Characterization and variation of the rhizosphere fungal community structure of cultivated tetraploid cotton

RESEARCH ARTICLE Characterization and variation of the rhizosphere fungal community structure of cultivated tetraploid cotton Qinghua Qiao1☯, Jingxia Zhang2☯, Changle Ma1☯, Furong Wang1,2, Yu Chen2, Chuanyun Zhang2, Hui Zhang1*, Jun Zhang ID1,2* 1 Key Laboratory of Plant Stress Research, College of Life Sciences, Shandong Normal University, Jinan, China, 2 Key Laboratory of Cotton Breeding and Cultivation in Huang-Huai-Hai Plain, Ministry of Agriculture, Cotton Research Center of Shandong Academy of Agricultural Sciences, Jinan, China a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Qiao Q, Zhang J, Ma C, Wang F, Chen Y, Zhang C, et al. (2019) Characterization and variation of the rhizosphere fungal community structure of cultivated tetraploid cotton. PLoS ONE 14(10): e0207903. https://doi.org/10.1371/journal. pone.0207903 Editor: Vijai Gupta, Tallinn University of Technology, ESTONIA Received: November 7, 2018 Accepted: October 3, 2019 Published: October 18, 2019 Copyright: © 2019 Qiao 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 financially supported in part by grants from National Project of Modern Agricultural Industry Technology System in China (CARS-15-05), Taishan Scholars Program of Shandong Province (No. ts201511070 and tshw20130962), National Major Project on Transgenic Breeding in China (2016ZX08005003- ☯ These authors contributed equally to this work. * (HZ); , (JZ) Abstract Rhizosphere fungal communities exert important influencing forces on plant growth and health. However, information on the dynamics of the rhizosphere fungal community structure of the worldwide economic crop cotton (Gossypium spp.) is limited. In the present study, next-generation sequencing of nuclear ribosomal internal transcribed spacer-1 (ITS1) was performed to characterize the rhizosphere fungal communities of G. hirsutum cv. TM-1 (upland cotton) and G. barbadense cv. Hai 7124 (island cotton). The plants were grown in field soil (FS) that had been continuously cropped with cotton and nutrient-rich soil (NS) that had not been cropped. The fungal species richness, diversity, and community composition were analyzed and compared among the soil resources, cotton genotypes, and developmental stages. We found that the fungal community structures were different between the rhizosphere and bulk soil and the difference were significantly varied between FS and NS. Our results suggested that cotton rhizosphere fungal community structure variation may have been primarily influenced by the interaction of cotton roots with different soil resources. We also found that the community composition of the cotton rhizosphere fungi varied significantly during different developmental stages. In addition, we observed fungi that was enriched or depleted at certain developmental stages and genotypes in FS and NS, and these insights can lay a foundation for deep research into the dynamics of pathogenic fungi and nutrient absorption of cotton roots. This research illustrates the characteristics of the cotton rhizosphere fungal communities and provides important information for understanding the potential influences of rhizosphere fungal communities on cotton growth and health. Introduction Soil microorganisms play a key role in agricultural ecosystem. The importance of the mutual influence between microbial communities and agronomic practices is increasingly being recognized. The rhizosphere is the soil area that adjacent to plant roots, in which the PLOS ONE | https://doi.org/10.1371/journal.pone.0207903 October 18, 2019 1 / 16 Cotton rhizosphere fungal community structure 008) and the Provincial Science Foundation in Shandong (ZR2014CQ047). Competing interests: The authors have declared that no competing interests exist. interactions between soil microorganism and plant roots are very intense. Plants play important roles on rhizosphere microbiome assembly and functions [1]. The composition of rhizosphere microbial communities is affected by the soil, plant developmental stage, and many other factors [2–6]. Rhizosphere microorganisms are considered pivotal for plant health and growth due to their involvement in such key processes as the formation of the root architecture [7]; formation of soil characteristics [8]; decomposition of organic matter [9, 10]; decomposition and removal of toxins [11, 12]; defense against plant pathogenic microorganisms and pests [7, 13]; and cycling of carbon [14], nitrogen, phosphorus, and sulfur [15–18]. Rhizosphere fungi are critical component of the rhizosphere microbial communities, and play an important role in plant growth and health. In turn, plants largely control rhizosphere fungi through the production of carbon- and energy-rich compounds and bioactive phytochemicals [19]. Some of the beneficial fungi are directly involved in the cycling of nutrients and function as an essential link for soil nutrient availability [20–23]. Some fungi are known for having biocontrol activity against pathogenic microorganisms [23, 24]. These fungi positively influence plant productivity by enhancing plant growth. However, certain rhizosphere fungi can negatively influence plant productivity by infecting roots and causing serious disease. For example, Fusarium graminearum can cause stalk rot disease of maize [25], Verticillium nonalfalfae could cause Verticillium wilt on tree-of-heaven [26], and Macrophomina phaseolina can cause dry root rot disease [27]. Cotton (Gossypium spp.) is the most important cash crop and is widely grown to produce both natural fibers and cotton seed soil. Cotton production is threatened by soil-borne plant pathogens, such as Rhizoctonia spp. [28], Fusarium moniliforme [29], Alternaria alternata [30], and Verticillium dahliae [31]. Understanding the dynamics of the rhizosphere fungal community structure of cotton during different developmental stages will not only provide basic information on the dynamics of the cotton rhizosphere fungal community structure but also help lay a foundation for understanding the mutual influence between rhizosphere fungal communities and the plant health of cotton. Knox et al. showed that rhizosphere microbial diversity in cotton is significantly influenced by the cultivar type in the field [32]. However, systematic studies on the rhizosphere fungal community structure of cultivated tetraploid cotton are still lacking. This study characterized the rhizosphere fungal community dynamics across cotton developmental stage growth using two cotton cultivars in two different types of soil. Our work lays the foundation for cotton rhizosphere fungal community research and pro (...truncated)