Browse > Article
http://dx.doi.org/10.1080/12298093.2021.1913826

Geographical Isolation and Root-Associated Fungi in the Marine Terrains: A Step Toward Establishing a Strategy for Acquiring Unique Microbial Resources  

Park, Jong Myong (Water Quality Research Institute, Waterworks Headquarters Incheon Metropolitan City)
Hong, Ji Won (Department of Hydrogen and Renewable Energy, Kyungpook National University)
Lee, Woong (Research Institute for Dok-do and Ulleung-do Island, Kyungpook National University)
Lee, Byoung-Hee (Biological and Genetic Resources Assessment Division, National Institute of Biological Resources)
You, Young-Hyun (Microorganism Resources Division, National Institute of Biological Resources)
Publication Information
Mycobiology / v.49, no.3, 2021 , pp. 235-248 More about this Journal
Abstract
This study aimed to understand whether the geo-ecological segregation of native plant species affects the root-associated fungal community. Rhizoplane (RP) and rhizosphere (RS) fungal microbiota of Sedum takesimense native to three geographically segregated coastal regions (volcanic ocean islands) were analyzed using culture-independent methods: 568,507 quality sequences, 1399 operational taxonomic units, five phyla, and 181 genera were obtained. Across all regions, significant differences in the phyla distribution and ratio were confirmed. The Chao's richness value was greater for RS than for RP, and this variance coincided with the number of genera. In contrast, the dominance of specific genera in the RS (Simpson value) was lower than the RP at all sites. The taxonomic identity of most fungal species (95%) closely interacting with the common host plant was different. Meanwhile, a considerable number of RP only residing fungal genera were thought to have close interdependency on their host halophyte. Among these, Metarhizium was the sole genus common to all sites. These suggest that the relationship between potential symbiotic fungi and their host halophyte species evolved with a regional dependency, in the same halophyte species, and of the same natural habitat (volcanic islands); further, the fungal community differenced in distinct geographical regions. Importantly, geographical segregation should be accounted for in national culture collections, based on taxonomical uniqueness.
Keywords
Fungal community; geographical segregation; rhizoplane; rhizosphere; Metarhizium;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Wilke AB, Marrelli MT. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors. 2015;8:342.   DOI
2 Xu F, Yang G, Wang J, et al. Spatial distribution of root and crown rot fungi associated with winter wheat in the north china plain and its relationship with climate variables. Front Microbiol. 2018;25:9.
3 Barton LL, Northup DE. Microbial ecology. Hoboken (NJ): Wiley-Blackwell; 2011.
4 Gong Y, Son SJ. A study of oceanic thermal fronts in the Southern Japan Sea. Bull Fish Res Dev Agency. 1982;28:25-54.
5 Park B, Kang GW, Song GM, et al. Ten newly recorded species of insect on Dokdo Island, South Korea. J Species Res. 2017;6(3):280-290.   DOI
6 Baumler A, Fang FC. Host specificity of bacterial pathogens. Cold Spring Harb Perspect Med. 2013;3(12):a010041.   DOI
7 Morris CE, Moury B. Revisiting the concept of host range of plant pathogens. Annu Rev Phytopathol. 2019;57:63-90.   DOI
8 Baker DK, Rice SJ, Leemon DM, et al. Horizontal transmission of Metarhizium anisopliae (Hypocreales: Clavicipitacea) and the effects of infection on oviposition rate in laboratory populations of Musca domestica (Diptera: Muscidae). Pest Manag Sci. 2017;74(4):987-991.   DOI
9 Lozupone CA, Knight R. Global patterns in bacterial diversity. Proc Natl Acad Sci USA. 2007;104:11436-11440.   DOI
10 Ma B, Gong J. A meta- analysis of the publicly available bacterial and archaeal sequence diversity in saline soils. World J Microbiol Biotechnol. 2013;29:2325-2334.   DOI
11 Liao X, Lovett B, Fang W, et al. Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology. 2017;163(7):980-991.   DOI
12 Kevin M. A review of living collections with special emphasis on sustainability and its impact on research across multiple disciplines. Biopreserv Biobank. 2017;15(1):20-30.   DOI
13 Bengtsson Palme J, Ryberg M, Hartmann M, et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol. 2013;4(10):914-919.
14 Blaud A, Lerch TZ, Phoenix GK, et al. Arctic soil microbial diversity in a changing world. Res Microbiol. 2015;166(10):796-813.   DOI
15 Haegeman B, Hamelin J, Moriarty J, et al. Robust estimation of microbial diversity in theory and in practice. ISME J. 2013;7:1092-1101.   DOI
16 Magurran AE. Measuring biological diversity. Oxford (UK): Blackwell Science; 2004.
17 Ryan MJ, McCluskey K, Verkleij G, et al. Fungal biological resources to support international development: challenges and opportunities. World J Microbiol Biotechnol. 2019;35(9):139.   DOI
18 Park JM, Hong JW, Son JS, et al. A strategy for securing unique microbial resources-focusing on Dokdo islands-derived microbial resources. Israel J Ecol Evol. 2018;64(1-4):1-11.   DOI
19 Bloemberg GV, Lugtenberg BJ. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol. 2001;4:343-350.   DOI
20 Li HB, Singh RK, Singh P, et al. Genetic diversity of nitrogen-fixing and plant growth promoting Pseudomonas species isolated from sugarcane rhizosphere. Front Microbiol. 2017;14(8):1268.
21 Wang Z, Li T, Wen X, et al. Fungal communities in rhizosphere soil under conservation tillage shift in response to plant growth. Front Microbiol. 2017;11(8):1301.   DOI
22 Chen K, Wu XQ, Huang MX, et al. First report of brown culm streak of Phyllostachys praecox caused by Arthrinium arundinis in Nanjing, China. Plant Dis. 2014;98(9):1274.   DOI
23 Chao A, Shen TJ, Ma KH, et al. User's guide for program SPADE (Species Prediction And Diversity Estimation). Taiwan: National Tsing Hua University; 2016 [cited 2019 Dec 18]. Available from: http://chao.stat.nthu.edu
24 Sonn YK, Park CW, Zhang YS, et al. Characteristics of soils distributed on the Dokdo Island in South Korea. Korean J Soil Sci. 2011;44(2):187-193.   DOI
25 Hameed A, Gulzar S, Aziz I, et al. Effects of salinity and ascorbic acid on growth, water status, and antioxidant system in a perennial halophyte. AoB Plants. 2015;7:1-11.
26 Sapkota R, Jorgensen LN, Nicolaisen M. Spatiotemporal variation and networks in the mycobiome of the wheat canopy. Front Plant Sci. 2017;8:1357.   DOI
27 Nehls U. Review Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot. 2008;59(5):1097-1108.   DOI
28 Lambshead PJD, Platt HM, Shaw KM. The detection of differences among assemblages of marine benthic species based on an assessment of dominance and diversity. J Nat Hist. 1983;17(6):859-874.   DOI
29 Zain Ul Arifeen M, Ma YN, Xue YR, et al. DeepSea fungi could be the new arsenal for bioactive molecules. Mar Drugs. 2019;18(1):9.   DOI
30 Amna T, Puri SC, Verma V, et al. Bioreactor studies on the endophytic fungus Entrophospora infrequens for the production of an anticancer alkaloid camptothecin. Can J Microbiol. 2006;52(3):189-196.   DOI
31 Busby PE, Ridout M, Newcombe G. Fungal endophytes: modifiers of plant disease. Plant Mol Biol. 2016;90(6):645-655.   DOI
32 Toju H, Tanabe AS, Sato H. Network hubs in root-associated fungal metacommunities. Microbiome. 2018;6(1):116.   DOI
33 Chapman VJ. Salt marshes and salt deserts of the world. In: Polunin N, editor. Ecology of halophytes. New York (NY): Academic Press; 1974.
34 Park JM, Hong JW, Lee W, et al. Fungal clusters and their uniqueness in geographically segregated wetlands: a step forward to marsh conservation for a wealth of future fungal resources. Mycobiology. 2020;48(5):351-363.   DOI
35 Ministry of Environment, Republic of Korea. Report: conservation and sustainable use of biological resources [Internet]. Sejong (South Korea): MoE; 2015 [cited 2019 October 19]. Available from: http://hdl.handle.net/20.500.11822/9049
36 Wu L, Chen J, Xiao Z, et al. Barcoded pyrosequencing reveals a shift in the bacterial community in the rhizosphere and rhizoplane of Rehmannia glutinosa under consecutive monoculture. Int J Mol Sci. 2018;19(3):850.   DOI
37 Lee DS. Geology of Korea. Seoul (Republic of Korea): Kyohak-sa; 1987.
38 Zhao C, Wang CB, Ma XG, et al. Phylogeographic analysis of a temperate-deciduous forest restricted plant (Bupleurum longiradiatum Turcz.) reveals two refuge areas in China with subsequent refugial isolation promoting speciation. Mol Phylogenet Evol. 2013;68(3):628-643.   DOI
39 Xu J, Saunders CW, Hu P, et al. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci USA. 2007;104(47):18730-18735.   DOI
40 Lovett B, St Leger RJ. Stress is the rule rather than the exception for Metarhizium. Curr Genet. 2015;1(3):253-261.   DOI
41 Kamel NM, Abdel-Motaal FF, El-Zayat SA. Endophytic fungi from the medicinal herb Euphorbia geniculata as a potential source for bio-active metabolites. Arch Microbiol. 2020;202(2):247-255.   DOI
42 Zhang Z, Zhou X, Tian L, et al. Fungal communities in ancient peatlands developed from different periods in the Sanjiang Plain, China. PLoS One. 2017;12(12):e0187575.   DOI
43 Rohini S, Aswani R, Kannan M, et al. Culturable endophytic bacteria of ginger rhizome and their remarkable multi-trait plant growth-promoting features. Curr Microbiol. 2017;75:505-511.   DOI
44 Jaber E, Xiao C, Asiegbu FO. Comparative pathobiology of Heterobasidion annosum during challenge on Pinus sylvestris and Arabidopsis roots: an analysis of defensin gene expression in two pathosystems. Planta. 2014;239(3):717-733.   DOI
45 Lucas M, Balbin-Suarez A, Smalla K, et al. Root growth, function, and rhizosphere microbiome analyses show local rather than systemic effects in apple plant response to replant disease soil. PLoS One. 2018;13(10):e0204922.   DOI
46 Sati SC, Belwal M. Aquatic hyphomycetes as endophytes of riparian plant roots. Mycologia. 2005;97(1):45-49.   DOI
47 Tazi L, Breakwell DP, Harker AR, et al. Life in extreme environments: microbial diversity in Great Salt Lake, Utah. Extremophiles. 2014;18(3):525-535.   DOI
48 Otlewska A, Migliore M, Dybka-SteRpien K, et al. When salt meddles between plant, soil, and microorganisms. Front Plant Sci. 2020;16(11):553087.
49 Johnson NC, Graham JH, Smith FA. Functioning of mycorrhizal associations along the mutualism--parasitism continuum. New Phytol. 1997;135(4):575-585.   DOI
50 Zhong X, Peng QY, Li SS, et al. Detection of Ophiocordyceps sinensis in the roots of plants in alpine meadows by nested-touchdown polymerase chain reaction. Fungal Biol. 2014;118(4):359-363.   DOI
51 NGII (National Geographic Information Institute). The geography of Dokdo. Suwon (Republic of Korea): Press of National Geographic Information Institute; 2015.
52 Kong WS, David W. The plant geography of Korea with an emphasis on the alpine zones. Berlin (Germany): Springer; 1993.
53 Thorpe RS, Surget-Groba Y, Johansson H. Genetic tests for ecological and allopatric speciation in anoles on an island archipelago. PLoS Genet. 2010;6(4):e1000929.   DOI
54 Yang Y, Dou Y, Huang Y, et al. Links between soil fungal diversity and plant and soil properties on the Loess plateau. Front Microbiol. 2017;78:2198.   DOI
55 You YH, Park JM, Park JH, et al. Specific rhizobacterial resources: characterization and comparative analysis from contrasting coastal environments of Korea. J Basic Microbiol. 2016;56(1):92-101.   DOI
56 CHA (Cultural Heritage Administration), Republic of Korea. Natural heritage of Korea, Dokdo, Cultural Heritage Administration of Korea. Daejeon (Republic of Korea): Cultural Heritage Administration; 2009.
57 FAO. Guidelines for soil description. 4th ed. Rome (Italy): Food and Agriculture Organisation of the United States; 2006.
58 Flores-Vargas RD, O'Hara GW. Isolation and characterization of rhizosphere bacterial with potential for biological control of weed in vineyards. J Appl Microbiol. 2006;100(5):946-954.   DOI
59 Vega NOW. A review on beneficial effects of rhizosphere bacterial on soil nutrient availability and plant nutrient uptake. Rev Fac Nac Agron Medellin. 2007;60(1):3621-3643.
60 U.S. Salinity Lab Staff. Diagnosis and improvement of saline and alkali soils. In: Richards LA, editor. Agriculture handbook 60. Washington (DC): USDA; 1954. p. 122-124.
61 Bremner JM, Mulvaney CS. Nitrogen total. In: Page AL, editor. Methods of soil analysis: part 2 chemical and microbiological properties, 9.2.2. 2nd ed. Madison (WI): American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America; 1983.
62 Quilliam RS, Jones DL. Fungal root endophytes of the carnivorous plant Drosera rotundifolia. Mycorrhiza. 2010;20(5):341-348.   DOI
63 Masella AP, Bartram AK, Truszkowski JM, et al. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinf. 2012;13(1):31.   DOI
64 Schloss PD, Westcott SL, Ryabin T, et al. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537-7541.   DOI
65 Ministry of Environment, Republic of Korea. The Fifth national report to the convention on biological diversity [Internet]. Sejong (South Korea): MoE; 2014 [cited 2019 October 19]. Available from: https://www.cbd.int/nr5/
66 Araujo CAS, Dias LP, Ferreira PC, et al. Responses of entomopathogenic fungi to the mutagen 4-nitroquinoline 1-oxide. Fungal Biol. 2018;122(6):621-628.   DOI
67 Barelli L, Waller AS, Behie SW, et al. Plant microbiome analysis after Metarhizium amendment reveals increases in abundance of plant growth-promoting organisms and maintenance of disease-suppressive soil. PLoS One. 2020;15(4):e0231150.   DOI
68 Renker C, Blanke V, Borstler B, et al. Diversity of Cryptococcus and Dioszegia yeasts (Basidiomycota) inhabiting arbuscular mycorrhizal roots or spores. FEMS Yeast Res. 2004;4(6):597-603.   DOI
69 Cullings K, Makhija S. Ectomycorrhizal fungal associates of Pinus contorta in soils associated with a hot spring in Norris Geyser Basin, Yellowstone National Park, Wyoming. Appl Environ Microbiol. 2001;67(12):5538-5543.   DOI
70 Wang JB, St LR. Wang C. Advances in genomics of entomopathogenic fungi. Adv Genet. 2016;94:67-105.   DOI
71 Park JM, You YH, Back CG, et al. Fungal load in Bradysia agrestis, a phytopathogen-transmitting insect vector. Symbiosis. 2018;74(2):145-158.   DOI
72 Mukherjee K, Vilcinskas A. The entomopathogenic fungus Metarhizium robertsii communicates with2-the insect host Galleria mellonella during infection. Virulence. 2017;9(1):402-413.   DOI
73 Palenzuela J, Barea JM, Ferrol N, et al. Entrophospora nevadensis, a new arbuscular mycorrhizal fungus from Sierra Nevada National Park (southeastern Spain). Mycologia. 2010;102(3):624-632.   DOI
74 Chao A, Gotelli NJ, Hsieh TC, et al. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr. 2014;84(1):45-67.   DOI
75 Ashraf M, Farooq M, Shakeel M, et al. Influence of entomopathogenic fungus, Metarhizium anisopliae, alone and in combination with diatomaceous earth and thiamethoxam on mortality, progeny production, mycosis, and sporulation of the stored grain insect pests. Environ Sci Pollut Res Int. 2017;24(36):28165-28174.   DOI
76 Kabaluk T, Li-Leger E, Nam S. Metarhizium brunneum - An enzootic wireworm disease and evidence for its suppression by bacterial symbionts. J Invertebr Pathol. 2017;150:82-87.   DOI
77 Alexopoulos CJ, Mims CW, Blackwell M. Introductory mycology. 4th ed. Hoboken (NJ): John Wiley & Sons, Inc.; 1996.
78 Park JM, You YH, Park JH, et al. Cutaneous microflora from geographically isolated groups of Bradysia agrestis, an insect vector of diverse plant pathogens. Mycobiology. 2017;45(3):160-171.   DOI
79 Masoudi A, Koprowski JL, Bhattarai UR, et al. Elevational distribution and morphological attributes of the entomopathogenic fungi from forests of the Qinling mountains in China. Appl Microbiol Biotechnol. 2017;102(3):1483-1499.   DOI
80 Pelizza SA, Schalamuk S, Simon MR, et al. Compatibility of chemical insecticides and entomopathogenic fungi for control of soybean defoliating pest, Rachiplusia nu. Rev Argent Microbiol. 2017;50(2):189-201.   DOI
81 FAO, United Nations. Standard operating procedure for soil organic carbon, Walkley-Black method (Titration and colorimetric method). Rome (Italy): Global Soil Laboratory; 2019.
82 Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-2461.   DOI
83 Karakkat BB, Hockemeyer K, Franchett M, et al. Data for designing two isothermal amplification assays for the detection of root-infecting fungi on cool-season turfgrasses. Data Brief. 2018;20:471-479.   DOI
84 Edgar RC, Haas BJ, Clemente JC, et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194-2200.   DOI
85 Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335-336.   DOI
86 Abarenkov K, Nilsson RH, Larsson KH, et al. The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol. 2010;186:281-285.   DOI
87 Heck KL, van Belle G, Simberloff D. Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology. 1975;56(6):1459-1461.   DOI