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Leaching alleviates phenol-mediated root rot in Panax notoginseng by modifying the soil microbiota

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Abstract

Background and aims

Overaccumulation of allelochemicals in soil from trees has a negative effect on the growth of Panax notoginseng and cause root rot. Many plant secreted phenols are water-soluble substances that can be depleted by leaching. However, comprehensive understanding of the effect of leaching of phenols in Chinese fir soil on P. notoginseng root rot disease is still lacking.

Methods

Soil with high level of phenols was leached with five intensities and their effect on the root rot of P. notoginseng was assessed. Then, the relationship of root rot with changes in soil chemical properties and phenol content as well as rhizospheric microorganisms was analyzed.

Results

With increasing leaching intensity, the levels of phenols in soils and the incidence of root rot decreased significantly. Decreased phenol content could alleviate root rot by modifying the soil microbial community. Network analysis showed that root rot incidence was positively correlated with the p-hydroxybenzoic acid-enriched pathogenic fungus Ilyonectria but negatively correlated with p-hydroxybenzoic acid (HA)-, ferulic acid (FA)- or vanillic acid (VA)-suppressed bacteria, including Sphingomonas, Lysobacter, Massilia and Burkholderia. Culture experiments confirmed that individual HA, FA and VA as well as a mixture of the five phenols with increasing concentrations could stimulate the growth and sporulation of I. destructans but suppress the growth and biofilm formation of bacteria (Burkholderia and Lysobacter). Moreover, Burkholderia isolates showed antagonistic activity against the growth of I. destructans.

Conclusions

Leaching could relieve the stimulation of pathogenic fungi by phenols and reduce the pressure on phenolic-suppressed bacteria, thereby reducing the incidence of root rot disease.

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Acknowledgements

This study was financed by the National Key Research and Development Program of China (2017YFC1702502), the Yunnan provincial key programs of Yunnan Eco-friendly Food International Cooperation Research Center Project (2019ZG00901), the Young and Middle-aged Academic and Technical Leaders Reserve Programme in Yunnan Province (202005 AC160045), the Natural Science Foundation of China (31760535; 31772404), the Yunnan Ten Thousand Talents Plan Young & Elite Talents Project (to Shusheng Zhu and Min Yang), the Innovative Research Team of Science and Technology in Yunnan Province (202105AE160016), the Central Government Guides Local Science and Technology Development Funds (202107AA110004). the Central Government.

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Correspondence to Min Yang or Shusheng Zhu.

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Responsible Editor: Hans Lambers.

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Supplementary Information

Table S1

Phenols identified by UPLC-MS. HA, V, SA, FA and VA represent p-hydroxybenzoic acid, vanillin, syringic acid, ferulic acid and vanillic acid, respectively. (DOCX 16 kb)

Table S2

Final concentrations of mixed phenols (HA + V + SA + FA + VA) in PDA or Minimal media. HA, V, SA, FA and VA represent p-hydroxybenzoic acid, vanillin, syringic acid, ferulic acid and vanillic acid, respectively. (DOCX 14 kb)

Table S3

Chemical properties of soil during the period of root rot occurrence. AN, AP, AK, OM, EC, HA, V, SA, FA and VA represent available nitrogen, available phosphorus, available potassium, organic matter and electrical conductivity, p-hydroxybenzoic acid, vanillin, syringic acid, ferulic acid and vanillic acid, respectively. All data are presented as the mean ± standard errors (SE) calculated from three biological replicates. Bars indicate SE, and the different letters indicate significant differences among the treatments (one-way ANOVA with Duncan’s test). (DOCX 15 kb)

Table S4

ITS and 16S rRNA gene sequence information of each treatment. All data are presented as the mean ± standard errors (SE) calculated from three biological replicates. Bars indicate SE, and the different letters indicate significant differences among the treatments (one-way ANOVA with Duncan’s test). (DOCX 15 kb)

Table S5

Relative abundance of fungi and bacteria in different leaching treatments. All data are presented as the mean ± standard errors (SE) calculated from three biological replicates. Bars indicate SE, and the different letters indicate significant differences among the treatments (one-way ANOVA with Duncan’s test). (DOCX 15 kb)

Table S6

Effect of leaching on the growth of P. notoginseng in the treatments without consecutive soil. All data are presented as the mean ± standard errors (SE) calculated from three biological replicates. Bars indicate SE, and the different letters indicate significant differences among the treatments (one-way ANOVA with Duncan’s test). (DOCX 16 kb)

Figure S1

Effects of phenols on the growth of Burkholderia sp. and Lysobacter sp. (A) Growth rate. (B) Biofilm formation. HA, V, SA, FA, VA, and M respectively represent p-hydroxybenzoic acid, vanillin, syringic acid, ferulic acid, vanillic acid and mixture. The final concentrations of mixture of phenols (HA + V + SA + FA + VA) in medium were respectively set at the same ratio and concentration as detected in five leaching treatments soil. All data are presented as the mean ± standard errors (SE) calculated from three biological replicates. Bars indicate SE, and the different letters indicate significant differences among the treatments (one-way ANOVA with Duncan’s test). All data are presented as the mean ± standard errors (SE) calculated from three biological replicates. Bars indicate SE, and the different letters indicate significant differences among the treatments (one-way ANOVA with Duncan’s test). (PNG 1075 kb)

High resolution image (TIF 742 kb)

Figure S2

Community alpha diversity indexes of the fungal community (A-C) and bacterial community (D-F) in rhizospheric soil by MiSeq sequencing. All data are presented as the mean ± standard errors (SE) calculated from three biological replicates. Bars indicate SE, and the different letters indicate significant differences among the treatments (one-way ANOVA with Duncan’s test). (PNG 156 kb)

High resolution image (TIF 2616 kb)

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Zhang, Y., Li, T., Ye, C. et al. Leaching alleviates phenol-mediated root rot in Panax notoginseng by modifying the soil microbiota. Plant Soil 468, 491–507 (2021). https://doi.org/10.1007/s11104-021-05136-z

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