Foliar pathogen-induced assemblage of beneficial rhizosphere consortia increases plant defense against Setosphaeria turcica

¹ Key Laboratory of Bio-organic Fertilizer Creation, Ministry of Agriculture and Rural Affairs, College of Resource and Environment, Anhui Science and Technology University, 233100 Bengbu, Anhui, China

² School of Life Science and Technology, Tongji University, 200092 Shanghai, China

^*Correspondence: luxm@ahstu.edu.cn (Xiaomin Lu)

Front. Biosci. (Landmark Ed) 2021, 26(9), 543–555; https://doi.org/10.52586/4966

Submitted: 3 May 2021 | Revised: 2 July 2021 | Accepted: 2 July 2021 | Published: 30 September 2021

This is an open access article under the CC BY 4.0 license (https://creativecommons.org/licenses/by/4.0/).

Abstract

Background: Foliar pathogen infection can induce the enrichment of beneficial microbial consortia in plant rhizosphere, but the mechanism for enhanced plant resistance is unclear. Methods: We investigated the effects of foliar pathogen infection on bacterial communities in maize rhizosphere using high throughput sequencing. Results: Maize plants grown in non-sterilized soils displayed stronger defense against the foliar pathogen Setosphaeria turcica than those in sterilized soils. Foliar pathogen infection further triggered the shift in the structure and composition of rhizosphere bacterial communities. The pathogen-infected plants specially promoted rhizosphere colonization of several bacterial taxa. The Pseudomonas genus increased in the rhizosphere after pathogen infection. Other bacterial genera such as Chitinophaga and Flavobacterium were also greatly enriched in the rhizosphere of pathogen-infected plants. Furthermore, the enriched bacterial species were isolated and were shown to interact synergistically to promote biofilm formation. Although both the Chitinophaga and Flavobacterium species did not induce plant defense, the Pseudomonas species markedly increased the resistance of plants against S. turcica. Furthermore, the consortium consisting of the Pseudomonas, Chitinophaga and Flavobacterium species (CONpcf) conferred long-acting disease resistance of maize plants as compared to the individual Pseudomonas species. Furthermore, the inoculation with the CONpcf significantly induced a marked increase in the levels of DIMBOA in maize leaves, indicating that the consortium-induced increases of DIMBOA levels partially contributed to enhancing disease resistance of plants. Conclusions: Foliar infection of maize plants by S. turcica specifically recruited a group of beneficial rhizosphere bacteria, which conferred enhanced plant defense against pathogen infection. This study provided important evidence that above-ground pathogen infection participated in the mediation of below-ground microbiome for regulating plant defense systems.

Keywords

Rhizosphere microbiome

Disease resistance

Benzoxazinoid

Setosphaeria turcica

Funding

202004a06020003/Key Research and Development Projects of Anhui Province

gxypZD2020038/Outstanding Talent Cultivation Program in Colleges and Universities of Education Department of Anhui province

KJ2018ZD051/Natural Science Foundation of Education Department of Anhui province

1908085QC110/Natural Science Foundation from Anhui province

KLFECPP201802/Open Funds of the Anhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention

ZHEP2019001/School-enterprise Cooperation Projects

Figures

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Fig. 1.

Effects of S. turcica infection on the rhizosphere bacterial communities of maize plants. (a) Three-week-old maize plants grown in non-sterilized soils were subjected to treatment with or without S. turcica. Rhizosphere bacterial communities were examined in the plants after 3 and 6 weeks of sterile water (mock) and foliar pathogen treatments. (b) Three-week-old maize plants grown in both the non-sterilized (NS) and sterilized (S) soils were challenged by S. turcica. Relative lesion area was assessed at 6 weeks post pathogen infection (n = 15 biological replicates). (c) Diversity (Shannon) and (d) richness (Chao1) of rhizosphere bacterial communities (n = 10 biological replicates). (e) NMDS analyses of rhizosphere bacterial communities (n = 10 biological replicates). M3W, plants grown in the NS soils at 3 weeks of mock treatment; M6W, plants grown in NS soils at 6 weeks of mock treatment; P3W, plants grown in NS soils at 3 weeks of foliar pathogen infection; P6W, plants grown in NS soils at 6 weeks of foliar pathogen infection. Different letters indicated significant differences using one-way ANOVA followed by Ducan’s multiple range test at p $<$ 0.05.

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