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

PLOS ONE RESEARCH ARTICLE Passion fruit plants alter the soil microbial community with continuous cropping and improve plant disease resistance by recruiting beneficial microorganisms Ye Wang1,2☯, Yao Teng1,2☯, Jianli Zhang3, Zixiong Zhang1, Chen Wang1, Xiukun Wu1, Xiuqin Long ID1* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Guizhou Botanical Garden, Guizhou Academy of Sciences, Guiyang, Guizhou, China, 2 Institute of Mountain Resources of Guizhou Province, Guizhou Academy of Sciences, Guiyang, Guizhou, China, 3 College of Eco-environmental Engineering, Guizhou Minzu University, Guiyang, Guizhou, China ☯ These authors contributed equally to this work. * Abstract OPEN ACCESS Citation: Wang Y, Teng Y, Zhang J, Zhang Z, Wang C, Wu X, et al. (2023) Passion fruit plants alter the soil microbial community with continuous cropping and improve plant disease resistance by recruiting beneficial microorganisms. PLoS ONE 18(2): e0281854. https://doi.org/10.1371/journal. pone.0281854 Editor: Muhammad Arif, Sakarya Uygulamali Bilimler Universitesi, TURKEY Received: March 1, 2022 Accepted: February 2, 2023 Published: February 21, 2023 Copyright: © 2023 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by Guizhou science and technology support project (QianKeHe support [2020] 1Y176). This project will provide appropriate Financial support for the paper fee. The revised Financial Disclosure is as follows:This work was supported by the National Key R & D Projects of China (2021YFD1100303), Youth Fund Project 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. PLOS ONE | https://doi.org/10.1371/journal.pone.0281854 February 21, 2023 1 / 17 PLOS ONE of Guizhou Academy of Sciences (Qiankeyuan J zi [2021] 20), Guizhou Science and Technology Plan Project (QianKeHe JiChu-ZK[2022] General 292), Guizhou science and technology support project (QianKeHe support [2019] 2269) and (QianKeHe support [2020] 1Y176). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: the authors have declared that no competing interests exist. Passion fruit plants improve disease resistance by recruiting beneficial microorganisms Introduction Passion fruit (Passiflora edulis), originating from South America, has been attractive to many consumers due to its bright colour, rich nutrients and unique flavour [1]. In recent years, the production area of passion fruit has doubled in China, surpassing Brazil by approximately 58.7% (IBGE, 2020). Two passion fruit cultivars, namely Tainong No. 1 and Fujian No. 3, cover approximately 95% of the planted area in China. Tainong No. 1 has a purple peel, intense flavour and higher cold tolerance, which is vulnerable to stem rot. Fujian No. 3, derived from an excellent single line of yellow fruits, has a yellow peel, higher sugar content and stronger disease resistance, but a milder flavour. The production scale of passion fruit in China has continued to expand, but viral diseases, stem rot, scab disease and brown spot, as well as high proportions of small and malformed fruits under continuous cropping strikingly reduce the yield and quality [2, 3]. With the increase of the market demand for passion fruit, continuous cropping has become a common practice, which usually leads to an obstacle in reducing plant growth and decreasing yield and quality by pests and diseases outbreak [4]. It is generally performed in grain and oil crops [5, 6], vegetables [7, 8], fruits [9, 10], herbal medicine [11, 12] and cash crops [13, 14]. In addition, continuous cropping has also been adopted for passion fruit in China [15]. According to preliminary investigations in different orchards, stem rot is one of the most important soil-borne disease of passion fruit and can destroy the whole garden when it breaks out. Fusarium oxysporum Schlecht and Fusarium solani (Mart) Sacc are pathogens causing stem rot of passion fruit in Guangdong, Guangxi, and Fujian provinces, and they mainly damage the base of plant stems in humid and hot environments, manifested as reddish-brown symptoms [16]. Due to a lack of effective fungicides, the diseases caused by Fusarium have always been a hard nut to crack. However, the large-scale planting of single cultivar and continuous cropping in orchards have aggravated the accumulation and spread of pathogens. In particular, there are few reports about the changes in soil microorganisms mediated by the continuous cropping of passion fruit. Some studies have confirmed that the rhizosphere is the most critica (...truncated)