Analysis of bacterial and fungal community composition and soil enzyme activities in the rhizosphere of transgenic Betula platyphylla

doi:10.12302/j.issn.1000-2006.202208001

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2024, Vol. 48 ›› Issue (6): 129-137.doi: 10.12302/j.issn.1000-2006.202208001

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Analysis of bacterial and fungal community composition and soil enzyme activities in the rhizosphere of transgenic Betula platyphylla

CAO Li¹(), JIN Dongxue¹, JIANG Jing¹, LI Tianfang²^,^*()

1. State Key Laboratory of Forest Genetics and Breeding,Northeast Forestry University,Harbin 150040,China
2. Heilongjiang Academy of Forestry, Harbin 150081, China

Received:2022-08-01 Revised:2023-03-19 Online:2024-11-30 Published:2024-12-10
Contact: LI Tianfang E-mail:cl08182022@163.com;18646079568@126.com

Abstract

Abstract:

【Objective】The BpGLK transcription factor of Betula platyphylla is involved in regulating chloroplast development and leaf color. The leaf color of B. platyphylla with inhibited BpGLK expression is yellow-green during the growth period, which holds great ornamental value in landscaping. However, as a genetically modified crop, concerns exist regarding the potential adverse environmental effects of widespread use. This study aims to examine the impact of transgenic BpGLK B. platyphylla on soil enzyme activity and the composition of rhizosphere soil bacterial and fungal communities, providing theoretical data for future environmental release and commercialization.【Method】Three-year-old transgenic B. platyphylla (OE and RE strains) and wild-type (WT) B. platyphylla are used as materials. Soil sucrase, urease, neutral protease, catalase, and cellulase activities were measured using the spectrophotometric method. In addition, 16S rRNA and ITS sequencing analyses of rhizosphere soil microorganisms were conducted using the Illumina-Miseq high-throughput sequencing platform. The richness and diversity of bacterial and fungal communities, structural differences, and community composition in rhizosphere soil were analyzed to understand the effects of transgenic activity on soil enzyme activity and microbial composition in the rhizosphere soil of B. platyphylla.【Result】Significant differences (P < 0.05) are observed in soil urease, sucrase, cellulase and neutral protease activities between BpGLK-transformed B. platyphylla and WT strains at four time points (June 15, July 15, August 15 and September 15). However, catalase activity showed significant differences between WT and some transgenic strains. Soil urease and cellulase activities decrease significantly in mid-August and mid-September. The activity of soil neutral protease in OE strains was higher than that of the WT strain at all four periods (P < 0.05). At the rhizosphere bacterial community level, Burkholderia, a growth-promoting function, was the dominant genus in transgenic and WT strains. The relative abundance of Burkholderia in the rhizosphere soil of transgenic strains significantly increased. At the rhizosphere fungal community level, Tomentella dominated the rhizosphere of transgenic RE strains, while Clavulina dominated the rhizosphere of WT and OE strains. The relative abundance of Laccaria was significantly lower in OE and RE strains (P < 0.05). The Observed, Chao1, Shannon and Simpson indices of transgenic B. platyphylla did not differ significantly from those of WT strains, while the community abundance and diversity of RE strains were significantly higher than those of WT strains. The difference between OE and WT strains was not significant. Venn diagram analysis revealed significant differences in ASV composition between transgenic and WT strains. In contrast, principal component analysis showed slight differences in community composition between RE and WT strains, while the difference between OE and WT strains was relatively larger. However, the difference between OE and WT strains remainsed smaller than that between RE and WT strains.【Conclusion】The results indicated that the introduction of the exogenous BpGLK gene had a specific effect on the abundance and diversity of rhizosphere bacterial and fungal communities in B. platyphylla. These changes can promote plant growth and enhance resistance. However, whether these effects persist over the long term remains to be confirmed in future experiments.

Key words: birch(Betula platyphylla), transgenic, soil enzyme activities, rhizosphere, bacteria, fungi, community composition

CLC Number:

S718
S68

CAO Li, JIN Dongxue, JIANG Jing, LI Tianfang. Analysis of bacterial and fungal community composition and soil enzyme activities in the rhizosphere of transgenic Betula platyphylla[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(6): 129-137.

Figures/Tables 6

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References 43

[1]	李天芳, 姜静, 杨传平, 等. 我国白桦育种研究概况[J]. 江苏林业科技, 2008, 35(2):47-49.
	LI T F, JIANG J, YANG C P, et al. Status of breeding research on Betula platyphylla in China[J]. J Jiangsu For Sci Technol, 2008, 35(2):47-49.DOI: 10.3969/j.issn.1001-7380.2008.02.013.
[2]	MERLE J. A second gene producing golden plant color in maize[J]. American Naturalist, 1926, 60(670):484-488.
[3]	ROSSINI L, CRIBB L, MARTIN D J, et al. The maize golden2 gene defines a novel class of transcriptional regulators in plants[J]. Plant Cell, 2001, 13(5):1231-1244.DOI: 10.1105/tpc.13.5.1231.
[4]	NGUYEN C V, VREBALOV J T, GAPPER N E, et al. Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening[J]. Plant Cell, 2014, 26(2):585-601.DOI: 10.1105/tpc.113.118794.
[5]	KOBAYASHI K, SASAKI D, NOGUCHI K, et al. Photosynthesis of root chloroplasts developed in Arabidopsis lines overexpressing GOLDEN2-LIKE transcription factors[J]. Plant Cell Physiol, 2013, 54(8):1365-1377.DOI: 10.1093/pcp/pct086.
[6]	CHEN M, JI M L, WEN B B, et al. GOLDEN 2-LIKE transcription factors of plants[J]. Front Plant Sci, 2016,7:1509.DOI: 10.3389/fpls.2016.01509.
[7]	HAN X Y, LI P X, ZOU L J, et al. GOLDEN2-LIKE transcription factors coordinate the tolerance to Cucumber mosaic virus in Arabidopsis[J]. Biochem Biophys Res Commun, 2016, 477(4):626-632.DOI: 10.1016/j.bbrc.2016.06.110.
[8]	GANG H X, LIU G F, CHEN S, et al. Physiological and transcriptome analysis of a yellow-green leaf mutant in birch (Betula platyphylla × B.pendula)[J]. Forests, 2019, 10(2):120.DOI: 10.3390/f10020120.
[9]	陆雅海, 张福锁. 根际微生物研究进展[J]. 土壤, 2006, 38(2):113-121.
	LU Y H, ZHANG F S. The advances in rhizosphere microbiology[J]. Soils, 2006, 38(2):113-121.DOI: 10.3321/j.issn:0253-9829.2006.02.001.
[10]	GUO Q, LU N, LUO Z J, et al. An assessment of the environmental impacts of transgenic triploid Populus tomentosa in field condition[J]. Forests, 2018, 9(8):482.DOI: 10.3390/f9080482.
[11]	侯英杰, 苏晓华, 焦如珍, 等. 转基因银腺杂种杨对土壤微生物的影响[J]. 林业科学, 2009, 45(5):148-153.
	HOU Y J, SU X H, JIAO R Z, et al. Effects of transgenic Populus alba × P.glandulosa on soil microorganism[J]. Sci Silvae Sin, 2009, 45(5):148-153.DOI: 10.3321/j.issn:1001-7488.2009.05.023.
[12]	吕秀华. 转基因银中杨ABJ系列对土壤微生物类群的影响[J]. 基因组学与应用生物学, 2017, 36(5):1991-1996.
	LYU X H. The impact of transgenic poplar (ABJ series) on soil microorganism group[J]. Genom Appl Biol, 2017, 36(5):1991-1996.DOI: 10.13417/j.gab.036.001991.
[13]	吕秀华. 转基因银中杨对根际土壤微生物的影响[J]. 基因组学与应用生物学, 2018, 37(5):1965-1970.
	LYU X H. The impact of transgenic poplar on soil microorganism group[J]. Genom Appl Biol, 2018, 37(5):1965-1970.DOI: 10.13417/j.gab.037.001965.
[14]	孙伟博, 魏朝琼, 马晓星, 等. 3类转基因南林895杨田间试验的安全性评估[J]. 林业科学, 2020, 56(10):53-62.
	SUN W B, WEI Z Q, MA X X, et al. Safety assessment of a field trial of three types of transgenic poplar Nanlin895[J]. Sci Silvae Sin, 2020, 56(10):53-62.DOI: 10.11707/j.1001-7488.20201006.
[15]	周培军, 李玲玲, 李红岩, 等. 转Bt基因‘南林895’杨时空表达及生物安全分析[J]. 分子植物育种, 2022, 20(5):1568-1580.
	ZHOU P J, LI L L, LI H Y, et al. Spatio-temporal expression and biosafety analysis of transgenic ‘Nanlin 895’ poplar with Bt[J]. Molecular Plant Breeding, 2022, 20(5): 1568-1580.
[16]	FAN J M, DONG Y, YU X Y, et al. Assessment of environmental microbial effects of insect-resistant transgenic Populus × Euramericana cv.‘74/76’ based on high-throughput sequencing[J]. Acta Physiol Plant, 2020, 42(11):167.DOI: 10.1007/s11738-020-03148-3.
[17]	王阳, 王伟, 姜静, 等. 转基因小黑杨根际土壤微生物群落特征研究[J]. 南京林业大学学报(自然科学版), 2023, 47(1):199-208.
	WANG Y, WANG W, JIANG J, et al. Diversity of microbial community in rhizosphere of genetically modified Populus simonii × P.nigra[J]. J Nanjing For Univ (Nat Sci Ed), 2023, 47(1):199-208.
[18]	CALLAHAN B J, MCMURDIE P J, ROSEN M J, et al. Dada 2:high-resolution sample inference from illumina amplicon dada[J]. Nature Methods, 2016, 13(7), 581-583.
[19]	戴伟, 白红英. 土壤过氧化氢酶活度及其动力学特征与土壤性质的关系[J]. 北京林业大学学报, 1995, 17(1):37-41.
	DAI W, BAI H Y. Correlations of soil catalase activity and it’s kinetic characteristic with some soil properties[J]. Journal of Beijing Forestry University, 1995, 17(1):37-41.
[20]	DICK R P, SANDOR J A, EASH N S. Soil enzyme activities after 1500 years of terrace agriculture in the Colca Valley,Peru[J]. Agric Ecosyst Environ, 1994, 50(2):123-131.DOI: 10.1016/0167-8809(94)90131-7.
[21]	林天, 何园球, 李成亮, 等. 红壤旱地中土壤酶对长期施肥的响应[J]. 土壤学报, 2005, 42(4):682-686.
	LIN T, HE Y Q, LI C L, et al. Response of soil enzymes to long-term fertilization in upland red soil[J]. Acta Pedol Sin, 2005, 42(4):682-686.DOI: 10.3321/j.issn:0564-3929.2005.04.022.
[22]	杨宁, 杨满元, 雷玉兰, 等. 衡阳紫色土丘陵坡地土壤酶活性对植被恢复的响应[J]. 生态环境学报, 2014, 23(4):575-580.
	YANG N, YANG M Y, LEI Y L, et al. Response of soil enzyme activities to re-vegetation on sloping-land with purple soils in Hengyang of Hunan Province,China[J]. Ecol Environ Sci, 2014, 23(4):575-580.DOI: 10.3969/j.issn.1674-5906.2014.04.005.
[23]	俞元春, 冷春龙, 舒洪岚, 等. 转基因抗虫棉对土壤养分和酶活性的影响[J]. 南京林业大学学报(自然科学版), 2011, 35(5):21-24.
	YU Y C, LENG C L, SHU H L, et al. Effects of insect-resistant transgenic cotton on soil nutrients and enzyme activities[J]. J Nanjing For Univ (Nat Sci Ed), 2011, 35(5):21-24.DOI: 10.3969/j.issn.1000-2006.2011.05.005.
[24]	DEFOREST J L. The influence of time,storage temperature,and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA[J]. Soil Biol Biochem, 2009, 41(6):1180-1186.DOI: 10.1016/j.soilbio.2009.02.029.
[25]	LUCAS-BORJA M E, HEDO J, CERDÁ A, et al. Unravelling the importance of forest age stand and forest structure driving microbiological soil properties,enzymatic activities and soil nutrients content in Mediterranean Spanish black pine(Pinus nigra Ar.ssp.salzmannii) forest[J]. Sci Total Environ, 2016, 562:145-154.DOI: 10.1016/j.scitotenv.2016.03.160.
[26]	冯翠莲, 万玥, 赵婷婷, 等. 抗虫转基因甘蔗对土壤酶活性的影响[J]. 热带生物学报, 2020, 11(1):1-6.
	FENG C L, WAN Y, ZHAO T T, et al. Effect of insect-resistant transgenic sugarcane on soil enzyme activities in the rhizosphere[J]. Journal of Tropical Biology, 2020, 11(1):1-6.DOI: 10.15886/j.cnki.rdswxb.2020.01.001.
[27]	WEN Z L, YANG M K, DU M H, et al. Enrichments/derichments of root-associated bacteria related to plant growth and nutrition caused by the growth of an EPSPS-transgenic maize line in the field[J]. Front Microbiol, 2019,10:1335.DOI: 10.3389/fmicb.2019.01335.
[28]	COENYE T, VANDAMME P. Diversity and significance of Burkholderia species occupying diverse ecological niches[J]. Environ Microbiol, 2003, 5(9):719-729.DOI: 10.1046/j.1462-2920.2003.00471.x.
[29]	SUÁREZ-MORENO Z R, CABALLERO-MELLADO J, COUTINHO B G, et al. Common features of environmental and potentially beneficial plant-associated Burkholderia[J]. Microb Ecol, 2012, 63(2):249-266.DOI: 10.1007/s00248-011-9929-1.
[30]	COMPANT S, NOWAK J, COENYE T, et al. Diversity and occurrence of Burkholderia spp. in the natural environment[J]. FEMS Microbiol Rev, 2008, 32(4):607-626.DOI: 10.1111/j.1574-6976.2008.00113.x.
[31]	张珂飞, 钟永嘉, 孙丽莉, 等. 植物有益伯克霍尔德氏菌的研究进展及其在农业中的应用[J]. 微生物学报, 2021, 61(8):2205-2218.
	ZHANG K F, ZHONG Y J, SUN L L, et al. Plant-associated beneficial Burkholderia[J]. Acta Microbiol Sin, 2021, 61(8):2205-2218.DOI: 10.13343/j.cnki.wsxb.20200562.
[32]	刘佳琦, 宋逸欣, 成星川, 等. 转BpGLK1基因白桦叶色变异规律及生长特性分析[J]. 江西农业学报, 2021, 33(8):17-23.
	LIU J Q, SONG Y X, CHENG X C, et al. Analysis of leaf color variation and growth characteristics of transgenic BpGLK1 brich[J]. Acta Agric Jiangxi, 2021, 33(8):17-23.DOI: 10.19386/j.cnki.jxnyxb.2021.08.004.
[33]	DE ROMAN M, CLAVERIA V, DE MIGUEL A M. A revision of the descriptions of ectomycorrhizas published since 1961[J]. Mycol Res, 2005, 109(Pt 10):1063-1104.DOI: 10.1017/s0953756205003564.
[34]	JAKUCS E, KOVÁCS G M, SZEDLAY G, et al. Morphological and molecular diversity and abundance of tomentelloid ectomycorrhizae in broad-leaved forests of the Hungarian Plain[J]. Mycorrhiza, 2005, 15(6):459-470.DOI: 10.1007/s00572-005-0351-8.
[35]	WALKER J F, MILLER O K Jr, HORTON J L. Hyperdiversity of ectomycorrhizal fungus assemblages on oak seedlings in mixed forests in the southern Appalachian Mountains[J]. Mol Ecol, 2005, 14(3):829-838.DOI: 10.1111/j.1365-294X.2005.02455.x.
[36]	HAUG I, WEISS M, HOMEIER J, et al. Russulaceae and Thelephoraceae form ectomycorrhizas with members of the Nyctaginaceae (Caryophyllales) in the tropical mountain rain forest of southern Ecuador[J]. New Phytol, 2005, 165(3):923-936.DOI: 10.1111/j.1469-8137.2004.01284.x.
[37]	JAKUCS E, EROS-HONTI Z. Morphological-anatomical characterization and identification of Tomentella ectomycorrhizas[J]. Mycorrhiza, 2008, 18(6/7):277-285.DOI: 10.1007/s00572-008-0183-4.
[38]	DAHLBERG A. Effect of soil humus cover on the establishment and development of mycorrhiza on containerised Pinus sylvestris and Pinus contorta ssp. Latifolia Engelm.after outplanting[J]. Scand J For Res, 1990, 5(1/2/3/4):103-112.
[39]	TROWBRIDGE J, JUMPPONEN A. Fungal colonization of shrub willow roots at the forefront of a receding glacier[J]. Mycorrhiza, 2004, 14(5):283-293.DOI: 10.1007/s00572-003-0264-3.
[40]	魏松坡, 宋怡静, 贾黎明, 等. 太行山片麻岩区栓皮栎外生菌根真菌多样性[J]. 菌物学报, 2018, 37(4):422-433.
	WEI S P, SONG Y J, JIA L M, et al. Diversity of ectomycorrhizal fungi associated with Quercus variabilis in gneissose area of Taihang Mountains[J]. Mycosystema, 2018, 37(4):422-433.DOI: 10.13346/j.mycosystema.170226.
[41]	杨岳, 闫伟, 魏杰. 黑里河和贺兰山自然保护区华北落叶松根区土壤中外生菌根真菌群落[J]. 菌物学报, 2019, 38(1):48-63.
	YANG Y, YAN W, WEI J. Ectomycorrhizal fungal community in the root zone soil of Larix gmelinii var. Principis-rupprechtii in Heilihe and Helanshan National Nature Reserve[J]. Mycosystema, 2019, 38(1):48-63.DOI: 10.13346/j.mycosystema.180153.
[42]	SMITH M E, HENKEL T W, CATHERINE AIME M, et al. Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest[J]. New Phytol, 2011, 192(3):699-712.DOI: 10.1111/j.1469-8137.2011.03844.x.
[43]	木兰. 白音敖包国家级自然保护区大型真菌资源调查兼中国蜡蘑属的分类学研究[D]. 长春: 吉林农业大学, 2015.
	MU L. Investigation on macrofungi resources in Baiyin Aobao National Nature Reserve and taxonomic study on Tricholoma in china[D]. Changchun: Jilin Agricultural University, 2015.

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微生物 microbial	样品 sample	可观测物种数 observed species	Chao1指数 Chao1 index	香农指数 Shannon index	辛普森指数 Simpson index	测序深度指数 coverage
细菌 bacteria	WT	4 868.37±170.75 a	5 491.06±122.26 a	10.51±0.14 a	0.997 6±0.000 3 a	0.985 7±0.000 4 ab
	OE1	4 107.43±537.31 a	4 724.57±559.73 a	9.47±0.51 b	0.989 6±0.004 7 a	0.998 59±0.00 1 ab
	OE2	4 743.73±94.58 a	5 363.12±109.37 a	9.95±0.19 ab	0.991 5±0.004 2 a	0.984 0±0.000 6 ab
	OE3	4 188.23±350.80 a	4 742.88±475.25 a	9.25±0.39 b	0.985 3±0.010 4 a	0.985 6±0.002 1 ab
	RE1	4 996.20±162.15 a	5 747.51±127.58 a	10.27±0.08 ab	0.996 5±0.000 8 a	0.982 2±0.000 2 b
	RE2	4 290.53±379.71 a	4 731.19±417.10 a	9.73±0.39 ab	0.990 4±0.004 8 a	0.986 9±0.001 7 a
	RE7	4 763.50±121.07 a	5 412.76±177.10 a	10.07±0.14 ab	0.994 6±0.001 0 a	0.983 9±0.000 8 ab
真菌 fungi	WT	256.10±26.30 bc	261.17±31.06 bc	2.68±0.31 bc	0.69±0.06 bc	0.999 7±0.000 2 a
	OE1	195.57±22.35 c	197.59±23.65 c	3.33±0.42 ab	0.82±0.06 ab	0.999 8±0.000 08 a
	OE2	262.75±33.45 bc	267.20±30.09 bc	1.89±0.01 c	0.42±0.04 d	0.999 7±0.000 12 a
	OE3	313.80±40.90 bc	319.76±37.89 bc	2.90±0.10 bc	0.63±0.10 c	0.999 7±0.000 07 a
	RE1	356.27±19.35 b	384.18±27.02 b	3.58±0.27 ab	0.82±0.02 ab	0.999 0±0.000 20 b
	RE2	488.43±3.00 a	515.52±3.72 a	4.39±0.23 a	0.87±0.02 a	0.999 1±0.000 14 b
	RE7	331.00±98.70 b	347.15±111.00 b	3.32±0.49 ab	0.77±0.04 ab	0.999 4±0.000 34 ab

Analysis of bacterial and fungal community composition and soil enzyme activities in the rhizosphere of transgenic Betula platyphylla

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