Passion fruit plants alter the soil microbial community with continuous cropping and improve plant disease resistance by recruiting beneficial microorganisms

Abstract

Passion fruit (Passiflora edulis) is widely grown in tropical and subtropical regions, showing high economic and ornamental value. Microorganisms are indicators for the stability and health of the soil ecosystem, which can affect the yield and quality of passion fruit under continuous cropping. High-throughput sequencing and interactive analysis were used to analyse the variation of microbial communities in the noncultivated soil (NCS), cultivated soil (CS), and the rhizosphere soil of purple passion fruit (Passiflora edulis f. edulis ×Passiflora edulis f. flavicarpa, RP) and yellow passion fruit (Passiflora edulis f. flavicarpa, RY). An average of 98,001 high-quality fungal internal transcribed spacer (ITS) sequences, mainly from Ascomycota, Basidiomycota, Mortierellomycota, Mucoromycota and Glomeromycota, as well as an average of 71,299 high-quality bacterial 16S rRNA sequences, mainly from Proteobacteria, Actinobacteria, Acidobacteria, Firmicutes and Chloroflexi, were obtained per sample. It was found that the continuous cropping of passion fruit increased the richness but reduced the diversity of soil fungi, while it dramatically increased the richness and diversity of soil bacteria. In addition, during the continuous cropping, grafting different scions in the same rootstock contributed to the aggregation of differential rhizosphere microbial communities. Among fungal genera, Trichoderma showed higher abundance in RY than in RP and CS, while the opposite was observed in the pathogen Fusarium. Moreover, the co-occurrence network and potential function analyses also showed that the appearance of Trichoderma was related to Fusarium and its contribution to plant metabolism was significantly greater in RY than in RP and CS. In conclusion, the rhizosphere of yellow passion fruit may be beneficial for the enrichment of disease-resistant microbes, such as Trichoderma, which may be an important factor inducing stronger resistance to stem rot. It will help to form a potential strategy for overcoming the pathogen-mediated obstacles in passion fruit and improve its yield and quality.

Multigenerational Adaptation Can Enhance the Pathogen Resistance of Plants via Changes in Rhizosphere Microbial Community Assembly

“…Our data show that the wild-type had a decrease in mean fresh weight due to the effects of continuous cropping, which have been shown to lead to crop growth retardation or yield reduction, , whereas rps2 plants showed significantly better growth in the third generation after successive Pst infections. The reason for this phenomenon may be that under the invasion of the same pathogen, the A. thaliana selectively enrich beneficial microorganisms at the rhizosphere, improving its immunity and passing on its legacy to the next generation. , It has been shown that continuous planting of crops (tomato, wheat, and common bean), for example, can maintain plant health despite exposure to pathogens. − Wang et al found that continuous cultivation of passion fruit increased plant disease resistance by altering the soil microbial community and by recruiting beneficial microorganisms. The exudation pattern of the plants was altered to recruit relevant beneficial microorganisms to the rhizosphere and trigger the spread of the soil legacy, maximizing the resistance of the next plant generation …”

“…40,41 It has been shown that continuous planting of crops (tomato, wheat, and common bean), for example, can maintain plant health despite exposure to pathogens. 42−44 Wang et al 45 found that continuous cultivation of passion fruit increased plant disease resistance by altering the soil microbial community and by recruiting beneficial microorganisms. The exudation pattern of the plants was altered to recruit relevant beneficial microorganisms to the rhizosphere and trigger the spread of the soil legacy, maximizing the resistance of the next plant generation.…”

Deciphering key factors in pathogen-suppressive microbiome assembly in the rhizosphere

“…To promote soil suppressiveness, beneficial microbes in the rhizosphere can be enriched by promoting their assembly ( Chen et al., 2020a ; Leite et al., 2023 ; Wang et al., 2023c ; Wantulla et al., 2023 ) or transferring pathogen-suppressive microbes into conducive soils ( Zhao et al., 2021b ; Shao et al., 2022 ; Sritongon et al., 2023 ). These enrichments have shown a great potential for improving plant health through minimized disease pressure.…”

“…Scientists argue whether changes in the microbiome structures are causal factors leading to diseases ( Li et al., 2023a ) or if they are merely consequences of diseases ( Kuang et al., 2023 ). Yet more investigations are needed to determine this phenomenon, numerous studies have demonstrated that the enhanced pathogen suppression in the rhizosphere is the result of changes in microbiome composition ( Carrión et al., 2019 ; Chen et al., 2020a ; Chen et al., 2022 ; Hong et al., 2023 ; Khatri et al., 2023b ; Wang et al., 2023c ; Zhu et al., 2023 ). Nevertheless, limited efforts have been devoted to systematic manipulation of the rhizosphere microbiome however, more insights have been gained through simplification of the core microbiome and developing synthetic microbial communities ( Hong et al., 2023 ; Zheng et al., 2023 ).…”

Seed Characteristics of Passion Fruit (Passiflora edulis f. flavicarpa) Rootstocks with Different Genotypes and Responses of Their Seedlings to Drought Stress

“…Due to continuous large-scale planting over many years, rot-inducing pathogens in passion fruit stems, such as Fusarium oxysporum f. sp. Passiflorae and F. solani, have accumulated in the soil (Salazar et al, 2016;Wang et al, 2023b). This issue is often managed by pesticide disinfection, crop rotation or interplanting, soil improvements, and the breeding of resistant varieties.…”