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Diversity of Root-Associated Fungi of Rhododendron Simsii in Subtropical

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Diversity of Root-Associated Fungi of Rhododendron Simsii in Subtropical J. For. Res. (2019) 30(6):2321–2330 https://doi.org/10.1007/s11676-019-01050-4 ORIGINAL PAPER Diversity of root‑associated fungi of Rhododendron simsii in subtropical forests: fungal communities with high resistance to anthropogenic disturbances Yanhua Zhang1 · Fangping Tang1 · Jian Ni1 · Lijia Dong1 · Lifu Sun1 Received: 15 January 2019 / Accepted: 23 April 2019 / Published online: 9 October 2019 © The Author(s) 2019 Abstract Species of the Ericaceae or heath family are (2) while there were a few indicator OTUs specifc to difer- widely distribute in continental ecosystems and their spe- ent forest types, seasons and years, the proportion of shared cial ericoid mycorrhizas (ERM) are considered benefcial to taxa was quite large, accounting for 44.9–79.4% of the total their survival and persistence in variable habitats. Currently, OTUs; (3) signifcantly positive correlations were found increasing anthropogenic disturbances and improper forest between disturbance sensitivity and temporal variations in management are afecting subtropical forests of China where common fungal orders, and both in major fungal orders were these native species located. These activities not only afect signifcantly diferent among fungal functional groups in plant communities above-ground, but also impose pressures which putative and possible ERM fungi were highly resist- on microbial communities below- ground. In this study, root- ant to disturbances and low temporal variations. The high associated fungal communities of Rhododendron simsii in disturbance resistance and temporal persistence of putative four forest types under diferent anthropogenic disturbances ERM fungi may be essential for the successful adaptation of were identifed using an Illumina Miseq platform, i.e., old R. simsii in disturbed subtropical forests of China. growth forests, secondary forests with one cutting (SEC I), secondary forests with two cuttings (SEC II), and Chinese- Keywords Rhododendron simsii · Mycorrhiza · Fungal fr plantations (PLF). Intra- and inter-annual variations were community · Diversity · Subtropical forests · Human analyzed by comparing samples taken in diferent seasons disturbance and years. The results show that: (1) over 1000 OTUs were found in hair roots with most from the division Ascomycota and Basidiomycota belonging to diferent functional groups; Introduction Rhododendron simsii Project funding: This study is supported by the National Natural Planch. is popular as a landscape Science Foundation of China (31170469 and 31700476), plant because of its beautiful fowers. It occurs naturally Zhejiang Natural Science Foundation (LY19C030002) and the in China, Japan, Laos, Myanmar and Thailand. In most Technology Division of Shaoxing (2017B70061). southern provinces of China, R. simsii populations occur The online version is available at http://www.sprin gerli nk.com. in subtropical forests, along forest margins and in open upland thickets at 500–2700 m a.s.l. (Editorial Committee Corresponding editor: Yu Lei. of Flora of China, Chinese Academy of Sciences 2006). However, their natural habitats are frequently disturbed by Electronic supplementary material The online version of this anthropogenic activities. Most Rhododendron species have article (https ://doi.org/10.1007/s1167 6-019-01050 -4) contains supplementary material, which is available to authorized users. typical ericoid mycorrhizas (ERM) (Fumiaki et al. 2003; Zhang et al. 2009; Tian et al. 2011), which are considered * Lifu Sun to be helpful for both the host plant and their fungal partners [email protected] to be distributed widely in the world (Cázares et al. 2005; 1 College of Life Sciences, Shaoxing University, Bougoure et al. 2007; Fujimura and Egger 2012; Gorzelak Shaoxing 312000, People’s Republic of China et al. 2012). Vol.:(0123456789)1 3 2322 Y. Zhang et al. Anthropogenic disturbances and particular types of forest thinned in the past 100 years. Both SEC I and SEC II were management such as clear-cutting, selective cutting, planting clear-cut about 50 years ago, and SEC II was selectively of high-value species, not only infuence plant communi- cut 20 years ago. Since the previous disturbances, all stands ties above-ground but also underground fungal communi- have naturally regenerated. Twelve 1-ha (100 m × 100 m) ties associated with plant roots. For example, ERM fungal plots were established with three replicates for each forest communities under diferent vegetation types such as bogs, type. rough grazing and forest plantations (Hazard et al. 2014), and arbuscular mycorrhizal fungi (AMF) along an anthro- Sampling procedure pogenic disturbance gradient (Gavito et al. 2008), show sig- nifcant changes. The results of 378 case studies summarized Hairy root samples of four R. simsii plants were collected by Shade et al. (2012) indicated that most soil microbial from each sample plot over six periods, March, June, Sep- communities were sensitive to disturbance. In addition, only tember and December of 2012, and March 2013, and March 23% of microbial communities recover based on their com- 2014. There were 288 individual samples (4 samples × 12 position and/or function from 148 cases involved in resil- plots × 6 sampling times). The fne roots were collected from ience, (the rate of recovery after disturbance), suggesting soils at four directions around the taproots. After soaking that disturbance plays a major role in mycorrhizal fungal and cleaning in sterile water, 20 (about 1-cm long) hair root and soil microbial communities, but recovery depends on segments were randomly selected and put separately into a specifc conditions. 1.5 mL centrifugal tube for DNA extraction. A 200-g soil In this study, intra- and inter-annual variations of fungal sample was collected for elemental analyses from the top communities associated with hair roots of R. simsii growing 10-cm layer of soil around each sample plant. in Chinese subtropical forests were examined across difer- ent types of anthropogenic disturbances. Three hypotheses DNA extraction and Illumina MiSeq sequencing are proposed: (1) fungal communities associated with hair roots of R. simsii would be diferent along the disturbance DNA was extracted according to Zhang et al. (2016). The gradient, across seasons and years; (2) diferent fungal taxa ITS1 region special for fungi was selected to be amplifed by would show diferent responses to disturbance and tempo- PCR with 1723F and 2043R primers; the PCR reaction and ral variations; and, (3) disturbance resistance and temporal amplicons purifcation procedures are based on Zhang et al. persistence of fungal functional groups might be correlated, (2017). The Illumina MiSeq sequencing were completed by and ERM fungi would be more consistently associated with Shanghai Majorbio Co. Ltd. in China. Raw fastq fles were their R. simsii hosts than any other fungal groups. demultiplexed and quality-fltered using QIIME (ver 1.7) following Zhang et al. (2016). Open reference operational taxonomic unit (OTU) pick- Materials and methods ing was done with pick_open_reference_otus.py using the default uclust method and ITS 12-11 dataset (97% similar- Study site ity), and singletons were removed during OTU picking. Sin- gle_rarefaction.py in Qiime was used to generate an OTU Gutianshan National Nature Reserve in Zhejiang Province table with even reads of 10,000 in each root sample. Rare (GNNR) was selected as the sampling site for this study. fungal OTUs occurring in only one or two samples out of Annual average temperatures are above 15 °C and Annual 72 were not considered in further analyses. precipitation are more than 1750 mm. The vegetation of Mean relative abundances (MRAd) of fungal orders under the site is subtropical evergreen broad-leaf forest (Yu et al. the four forest types were calculated and the disturbance sen- 2001), and the main soil type is subtropical red soil (Zhang sitivity of each fungal order defned as the coefcient of vari- et al. 2011). The dominant species are Castanopsis eyrei ance (CVd) of MRAd. Mean relative abundances (MRA t) of (Champ. ex Benth.) Tutcher and Schima superba Gardner fungal orders in six sampling times were also calculated and & Champ. the temporal variation of each fungal order was defned as Due to diferent disturbance histories, there are four dis- the coefcient of variance (CV t) of MRAt of sampling times. tinct types of stands in the GNNR: Chinese- fr (Cunningha- mia lanceolata (Lamb.) Hook) plantations (PLF), old growth Statistical analysis forests (OGF), secondary forests with one cutting (SEC I), and secondary forests with two cuttings (SEC II). The PLF The differences population densities and mean DBH were planted 20 years ago after clear- cutting of second- (diameter at breast height) of R. simsii between the four ary growth forests. The OGF are undisturbed forests located forest types was analyzed using one-way ANOVA with at the heart of the GNNR and have not been harvested or SPSS 22.0. The otu_category_signifcance.py in Qiime 1 3 Diversity of root‑associated fungi of Rhododendron simsii in subtropical forests: fungal… 2323 analyzed and determined the indicator fungal species for large-diameter trees in the OGF. The dominant species the diferent forest types, seasons, and years. The main (Chinese- fr) and plant composition in PLF are obviously infuencing factors of root-associated fungal communities diferent from the secondary and old growth forests. Mean were identifed with “Envft” function. The “rda” function DBH and population density of R. simsii in the four forest in the R package “vegan” performed principal components types are shown in Appendix S1. There were no signifcant analysis (PCA), and the frst three components (PC1, PC2, diferences in these two parameters among the forest types and PC3) were used as plant parameters in “envft”. The (P > 0.05), although the density was the lowest and mean impacts of forest type, season and year on the community DBH was the highest in the OGF. composition of root-associated fungi were evaluated with the “Adonis” function in the R package “vegan”. Fungal OTUs in hair roots of Rhododendron simsii Rarefaction curves of the observed fungal OTUs in hair roots Results of R.
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