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Different toxic effects of ferulic and p-hydroxybenzoic acids on cucumber seedling growth were related to their different influences on rhizosphere microbial composition

  • Xue Jin
  • Fengzhi Wu
  • Xingang ZhouEmail author
Original Paper
  • 44 Downloads

Abstract

Rhizosphere microbial communities of cucumber seedlings treated with ferulic (FA) and p-hydroxybenzoic acids (PHBA) were analyzed by quantitative PCR and Illumina sequencing. Then, growth responses of cucumber seedlings to changes in the composition of rhizosphere microbial communities were assessed. Compared with PHBA, FA had higher inhibitory effects on cucumber seedling growth and higher stimulating effects on the pathogen Fusarium oxysporum f.sp. cucumerinum, which led to severer Fusarium wilting. Both FA and PHBA increased the abundances and changed the compositions of bacterial and fungal communities. However, bacterial and fungal community compositions differed between the treatments of FA and PHBA. Both FA- and PHBA-treated cucumber rhizosphere biota inhibited cucumber seedling growth with FA having stronger inhibitory effects. F. oxysporum f.sp. cucumerinum can utilize FA and PHBA in vitro. Overall, the higher phytotoxic effect of FA than PHBA on cucumber seedling growth was linked to their different influences on the composition of rhizosphere microbial communities, especially the stronger stimulating effect of FA than PHBA on F. oxysporum f.sp. cucumerinum.

Keywords

Cucumis sativus Phenolic acid Rhizosphere microbial communities Structure-function relationship Soil-borne pathogen 

Notes

Funding information

This work was supported by the National Key Research and Development Program (2018YFD1000800), National Natural Science Foundation of China (31772361), Natural Science Foundation of Heilongjiang Province (YQ2019C009), and China Agricultural Research System (CARS-23-B-10).

Supplementary material

374_2019_1408_MOESM1_ESM.doc (4 mb)
ESM 1 (DOC 4211 kb)

References

  1. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotech 20:642–650PubMedCrossRefGoogle Scholar
  2. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511PubMedCrossRefGoogle Scholar
  4. Bennett AJ, Bending GD, Chandler D, Hilton S, Mills P (2012) Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations. Biol Rev 87:52–71PubMedCrossRefGoogle Scholar
  5. Blum U, Staman KL, Flint LJ, Shaffer SR (2000) Induction and/or selection of phenolic acid-utilizing bulk-soil and rhizosphere bacteria and their influence on phenolic acid phytotoxicity. J Chem Ecol 26:2059–2078CrossRefGoogle Scholar
  6. Brinkman EP, van der Putten WH, Bakker EJ, Verhoeven KJF (2010) Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073CrossRefGoogle Scholar
  7. Bugos RC, Sutherland JB, Adler JH (1988) Phenolic compound utilization by the soft rot fungus Lecythophora hoffmannii. Appl Environ Microbiol 54:1882–1885PubMedPubMedCentralGoogle Scholar
  8. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedPubMedCentralCrossRefGoogle Scholar
  9. Cipollini D, Rigsby CM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Ecol 38:714–727Google Scholar
  10. Crowther TW, Maynard DS, Leff JW, Oldfield EE, McCulley RL, Fierer N, Bradford MA (2014) Predicting the responsiveness of soil biodiversity to deforestation: a cross-biome study. Glob Change Biol 20:2983–2994CrossRefGoogle Scholar
  11. Delgado-Baquerizo M, Giaramida L, Reich PB, Khachane AN, Hamonts K, Edwards C, Lawton LA, Singh BK (2016) Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning. J Ecol 104:936–946CrossRefGoogle Scholar
  12. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998PubMedCrossRefGoogle Scholar
  13. Expósito RG, Postma J, Raaijmakers JM, De Bruijn I (2015) Diversity and activity of Lysobacter species from disease suppressive soils. Front Microbiol 6:1243Google Scholar
  14. Fernandez PM, Martorell MM, Blaser MG, Ruberto LAM, de Figueroa LIC, Mac Cormack W (2017) Phenol degradation and heavy metal tolerance of Antarctic yeasts. Extremophiles 21:445–457PubMedCrossRefGoogle Scholar
  15. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626PubMedPubMedCentralCrossRefGoogle Scholar
  16. Figueroa-Espinoza MC, Villeneuve P (2005) Phenolic acids enzymatic lipophilization. J Agr Food Chem 53:2779–2787CrossRefGoogle Scholar
  17. Gerig TM, Blum U (1991) Effects of mixtures of four phenolic acids on leaf area expansion of cucumber seedlings grown in Portsmouth B 1 soil materials. J Chem Ecol 17:29–40PubMedCrossRefGoogle Scholar
  18. Inderjit, Wardle W, Karban R, Callaway RM (2011) The ecosystem and evolutionary contexts of allelopathy. Trend Ecol Evolut 26:655–662CrossRefGoogle Scholar
  19. Jin X, Zhang J, Shi Y, Wu F, Zhou X (2019) Green manures of Indian mustard and wild rocket enhance cucumber resistance to Fusarium wilt through modulating rhizosphere bacterial community composition. Plant Soil 441:283–300CrossRefGoogle Scholar
  20. Kaur H, Kaur R, Kaur S, Baldwin IT, Inderjit (2009) Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PLoS One 4:e4700PubMedPubMedCentralCrossRefGoogle Scholar
  21. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiß M, Larsson KH (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277PubMedCrossRefGoogle Scholar
  22. Lanoue A, Burlat V, Henkes GJ, Koch I, Schurr U, Röse US (2010) De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. New Phytol 185:577–588PubMedCrossRefPubMedCentralGoogle Scholar
  23. Lau JA, Lennon JT (2011) Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192:215–224PubMedCrossRefPubMedCentralGoogle Scholar
  24. Liu L, Kloepper JW, Tuzun S (1995) Induction of systemic resistance in cucumber against Fusarium wilt by plant growth-promoting rhizobacteria. Phytopathology 85:695–698CrossRefGoogle Scholar
  25. Liu J, Li X, Jia Z, Zhang T, Wang X (2017) Effect of benzoic acid on soil microbial communities associated with soilborne peanut diseases. Appl Soil Ecol 110:34–42CrossRefGoogle Scholar
  26. Lowe TM, Ailloud F, Allen C (2015) Hydroxycinnamic acid degradation, a broadly conserved trait, protects Ralstonia solanacearum from chemical plant defenses and contributes to root colonization and virulence. Mol Plant Microbe Interaction 28:286–297CrossRefGoogle Scholar
  27. Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963PubMedPubMedCentralCrossRefGoogle Scholar
  28. Maijala P, Mattinen ML, Nousiainen P, Kontro J, Asikkala J, Sipila J, Viikari L (2012) Action of fungal laccases on lignin model compounds in organic solvents. J Mol Catal B-Enzym 76:59–67CrossRefGoogle Scholar
  29. Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368PubMedPubMedCentralCrossRefGoogle Scholar
  30. Michielse CB, Reijnen L, Olivain C, Alabouvette C, Rep M (2012) Degradation of aromatic compounds through the β-ketoadipate pathway is required for pathogenicity of the tomato wilt pathogen Fusarium oxysporum f. sp. lycopersici. Mol Plant Pathol 13:1089–1100PubMedPubMedCentralCrossRefGoogle Scholar
  31. Mommer L, Cotton TEA, Raaijmakers JM, Termorshuizen AJ, van Ruijven J, Hendriks M, van Rijssel SQ, van de Mortel JE, van der Paauw JW, Schijlen E, Smit-Tiekstra AE, Berendse F, de Kroon H, Dumbrell AJ (2018) Lost in diversity: the interactions between soil-borne fungi, biodiversity and plant productivity. New Phytol 218:542–553PubMedPubMedCentralCrossRefGoogle Scholar
  32. Muscolo A, Sidari M (2006) Seasonal fluctuations in soil phenolics of a coniferous forest: effects on seed germination of different coniferous species. Plant Soil 284:305–318CrossRefGoogle Scholar
  33. Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248CrossRefGoogle Scholar
  34. Patel JK, Archana G (2017) Diverse culturable diazotrophic endophytic bacteria from Poaceae plants show cross-colonization and plant growth promotion in wheat. Plant Soil 417:99–116CrossRefGoogle Scholar
  35. Piotrowski J, Morford S, Rillig M (2008) Inhibition of colonization by a native arbuscular mycorrhizal fungal community via Populus trichocarpa litter, litter extract, and soluble phenolic compounds. Soil Biol Biochem 40:709–717CrossRefGoogle Scholar
  36. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(Database issue):D590–D596PubMedGoogle Scholar
  37. Sánchez-Maldonado AF, Schieber A, Gänzle MG (2011) Structure-function relationships of the antibacterial activity of phenolic acids and their metabolism by lactic acid bacteria. J Appl Microbiol 111:1176–1184PubMedCrossRefGoogle Scholar
  38. Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fert Soils 53:485–489CrossRefGoogle Scholar
  39. Shalaby S, Horwitz BA, Larkov O (2012) Structure-activity relationships delineate how the maize pathogen Cochliobolus heterostrophus uses aromatic compounds as signals and metabolites. Mol Plant Microbe Interaction 25:931–940CrossRefGoogle Scholar
  40. Singh HP, Batish DR, Kohli RK (1999) Autotoxicity: concept, organisms and ecological significance. Crit Rev Plant Sci 18:757–772CrossRefGoogle Scholar
  41. Sulistyaningdyah WT, Ogawa J, Tanaka H, Maeda C, Shimizu S (2004) Characterization of alkaliphilic laccase activity in the culture supernatant of Myrothecium verrucaria 24G-4 in comparison with bilirubin oxidase. FEMS Microbiol Lett 230:209–214PubMedCrossRefGoogle Scholar
  42. van der Heijden MG, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310PubMedCrossRefGoogle Scholar
  43. Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fert Soils 53:479–484CrossRefGoogle Scholar
  44. Wadke N, Kandasamy D, Vogel H, Lah L, Wingfield BD, Paetz C, Wright LP, Gershenzon J, Hammerbacher A (2016) The bark-beetle-associated fungus, Endoconidiophora polonica, utilizes the phenolic defense compounds of its host as a carbon source. Plant Physiol 171:914–931PubMedPubMedCentralGoogle Scholar
  45. Xue C, Hao Y, Pu X, Penton CR, Wang Q, Zhao M, Zhang B, Ran W, Huang Q, Shen Q, Tiedje JM (2019) Effect of LSU and ITS genetic markers and reference databases on analyses of fungal communities. Biol Fert Soils 55:79–88CrossRefGoogle Scholar
  46. Zheng M, Han Y, Han H, Xu C, Zhang Z, Ma W (2019) Synergistic degradation on phenolic compounds of coal pyrolysis wastewater (CPW) by lignite activated coke-active sludge (LAC-AS) process: insights into succession of microbial community under selective pressure. Bioresour Technol 281:129–134CrossRefGoogle Scholar
  47. Zhou X, Yu G, Wu F (2012) Soil phenolics in a continuously mono-cropped cucumber (Cucumis sativus L.) system and their effects on cucumber seedling growth and soil microbial communities. Eur J Soil Sci 63:332–340CrossRefGoogle Scholar
  48. Zhou X, Liu J, Wu F (2017) Soil microbial communities in cucumber monoculture and rotation systems and their feedback effects on cucumber seedling growth. Plant Soil 415:507–520CrossRefGoogle Scholar
  49. Zhou X, Zhang J, Pan D, Ge X, Jin X, Chen S, Wu F (2018) p-Coumaric can alter the composition of cucumber rhizosphere microbial communities and induce negative plant-microbial interactions. Biol Fert Soils 54:363–372CrossRefGoogle Scholar
  50. Zwetsloot MJ, Kessler A, Bauerle TL (2018) Phenolic root exudate and tissue compounds vary widely among temperate forest tree species and have contrasting effects on soil microbial respiration. New Phytol 218:530–541PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural AffairsNortheast Agricultural UniversityHarbinChina
  2. 2.Department of HorticultureNortheast Agricultural UniversityHarbinChina

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