671.2016.1146306
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chakraborty S, Obanor F, Westecott R, Abeywickrama K (2010) Wheat crown rot pathogens Fusarium graminearum and F. pseudograminearum lack specialization. Phytopathology 100:1057–1065. https://doi.org/10.1094/Phyto-01-10-0007
Cobo-Díaz JF, Baroncelli R, Le Floch G, Picot A (2019) Combined metabarcoding and co-occurrence network analysis to profile the bacterial, fungal and Fusarium communities and their interactions in maize stalks. Front Microbiol 10:261. https://doi.org/10.3389/fmicb.2019.00261
Corneo PE, Suenaga H, Kertesz MA, Dijkstra FA (2016) Effect of twenty four wheat genotypes on soil biochemical and microbial properties. Plant Soil 404:141–155. https://doi.org/10.1007/s11104-016-2833-1
De Vrieze M, Pandey P, Bucheli TD, Varadarajan AR, Ahrens CH, Weisskopf L, Bailly A (2015) Volatile organic compounds from native potato-associated Pseudomonas as potential anti-oomycete agents. Front Microbiol 6:1295. https://doi.org/10.3389/fmicb.2015.01295
Donn S, Kirkegaard JA, Perera G, Richardson AE, Watt M (2015) Evolution of bacterial communities in the wheat crop rhizosphere. Environ Microbiol 17:610–621. https://doi.org/10.1111/1462-2920.12452
Dyer RB, Kendra DF, Brown DW (2006) Real-time PCR assay to quantify Fusarium graminearum wild-type and recombinant mutant DNA in plant material. J Microbiol Meth 67:534–542. https://doi.org/10.1016/j.mimet.2006.05.011
Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microb 57:2351–2359
Gu WJ, Lu YS, Tan ZY, Xu PZ, Xie KZ, Li X, Sun LL (2017) Fungi diversity from different depths and times in chicken manure waste static aerobic composting. Bioresour Technol 239:447–453. https://doi.org/10.1016/j.biortech.2017.04.047
Han YS, Xu LX, Liu LQ, Yi M, Guo EH, Zhang AY, Yi HL (2017) Illumina sequencing reveals a rhizosphere bacterial community associated with foxtail millet smut disease suppression. Plant Soil 410:411–421. https://doi.org/10.1007/s11104-016-3042-7
Hu WA, Gao QX, Hamada MS, Dawood DH, Zheng JW, Chen Y, Ma ZH (2014) Potential of Pseudomonas chlororaphis subsp aurantiaca strain Pcho10 as a biocontrol agent against Fusarium graminearum. Phytopathology 104:1289–1297. https://doi.org/10.1094/Phyto-02-14-0049-R
Huang XQ, Zhou X, Zhang JB, Cai ZC (2019) Highly connected taxa located in the microbial network are prevalent in the rhizosphere soil of healthy plant. Biol Fert Soils 55:299–312. https://doi.org/10.1007/s00374-019-01350-1
İnceoğlu O, Salles JF, van Overbeek L, van Elsas JD (2010) Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl Environ Microb 76:3675–3684. https://doi.org/10.1128/aem.00040-10
Kaiserer L, Oberparleiter C, Weiler-Gorz R, Burgstaller W, Leiter E, Marx F (2003) Characterization of the Penicillium chrysogenum antifungal protein PAF. Arch Microbiol 180:204–210. https://doi.org/10.1007/s00203-003-0578-8
Kumar A, Karre S, Dhokane D, Kage U, Hukkeri S, Kushalappa AC (2015) Real-time quantitative PCR based method for the quantification of fungal biomass to discriminate quantitative resistance in barley and wheat genotypes to fusarium head blight. J Cereal Sci 64:16–22. https://doi.org/10.1016/j.jcs.2015.04.005
Kwak MJ, Kong HG, Choi K, Kwon SK, Song JY, Lee J, Lee PA, Choi SY, Seo M, Lee HJ, Jung EJ, Park H, Roy N, Kim H, Lee MM, Rubin EM, Lee SW, Kim JF (2018) Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol 36:1100–1109. https://doi.org/10.1038/nbt1118-1117
Li XG, Zhang TL, Wang XX, Hua K, Zhao L, Han ZM (2013) The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. Int J Biol Sci 9:164–173. https://doi.org/10.7150/ijbs.5579
Li ZQ, Zhao BZ, Hao XY, Zhang JB (2017) Effects of residue incorporation and plant growth on soil labile organic carbon and microbial function and community composition under two soil moisture levels. Environ Sci Pollut Res 24:18849–18859. https://doi.org/10.1007/s11356-017-9529-9
Liu XY, Jin JY, He P, Liu HL, Li WJ (2007) Preliminary study on the relation between potassium chloride suppressing corn stalk rot and soil microorganism characteristics (in Chinese). Plant Nutri Fert Sci 13:279–285
Liu X, Zhang JL, Gu TY, Zhang WM, Shen QR, Yin SX, Qiu HZ (2014) Microbial community diversities and taxa abundances in soils along a seven-year gradient of potato monoculture using high throughput pyrosequencing approach. PLoS One 9:86610. https://doi.org/10.1371/journal.pone.0086610
Liu LJ, Sun CL, Liu XX, He XL, Liu M, Wu H, Tang CX, Jin CW, Zhang YS (2016) Effect of calcium cyanamide, ammonium bicarbonate and lime mixture, and ammonia water on survival of Ralstonia solanacearum and microbial community. Sci Rep 6:19037. https://doi.org/10.1038/srep19037
Lu RK (1999) Methods of analysis on soil agricultural and chemical properties (in Chinese). China Agricultural and Scientific Technology Press, Beijing
Mahoney AK, Yin CT, Hulbert SH (2017) Community structure, species variation, and potential functions of rhizosphere-associated bacteria of different winter wheat (Triticum aestivum) cultivars. Front Plant Sci 8:132. https://doi.org/10.3389/fpls.2017.00132
Manici LM, Caputo F (2009) Fungal community diversity and soil health in intensive potato cropping systems of the East Po valley, northern Italy. Ann Appl Biol 155:245–258. https://doi.org/10.1111/j.1744-7348.2009.00335.x
Martinez A, Cavello I, Garmendia G, Rufo C, Cavalitto S, Vero S (2016) Yeasts from sub-Antarctic region: biodiversity, enzymatic activities and their potential as oleaginous microorganisms. Extremophiles 20:759–769. https://doi.org/10.1007/s00792-016-0865-3
Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009) Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J 3:977–991. https://doi.org/10.1038/ismej.2009.33
McCallum BD, Tekauz A, Gilbert J (2004) Reaction of a diverse collection of barley lines to Fusarium head blight. Plant Dis 88:167–174. https://doi.org/10.1094/pdis.2004.88.2.167
Mendes LW, Raaijmakers JM, de Hollander M, Mendes R, Tsai SM (2018a) Influence of resistance breeding in common bean on rhizosphere microbiome composition and function. ISME J 12:212–224. https://doi.org/10.1038/ismej.2017.158
Mendes LW, Mendes R, Raaijmakers JM, Tsai SM (2018b) Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean. ISME J 12:3038–3042. https://doi.org/10.1038/s41396-018-0234-6
Mesterhazy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386. https://doi.org/10.1111/j.1439-0523.1995.tb00816.x
Mestre MC, Fontenla S, Bruzone MC, Fernandez NV, Dames J (2016) Detection of plant growth enhancing features in psychrotolerant yeasts from Patagonia (Argentina). J Basic Microb 56:1098–1106. https://doi.org/10.1002/jobm.201500728
Michel VV, Mew TW (1998) Effect of a soil amendment on the survival of Ralstonia solanacearum in different soils. Phytopathology 88:300–305. https://doi.org/10.1094/PHYTO.1998.88.4.300
Mousa WK, Shearer C, Limay-Rios V, Ettinger CL, Eisen JA, Raizada MN (2016) Root-hair endophyte stacking in finger millet creates a physicochemical barrier to trap the fungal pathogen Fusarium graminearum. Nat Microbiol 1:16167. https://doi.org/10.1038/Nmicrobiol.2016.167
Müller T, Behrendt U, Ruppel S, von der Waydbrink G, Müller MEH (2016) Fluorescent pseudomonads in the phyllosphere of wheat: potential antagonists against fungal phytopathogens. Curr Microbiol 72:383–389. https://doi.org/10.1007/s00284-015-0966-8
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology package v.2.3-0
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124. https://doi.org/10.1093/bioinformatics/btu494
Paul EA (2015) Soil microbiology, ecology and biochemistry, 4th edn. Academic Press
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340
Poli A, Lazzari A, Prigione V, Voyron S, Spadaro D, Varese GC (2016) Influence of plant genotype on the cultivable fungi associated to tomato rhizosphere and roots in different soils. Fungal Biol 120:862–872. https://doi.org/10.1016/j.funbio.2016.03.008
Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci U S A 112:5013–5020. https://doi.org/10.1073/pnas.1505765112
Shah L, Ali A, Yahya M, Zhu Y, Wang S, Si H, Rahman H, Ma C (2018) Integrated control of Fusarium head blight and deoxynivalenol mycotoxin in wheat. Plant Pathol 67:532–548. https://doi.org/10.1111/ppa.12785
Shen ZZ, Penton CR, Lv N, Xue C, Yuan XF, Ruan YZ, Li R, Shen QR (2018) Banana Fusarium wilt disease incidence is influenced by shifts of soil microbial communities under different monoculture spans. Microbial Ecol 75:739–750. https://doi.org/10.1007/s00248-017-1052-5
Shen ZZ, Xue C, Penton CR, Thomashow LS, Zhang N, Wang BB, Ruan YZ, Li R, Shen QR (2019) Suppression of banana Panama disease induced by soil microbiome reconstruction through an integrated agricultural strategy. Soil Biol Biochem 128:164–174. https://doi.org/10.1016/j.soilbio.2018.10.016
Shi WC, Li MC, Wei GS, Tian RM, Li CP, Wang B, Lin RS, Shi CY, Chi XL, Zhou B, Gao Z (2019) The occurrence of potato common scab correlates with the community composition and function of the geocaulosphere soil microbiome. Microbiome 7:14. https://doi.org/10.1186/s40168-019-0629-2
Siegel-Hertz K, Edel-Hermann V, Chapelle E, Terrat S, Raaijmakers JM, Steinberg C (2018) Comparative microbiome analysis of a Fusarium wilt suppressive soil and a Fusarium wilt conducive soil from the Châteaurenard region. Front Microbiol 9:568. https://doi.org/10.3389/fmicb.2018.00568
Sorahinobar M, Niknam V, Ebrahimzadeh H, Soltanloo H, Behmanesh M, Enferadi ST (2016) Central role of salicylic acid in resistance of wheat against Fusarium graminearum. J Plant Growth Regul 35:477–491. https://doi.org/10.1007/s00344-015-9554-1
Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448. https://doi.org/10.1016/j.pbi.2008.05.005
Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK, Suman A (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65:1885–1899. https://doi.org/10.1007/s13213-014-1027-4
Wang LP, Li Q, Liu ZY, Surendra A, Pan YL, Li YF, Zaharia LI, Ouellet T, Fobert PR (2018) Integrated transcriptome and hormone profiling highlight the role of multiple phytohormone pathways in wheat resistance against fusarium head blight. PLoS One 13:e0207036. https://doi.org/10.1371/journal.pone.0207036
Wicklow DT, Poling SM (2009) Antimicrobial activity of pyrrocidines from Acremonium zeae against endophytes and pathogens of maize. Phytopathology 99:109–115. https://doi.org/10.1094/Phyto-99-1-0109
Wu HS, Liu DY, Ling N, Bao W, Ying RR, Shen QR (2009) Influence of root exudates of watermelon on Fusarium oxysporum f. sp niveum. Soil Sci Soc Am J 73:1150–1156. https://doi.org/10.2136/sssaj2008.0266
Wu K, Yuan SF, Xun GH, Shi W, Pan B, Guan HL, Shen B, Shen QR (2015) Root exudates from two tobacco cultivars affect colonization of Ralstonia solanacearum and the disease index. Eur J Plant Pathol 141:667–677. https://doi.org/10.1007/s10658-014-0569-4
Xiong W, Zhao QY, Zhao J, Xun WB, Li R, Zhang RF, Wu HS, Shen QR (2015) Different continuous cropping spans significantly affect microbial community membership and structure in a vanilla-grown soil as revealed by deep pyrosequencing. Microbial Ecol 70:209–218. https://doi.org/10.1007/s00248-014-0516-0
Xiong W, Li R, Ren Y, Liu C, Zhao QY, Wu HS, Jousset A, Shen QR (2017) Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem 107:198–207. https://doi.org/10.1016/j.soilbio.2017.01.010
Zhang L, Khabbaz SE, Wang A, Li H, Abbasi PA (2015) Detection and characterization of broad-spectrum antipathogen activity of novel rhizobacterial isolates and suppression of Fusarium crown and root rot disease of tomato. J Appl Microbiol 118:685–703. https://doi.org/10.1111/jam.12728
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This work was financially supported by the China Agriculture Research System (CARS-03) and National Natural Sciences Foundation of China (41977102).
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Li, Z., Ma, L., Zhang, Y. et al. Effect of wheat cultivars with different resistance to Fusarium head blight on rhizosphere Fusarium graminearum abundance and microbial community composition. Plant Soil 448, 383–397 (2020). https://doi.org/10.1007/s11104-020-04441-3
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DOI: https://doi.org/10.1007/s11104-020-04441-3