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Journal of Integrative Agriculture  2023, Vol. 22 Issue (8): 2412-2425    DOI: 10.1016/j.jia.2023.01.006
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Host niche, genotype, and field location shape the diversity and composition of the soybean microbiome

YANG Hong-jun1, 2, 3, YE Wen-wu1, 2#, YU Ze1, 2, SHEN Wei-liang4, LI Su-zhen5, WANG Xing6, CHEN Jia-jia1, 2, 7, WANG Yuan-chao1, 2, ZHENG Xiao-bo1, 2

1 Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, P.R.China

2 Key Laboratory of Soybean Disease and Pest Control of Ministry of Agriculture and Rural Affairs, Nanjing Agricultural University, Nanjing 210095, P.R.China

3 College of Agronomy and Horticulture, Jiangsu Vocational College of Agriculture and Forestry, Zhenjiang 212400, P.R.China

4 Suzhou Academy of Agricultural Sciences, Suzhou 234000, P.R.China

5 Jining Academy of Agricultural Sciences, Jining 272131, P.R.China

6 Xuzhou Academy of Agricultural Sciences, Xuzhou 221131, P.R.China

7 College of Landscape Architecture, Jiangsu Vocational College of Agriculture and Forestry, Zhenjiang 212400, P.R.China

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摘要  内生微生物可以帮助植物获得营养物质,抑制病原菌等生物和非生物胁迫,是影响植物生长、营养和健康的关键因素之一;然而,对于田间条件下存在于大豆不同组织中的细菌和真菌微生物群落的组成及影响因素,仍缺乏足够的了解。本研究以大豆为研究对象,对16S rRNA和ITS特定区段的PCR扩增子进行高通量测序,探究不同组织(根、茎、叶和荚)、不同品种(安豆203、荷豆12、山宁16和中黄13)以及不同地理位置(济宁、宿州和徐州)对大豆内生细菌和真菌群落组成及多样性的影响。结果表明,不同组织之间的内生微生物群落差异明显,根部内生细菌和真菌群落的组成及多样性显著区分于地上部的茎、叶和荚;供试品种间茎部的细菌群落和叶部的真菌群落组成差异最大;试验地点显著影响各个器官中的细菌群落组成,其中对根茎部的影响比叶荚部更强,而对于真菌群落组成,茎叶部所受影响比根荚部更明显。此外,与大豆病害相关的微生物丰度在不同组织和品种间存在差异(如:镰刀菌在根部丰度更高,而链格孢菌在叶部丰度更高),可能与这些微生物在寄主中的生态位以及寄主的抗感性有关。微生物群落组成与多样性的系统分析将有助于植物保护技术的发展,从而有益于大豆健康。

Abstract  Plant-associated microbes represent a key determinant of plant fitness through acquiring nutrients, promoting growth, and resisting to abiotic and biotic stresses.  However, an extensive characterization of the bacterial and fungal microbiomes present in different plant compartments of soybean in field conditions has remained elusive.  In this study, we investigated the effects of four niches (roots, stems, leaves, and pods), four genotypes (Andou 203, Hedou 12, Sanning 16, and Zhonghuang 13), and three field locations (Jining, Suzhou, and Xuzhou) on the diversity and composition of bacterial and fungal communities in soybean using 16S and internal transcribed spacer rRNA amplicon sequencing, respectively.  The soybean microbiome significantly differed across organs.  Host genotypes explained more variation in stem bacterial community composition and leaf fungal community composition.  Field location significantly affected the composition of bacterial communities in all compartments and the effects were stronger in the root and stem than in the leaf and pod, whereas field location explained more variation in stem and leaf fungal community composition than in the root and pod.  The relative abundances of potential soybean fungal pathogens also differed among host organs and genotypes, reflecting the niches of these microbes in the host and probably their compatibility to the host genotypes.  Systematic profiling of the microbiome composition and diversity will aid the development of plant protection technologies to benefit soybean health.  
Keywords:  microbiome soybean        plant pathogen       endophytes       host niche       genotype       field  
Received: 18 August 2022   Accepted: 05 December 2022
Fund: This work was supported by grants from the earmarked fund for China Agriculture Research System (CARS-004-PS14), the National Key R&D Program of China (2018YFD0201000), and the Special Fund for Agro-scientific Research in the Public Interest, China (201303018).
About author:  YANG Hong-jun, E-mail: hjyang@jsafc.edu.cn; #Correspondence YE Wen-wu, E-mail: yeww@njau.edu.cn

Cite this article: 

YANG Hong-jun, YE Wen-wu, YU Ze, SHEN Wei-liang, LI Su-zhen, WANG Xing, CHEN Jia-jia, WANG Yuan-chao, ZHENG Xiao-bo. 2023. Host niche, genotype, and field location shape the diversity and composition of the soybean microbiome. Journal of Integrative Agriculture, 22(8): 2412-2425.

Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M. 2017. Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proceedings of the National Academy of Sciences of the United States of America114, E9403–E9412.

de Almeida Lopes K B, Carpentieri-Pipolo V, Oro T H, Stefani Pagliosa E, Degrassi G. 2016. Culturable endophytic bacterial communities associated with field-grown soybean. Journal of Applied Microbiology120, 740–755.

Bai L, Cui J, Jie W, Cai B. 2015. Analysis of the community compositions of rhizosphere fungi in soybeans continuous cropping fields. Microbiological Research180, 49–56.

Beckers B, Op De Beeck M, Weyens N, Boerjan W, Vangronsveld J. 2017. Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome5, 25.

Berendsen R L, Pieterse C M, Bakker P A. 2012. The rhizosphere microbiome and plant health. Trends in Plant Science17, 478–486.

Bulgarelli D, Rott M, Schlaeppi K, Themaat E V L V, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner F O, Amann R, Eickhorst T, Schulze-Lefert P. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature488, 91–95.

Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P. 2013. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology64, 807–838.

Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Lozupone C A, Turnbaugh P J, Fierer N, Knight R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America108, 4516–4522.

Carrión V J, Perez-Jaramillo J, Cordovez V, Tracanna V, Raaijmakers J M. 2019. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science366, 606–612.

Chen S, Zhou Y, Chen Y, Gu J. 2018. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics34, i884–i890.

Chesneau G, Torres-Cortes G, Briand M, Darrasse A, Preveaux A, Marais C, Jacques M A, Shade A, Barret M. 2020. Temporal dynamics of bacterial communities during seed development and maturation. FEMS Microbiology Ecology96, 12.

Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez L P, Tringe S G. 2016. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. The New Phytologist209, 798–811.

Cregger M A, Veach A M, Yang Z K, Crouch M J, Vilgalys R, Tuskan G A, Schadt C W. 2018. The Populus holobiont: Dissecting the effects of plant niches and genotype on the microbiome. Microbiome6, 31.

Kuklinsky-Sobral J, Araújo W L, Mendes R, Geraldi I O, Pizzirani-Kleiner A A, Azevedo J L. 2004. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environmental Microbiology6, 12.

Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods10, 996–998.

Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics27, 2194–2200.

Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty N K, Bhatnagar S, Eisen J A, Sundaresan V. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America112, E911–E920.

Fernandes E G, Pereira O L, da Silva C C, Bento C B, de Queiroz M V. 2015. Diversity of endophytic fungi in Glycine maxMicrobiological Research181, 84–92.

Friesen M L, Porter S S, Stark S C, Von Wettberg E J, Sachs J L, Martinez-Romero E. 2011. Microbially mediated plant functional traits. Annual Review of Ecology Evolution and Systematics, 42, 23–46.

Gdanetz K, Noel Z, Trail F. 2021. Influence of plant host and organ, management strategy, and spore traits on microbiome composition. Phytobiomes Journal5, 202–219.

Hacquard S, Schadt C W. 2015. Towards a holistic understanding of the beneficial interactions across the Populus microbiome. The New phytologist205, 1424–1430.

Hirooka Y, Kawaradani M, Sato T. 2014. Description of Gibellulopsis chrysanthemi sp. nov. from leaves of garland chrysanthemum. Mycological Progress13, 13–19.

Impullitti A E, Malvick D K. 2013. Fungal endophyte diversity in soybean. Journal of Applied Microbiology114, 1500–1506.

Khare E, Mishra J, Arora N K. 2018. Multifaceted interactions between endophytes and plant: developments and prospects. Frontiers in Microbiology9, 2732.

Kõljalg U, Nilsson R H, Abarenkov K, Tedersoo L, Taylor A F, Bahram M, Bates S T, Bruns T D, Bengtsson-Palme J, Callaghan T M, Douglas B, Drenkhan T, Eberhardt U, Duenas M, Grebenc T, Griffith G W, Hartmann M, Kirk P M, Kohout P, Larsson E, et al. 2013. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology22, 5271–5277.

Kosma D K, Jenks M A. 2007. Eco-physiological and molecular genetic determinants of plant cuticle function in drought and salt stress tolerance. In: Jenks M A, Hasegawa P M, Jain S M, eds., Advances in Molecular-Breeding toward Drought and Salt Tolerant Crops. Springer Publishing, Inc., Netherlands. pp. 91–120.

Kumar S, Kumar P. 2017. Effect of date of sowing and varieties on severity of Alternaria leaf spot, rust and yield in soybean (Glycine max L. Merrill). Bulletin of EnvironmentPharmacology and Life Sciences6, 448–451.

Langille M G, Zaneveld J, Caporaso J G, McDonald D, Knights D, Reyes J A, Clemente J C, Burkepile D E, Vega Thurber R L, Knight R, Beiko R G, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology31, 814–821.

Lindow S E, Leveau J H J. 2002. Phyllosphere microbiology. Current Opinion in Biotechnology13, 238–243.

Longley R, Noel Z A, Benucci G M N, Chilvers M I, Trail F, Bonito G. 2020. Crop management impacts the soybean (Glycine max) microbiome. Frontiers in Microbiology11, 1116.

Lu C, Zhang H, Wang Y, Zheng X. 2015. Rapid diagnosis of Fusarium root rot in soybean caused by Fusarium equiseti or Fusarium graminearum using loop-mediated isothermal amplification (LAMP) assays. Australasian Plant Pathology44, 437–443.

Lundberg D S, Lebeis S L, Paredes S H, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio T G, Edgar R C, Eickhorst T, Ley R E, Hugenholtz P, Tringe S G, Dangl J L. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature Reviews Microbiology488, 86–90.

Maarastawi S A, Frindte K, Linnartz M, Knief C. 2018. Crop rotation and straw application impact microbial communities in Italian and Philippine soils and the rhizosphere of Zea maysFrontiers in Microbiology9, 1295.

Magoc T, Salzberg S L. 2011. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics27, 2957–2963.

Marques J M, da Silva T F, Vollú R E, de Lacerda J R M, Blank A F, Smalla K, Seldin L. 2015. Bacterial endophytes of sweet potato tuberous roots affected by the plant genotype and growth stage. Applied Soil Ecology96, 273–281.

McGuire K L, Payne S G, Palmer M I, Gillikin C M, Keefe D, Kim S J, Gedallovich S M, Discenza J, Rangamannar R, Koshner J A, Massmann A L, Orazi G, Essene A, Leff J W, Fierer N. 2013. Digging the New York City Skyline: soil fungal communities in green roofs and city parks. PLoS ONE8, e58020.

Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der Voort M, Schneider J H M, Piceno Y M, Desantis T Z, Andersen G L, Bakker P A H M, Raaijmakers J M. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science332, 1097–1100.

Moroenyane I, Mendes L, Tremblay J, Tripathi B, Yergeau E. 2021a. Plant compartments and developmental stages modulate the balance between niche-based and neutral processes in soybean microbiome. Microbial Ecology82, 416–428.

Moroenyane I, Tremblay J, Yergeau É. 2021b. Soybean microbiome recovery after disruption is modulated by the seed and not the soil microbiome. Phytobiomes, 5, 418–431.

Moroenyane I, Tremblay J, Yergeau E. 2021c. Temporal and spatial interactions modulate the soybean microbiome. FEMS Microbiology Ecology8, 97.

Nguyen N H, Song Z, Bates S T, Branco S, Tedersoo L, Menke J, Schilling J S, Kennedy P G. 2016. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology20, 241–248.

Ottesen A R, Peña A G, White J R, Pettengill J B, Li C, Allard S, Strain E. 2013. Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiology13, 114.

Peiffer J A, Spor A, Koren O, Jin Z, Tringe S G, Dangl J L, Buckler E S, Ley R E. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America110, 6548–6553.

Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C. 2015. Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biology and Fertility of Soils51, 403–415.

Pimentel I C, Glienke-Blanco C, Gabardo J, Stuart R M, Azevedo J L. 2006. Identification and colonization of endophytic fungi from soybean (Glycine max (L.) Merril) under different environmental conditions. Brazilian Archives of Biology and Technology49, 705–711.

Pinto C, Pinho D, Sousa S, Pinheiro M, Egas C, Gomes A C. 2014. Unravelling the diversity of grapevine microbiome. PLoS ONE16, 9.

Potshangbam M, Devi S I, Sahoo D, Strobel G A. 2017. Functional characterization of endophytic fungal community associated with Oryza sativa L. and Zea mays L. Frontiers in Microbiology8, 325.

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner F O. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research41, D590–D596.

Ritpitakphong U, Falquet L, Vimoltust A, Berger A, Metraux J P, L’Haridon F. 2016. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. The New Phytologist210, 1033–1043.

Rodríguez-Blanco A, Sicardi M, Frioni L. 2015. Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biology and Fertility of Soils51, 391–402.

Rogerio F, Ciampi-Guillardi M, Barbieri M C, Braganca C A, Seixas C D, Almeida A M, Massola Jr N S. 2017. Phylogeny and variability of Colletotrichum truncatum associated with soybean anthracnose in Brazil. Journal of Applied Microbiology122, 402–415.

Santos-Medellin C, Edwards J, Liechty Z, Nguyen B, Sundaresan V. 2017. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio8, 4.

Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda Mdel C, Glick B R. 2016. Plant growth-promoting bacterial endophytes. Microbiological Research183, 92–99.

Schlaeppi K, Dombrowski N, Oter R G, van Themaat E V L, Schulze-Lefert P. 2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proceedings of the National Academy of Sciences of the United States of America111, 585–592.

Toju H, Kishida O, Katayama N, Takagi K. 2016. Networks depicting the fine-scale co-occurrences of fungi in soil horizons. PLoS ONE11, e0165987.

Turner T R, James E K, Poole P S. 2013. The plant microbiome. Genome Biology14, 1–10.

Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A. 2015. The importance of the microbiome of the plant holobiont. The New Phytologist206, 1196–1206.

Vorholt J A. 2012. Microbial life in the phyllosphere. Nature Reviews Microbiology10, 828–840.

Wagner M R, Lundberg D S, Del Rio T G, Tringe S G, Dangl J L, Mitchell-Olds T. 2016. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nature Communications7, 12151.

Xiong W, Li R, Ren Y, Liu C, Zhao Q, Wu H, Jousset A, Shen Q. 2017. Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biology and Biochemistry107, 198–207.

Yang H, Ma J, Rong Z, Zeng D, Wang Y, Hu S, Ye W, Zheng X. 2019. Wheat straw return influences nitrogen-cycling and pathogen associated soil microbiota in a wheat–soybean rotation system. Frontiers in Microbiology10, 1811.

Yang H, Ye W, Ma J, Zeng D, Rong Z, Xu M, Wang Y, Zheng X. 2018. Endophytic fungal communities associated with field-grown soybean roots and seeds in the Huang-Huai region of China. PeerJ6, e4713.

Yang H C, Haudenshield J S, Hartman G L. 2014. Colletotrichum incanum sp. nov., a curved-conidial species causing soybean anthracnose in USA. Mycologia106, 32–42.

Yang S, Wang Y, Liu R, Xing L, Yang Z. 2018. Improved crop yield and reduced nitrate nitrogen leaching with straw return in a rice–wheat rotation of Ningxia irrigation district. Scientific Reports8, 9458.

de Zelicourt A, Al-Yousif M, Hirt H. 2013. Rhizosphere microbes as essential partners for plant stress tolerance. Molecular Plant6, 242–245.

Zhou G, Qiu X, Chen L, Zhang C, Ma D, Zhang J. 2019. Succession of organics metabolic function of bacterial community in response to addition of earthworm casts and zeolite in maize straw composting. Bioresource Technology280, 229–238.

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