Abstract
Background
Casuarina equisetifolia is one of the most important artificially planted protective forests along the coast in southern China for windbreaks, soil erosion, and sand dune stabilization. Self-renewing of C. equisetifolia is very limited, which might be caused by low soil nutrient levels and reduced microbial activity.
Methods
Use of high-throughput sequencing of the 18S rDNA to investigate the microbial communities from the rhizosphere and root endosphere of C. equisetifolia in young-aged, intermediate-aged, and mature-aged forests.
Results
Our results indicate that the diversity of rhizosphere fungal microbiomes in field-grown C. equisetifolia is much lower than that of the endosphere microbiomes. Bioinformatic analysis showed that rhizocompartments produce the strongest differentiation of rhizosphere and endosphere communities. Notably, the distribution of rhizosphere fungi communities was significantly influenced by the environmental factors, not by forest ages.
Conclusions
The presented study suggests that the rhizocompartments and environmental factors, rather than forest ages, determine the diversities of fungal community.
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References
Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. https://doi.org/10.1146/annurev-arplant-050312-120106
Bakker PAHM, Berendsen RL, Doornbos RF, Wintermans PCA, Pieterse CMJ (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4:165. https://doi.org/10.3389/fpls.2013.00165
Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209. https://doi.org/10.1186/gb-2013-14-6-209
Tkacz A, Cheema J, Chandra G, Grant A, Poole PS (2015) Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition. ISME J 9:2349–2359. https://doi.org/10.1038/ismej.2015.41
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Mendes R, Kruijt M, Ide B, Dekkers E et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100. https://doi.org/10.1126/science.1203980
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low nutrient environments. Plant Soil 245:35–47. https://doi.org/10.1023/A:1020809400075
Raaijmakers JM, Paulitz TC, Steinberg C (2009) Alabouvette, C., Moënne-Loccoz, Y. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil. 321:341–361. https://doi.org/10.1007/s11104-008-9568-6
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. https://doi.org/10.1038/nrmicro3109
Peiffer JA, Spor A, Koren O et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. PNAS 110:6548–6553. https://doi.org/10.1073/pnas.1302837110
Xiao X, Chen WM, Zong L, Yang J, Jiao S, Lin YB, Wang ET, Wei GH.(2016)Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments. Mol Ecol 26(6). https://doi.org/10.1111/mec.14027
Chen XY, Lin P (2002) Mating system and inbreeding retrogression of Casuarina equisetifolia plantation, an introduced species in Xiamen. J Appl Ecol 13:1377–1380. https://doi.org/10.13287/j.1001-9332.2002.0317
Zhu R (2005) Summarize on woodland soil principal genes of influencing Casuarina equisetifolia protection forest growth. Sci Technol Qinghai Agric For 4:23–24
Liu KX, Hao QY, Zhong QX (2009) Investigation and comparative analysis on coastal shelterbelt of Wenchang and Wanning in Hainan province. Prot For. Sci Technol 27:12–15. https://doi.org/10.13601/j.issn.1005-5215.2009.05.033
Yang ZY, Xue Y, Liu XZ, Wang XY, Lin ZP (2014) Additivity in tree biomass models of Casuarina equisetifolia in Hainan province. J Northeast Fore Univ 43:36–40. https://doi.org/10.13759/j.cnki.dlxb.20141226.027
Zhang Y, Zhong CL, Chen Y, Chen Z (2006) The advance of casuarina symbiotic microbe research. Guangdong For Sci Technol 22:70–74. https://doi.org/10.3969/j.issn.1006-4427.2006.01.018
Lin YQ, Wu CZ, Xie AQ, Lin H, Li J, Hong T, Hong W (2015) Isolation of endophytic fungi from Casuarina equisetifolia and screening of promoting strains. J BeiHua Univ 16:522–528. https://doi.org/10.11713/j.issn.1009-4822.2015.04.027
Wang X, Li HM, Cao TT, Gu MZ, Chen Y, Feng L, Li L (2017) The diversity of soil fungi and allelopathic potentials of special fungal metabolites in Casuarina equisetifolia woodlands of different stand ages. Chin J Appl Environ Biol 23:670–677. https://doi.org/10.3724/SP.J.1145.2016.08023
Huang R, Jin SK, Wang X, Xu ZX, Li HM, Li L (2018) Allelopathic potential of root endophytic fungal metabolites of Casuarina equisetifolia. Allelopathy J 45:213–228. https://doi.org/10.26651/allelo.j/2018-45-2-1188
Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M, Karpinets T, Schadt W et al (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77:5934–5944. https://doi.org/10.1128/AEM.05255-11
Gang GH, Cho G, Kwak YS, Park EH (2017) Distribution of rhizosphere and endosphere fungi on the first-class endangered plant Cypripedium japonicum. Mycobiology 45:97–100. https://doi.org/10.5941/MYCO.2017.45.2.97
Rojas C, Gutierrez RM, Bruns MA (2016) Bacterial and eukaryal diversity in soils forming from acid mine drainage precipitates under reclaimed vegetation and biological crusts. Appl Soil Ecol 105:57–66. https://doi.org/10.1016/j.apsoil.2016.03.012
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Update on root exudation and rhizosphere biology: root exudation and rhizosphere biology. Plant Physiol 2003(132):44–51. https://doi.org/10.1104/pp.102.019661
Lugtenberg BJJ, Dekkers LC, Minireview (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1:9–13. https://doi.org/10.1046/j.1462-2920.1999.00005.x
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. https://doi.org/10.1016/j.soilbio.2009.11.024
Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252:169–175. https://doi.org/10.1023/A:1024106605806
Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914. https://doi.org/10.1177/0095244305054674
Shakya M, Gottel N, Castro H, Yang ZK, Labbé J et al (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One 8:e76382. https://doi.org/10.1371/journal.pone.0076382
Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S, van der Lelie D, Gilbert JA (2015) The soil microbiome influences grapevine-associated microbiota. MBio 6:e02527–e02514. https://doi.org/10.1128/mBio.02527-14
Chen F, Yang B, Ma J, Hou H, Zhang S (2016) Effects of CO2 geological storage leakage on soil microbial community. J China Univ Min Technol 45(1285–1293):1299. https://doi.org/10.13247/j.cnki.jcumt.000527
Chen X, Wang F, Yan J, Liu Y, Tan H, Zhou Y (2016) Effect of coversoil thickness on diurnal variation characteristics of reclaimed soil respiration in coal mining areas. J China Univ Min Technol 45:164–169. https://doi.org/10.13247/j.cnki.jcumt.000462
Mu SG, Dong JH, Hui W, Hua Z, Bian ZF (2007) Study of reclaimed soil respiration on the site by filling mining wastes and fly ash into subsidence area due to coal mining. J China Univ Min Technol 36:663–668 1000-1964(2007)05-0663-06
Bouchez T, Blieux AL, Dequiedt S, Domaizon I, Dufresne A, Ferreira S, Godon JJ, Hellal J, Joulian C, Quaiser A, Martin-Laurent F, Mauffret A, Monier JM, Peyret P, Schmitt-Koplin P, Sibourg O, D’oiron E, Bispo A, Deportes I, Grand C, Cuny P, Maron PA, Ranjard L (2016) Molecular microbiology methods for environmental diagnosis. Environ Chem Lett 14:423–441. https://doi.org/10.1007/s10311-016-0581-3
Bachmann G, Kinzel H (1992) Physiological and ecological aspects of the interactions between plant-roots and rhizosphere soil. Soil Biol Biochem 24:543–552. https://doi.org/10.1016/0038-0717(92)90079-D
Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152. https://doi.org/10.1007/s11104-008-9885-9
Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manag 309:19–27. https://doi.org/10.1016/j.foreco.2013.02.034
Thoms C, Gleixner G (2013) Seasonal differences in tree species’ influence on soil microbial communities. Soil Biol Biochem 66:239–248. https://doi.org/10.1016/j.soilbio.2013.05.018
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil ph as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. https://doi.org/10.1128/AEM.00335-09
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a ph gradient in an arable soil. ISME J. 4:1340–1351. https://doi.org/10.1038/ismej.2010.58
Li XR, Bai LJ, Chen BL, Lan HK, Fu CD, Li L (2014) Analysis of soil physicochemical properties and biological activity of the Casuarina equisetifolia forests with different ages. J Northwest For Univ 29:37–41. https://doi.org/10.3969/j.issn.1001-7461
Wang MY, Liu Q, Ding YF, Fu SZ, Ye ZL, Feng TS (2008) Nutrients and litter decomposition in Vatica mangachapoi forest versus Casuarina equisetifolia plantation. J Zhejiang For Coll 25:597–603
West TO, Post WM (2002) Soil organic carbon sequestration rates by tillage and crop rotation. Soil Sci Soc Am J 66:1930–1946. https://doi.org/10.2136/sssaj2002.1930
Tian Z, Wu XQ, Dai EF, Zhao DS (2016) SOC storage and potential of grasslands from 2000 to 2012 in central and eastern Inner Mongolia, China. J Arid Land 8:364–374. https://doi.org/10.1007/s40333-016-0041-8
Carter MR (1986) Microbial biomass as an index for tillage-induced changes in soil biological properties. Soil Tillage Res 7:29–40. https://doi.org/10.1016/0167-1987(86)90005-X
Bastida F, Selevsek N, Torres IF, Hernández T, García C (2015) Soil restoration with organic amendments: linking cellular functionality and ecosystem processes. Sci Rep 5:15550. https://doi.org/10.1038/srep15550
Acknowledgments
We thank Dr. Xiang Jin from the College of Life Sciences, Hainan Normal University, for the kind advices on processing the data and manuscript writing.
Funding
This research was funded by the Hainan Provincial Natural Science Foundation of China (2018CXTD337).
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Huang, R., Chen, P., Wang, X. et al. Structural variability and niche differentiation of the rhizosphere and endosphere fungal microbiome of Casuarina equisetifolia at different ages. Braz J Microbiol 51, 1873–1884 (2020). https://doi.org/10.1007/s42770-020-00337-7
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DOI: https://doi.org/10.1007/s42770-020-00337-7