作物轮作系统对小麦根系微生物群落的影响

doi:10.1016/j.jia.2024.07.004

摘要/Abstract

摘要：

小麦-玉米（麦玉）和小麦-大豆（麦豆）轮作系统是我国华北平原的主要轮作制度，对国家农业生产及其可持续性具有重要影响。由于轮作方式对土壤健康和作物生产力具有遗留效应，轮作系统对后续作物根部微生物组的影响已成为土壤管理研究的重要方面之一。本研究调查了连续两年麦玉和麦豆轮作对后茬小麦生长阶段根部细菌群落的招募和筛选的影响。结果显示，细菌群落的多样性和组成主要受到小麦根系部位和发育阶段的影响，而轮作方式对小麦根部细菌群落的影响虽相对轻微但显著。在两年麦玉轮作后，小麦根际和根表的共现网络更为复杂，其中与纤维素分解相关的OTU具有更高的连接度；在两年麦豆轮作后，根际的共现网络相对简单但稳定，而根表和内生的共现网络更为复杂，其中与尿素分解和固氮相关的OTU具有更高的连接度。虽然随机和确定性过程都参与了小麦根系细菌群落的组装，但在麦豆轮作后，确定性过程的贡献比麦玉轮作高出19.4-38.5%，这表明大豆遗留效应对小麦根系微生物选择具有更为显著的影响。具有固氮、产生吲哚乙酸和抑制疾病潜力的有益菌，如Betaproteobacteriales、Azospirillales和Dyella sp.等，在小麦所有根系部位和发育阶段中被持续富集，且可作为小麦产量的重要预测因子。本研究阐明了轮作方式在调节作物根系细菌群落动态中的作用，为利用微生物组调控技术优化小麦生产和增强土壤健康提供基础。

Abstract:

Wheat–maize (WM) and wheat–soybean (WS) double-cropping rotation systems are predominant in the North China Plain, with implications for national agricultural output and sustainability. As rotation systems exert legacy effects on soil health and crop productivity, the role of crop rotation in shaping the root-associated microbiome of the succeeding crops has emerged as a pivotal aspect of crop management research. Here, the effects of the preceding two cycles of WM and WS rotations on the recruitment and filtering of wheat root-associated bacterial communities across wheat developmental stages were investigated. Our results revealed that bacterial community diversity and composition were primarily influenced by compartment and developmental stage, while the preceding rotation systems had a slight but significant effect on wheat root-associated bacterial communities. The co-occurrence networks under WM were more complex in the wheat rhizosphere and rhizoplane, with the operational taxonomic units (OTUs) related to cellulolysis showing greater connectivity. The co-occurrence networks under WS were simple but stable in the rhizosphere and complex in the rhizoplane and endosphere, with the OTUs related to ureolysis and nitrogen fixation showing greater connectivity. While both stochastic and deterministic processes contributed to the assembly of wheat root-associated bacterial communities, the contributions of deterministic processes under WS were 19.4–38.5% higher than those under the WM rotation across the root-associated compartments, indicating the substantial impact of a soybean legacy effect on wheat root selection of microbes. Plant growth-promoting rhizobacteria with the potential to fix nitrogen, produce indole-3-acetic acid, and inhibit diseases such as Betaproteobacteriales, Azospirillales and Dyella sp., were identified within the OTUs that were consistently enriched across all the wheat root-associated compartments and developmental stages, which were also important predictors of wheat yield. This study elucidates the role of crop rotation in modulating the dynamics of crop root-associated bacterial communities, and underscores the potential of targeted microbiome manipulation for optimizing wheat production and enhancing soil health.

Key words: crop rotation , root-associated bacterial community , co-occurrence network , assembly process , wheat yield

Shuting Yu, Tianshu Wang, Li Wang, Shuihong Yao, Bin Zhang. 作物轮作系统对小麦根系微生物群落的影响[J]. Journal of Integrative Agriculture, 2025, 24(2): 739-753.

Shuting Yu, Tianshu Wang, Li Wang, Shuihong Yao, Bin Zhang. Preceding crop rotation systems shape the selection process of wheat root-associated bacterial communities[J]. Journal of Integrative Agriculture, 2025, 24(2): 739-753.

参考文献

Ai C, Zhang S, Zhang X, Guo D, Zhou W, Huang S. 2018. Distinct responses of soil bacterial and fungal communities to changes in fertilization regime and crop rotation. Geoderma, 319, 156–166.

Bastian F, Bouziri L, Nicolardot B, Ranjard L. 2009. Impact of wheat straw decomposition on successional patterns of soil microbial community structure. Soil Biology and Biochemistry, 41, 262–275.

Bei S, Zhang Y, Li T, Christie P, Li X, Zhang J. 2018. Response of the soil microbial community to different fertilizer inputs in a Wheat–maize rotation on a calcareous soil. Agriculture, Ecosystems & Environment, 260, 58–69.

Benitez M S, Ewing P M, Osborne S L, Lehman R M. 2021. Rhizosphere microbial communities explain positive effects of diverse crop rotations on maize and soybean performance. Soil Biology and Biochemistry, 159, 108309.

Benjamini Y, Krieger A M, Yekutieli D. 2006. Adaptive linear step-up procedures that control the false discovery rate. Biometrika, 93, 491–507.

Bhuyan B, Debnath S, Pandey P. 2020. The rhizosphere microbiome and its role in plant growth in stressed conditions. In: Sharma S K, Singh U B, Sahu P K, Singh H V, Sharma P K, eds., Rhizosphere Microbes: Soil and Plant Functions. Springer Singapore, Singapore. pp. 503–529.

Callahan B J, McMurdie P J, Rosen M J, Han A W, Johnson A J A, Holmes S P. 2016. Dada2: High-resolution sample inference from illumina amplicon data. Nature Methods, 13, 581–583.

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 America, 108, 4516–4522.

Chang J, Tian L, Leite M F A, Sun Y, Shi S, Xu S, Wang J, Chen H, Chen D, Zhang J, Tian C, Kuramae E E. 2022. Nitrogen, manganese, iron, and carbon resource acquisition are potential functions of the wild rice Oryza rufipogon core rhizomicrobiome. Microbiome, 10, 196.

Chen Q L, Ding J, Zhu D, Hu H W, Delgado-Baquerizo M, Ma Y B, He J Z, Zhu Y G. 2020. Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils. Soil Biology and Biochemistry, 141, 107686.

Chen S, Waghmode T, Sun R, Kuramae E, Hu C, Liu B. 2019. Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome, 7, 136.

Compant S, Cambon M C, Vacher C, Mitter B, Samad A, Sessitsch A. 2021. The plant endosphere world - bacterial life within plants. Environmental Microbiology, 23, 1812–1829.

Dai T, Zhang Y, Tang Y, Bai Y, Tao Y, Huang B, Wen D. 2016. Identifying the key taxonomic categories that characterize microbial community diversity using full-scale classification: A case study of microbial communities in the sediments of Hangzhou bay. FEMS Microbiology Ecology, 92, fiw150.

Dini-Andreote F, Stegen J C, van Elsas J D, Salles J F. 2015. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proceedings of the National Academy of Sciences of the United States of America, 11, E1326–E1332.

Edwards J, Johnson C, Santos-Medellín 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 America, 112, E911.

Emmett B D, Buckley D H, Drinkwater L E. 2020. Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field. New Phytologist, 225, 960–973.

Emmett B D, Lévesque-Tremblay V, Harrison M J. 2021. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. The ISME Journal, 15, 2276–2288.

Fan K, Weisenhorn P, Gilbert J A, Chu H. 2018. Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biology and Biochemistry, 125, 251–260.

Galindo F S, Rodrigues W L, Fernandes G C, Boleta E H M, Jalal A, Rosa P A L, Buzetti S, Lavres J, Filho M C M T. 2022. Enhancing agronomic efficiency and maize grain yield with Azospirillum brasilense inoculation under Brazilian savannah conditions. European Journal of Agronomy, 134, 126471.

Geng S, Tan J, Li L, Miao Y, Wang Y. 2023. Legumes can increase the yield of subsequent wheat with or without grain harvesting compared to gramineae crops: A meta-analysis. European Journal of Agronomy, 142, 126643.

Guo J H, Liu X J, Zhang Y, Shen J L, Han W X, Zhang W F, Christie P, Goulding K W, Vitousek P M, Zhang F S. 2010. Significant acidification in major chinese croplands. Science, 327, 1008–1010.

Hannula S E, Heinen R, Huberty M, Steinauer K, De Long J R, Jongen R, Bezemer T M. 2021. Persistence of plant-mediated microbial soil legacy effects in soil and inside roots. Nature Communications, 12, 5686.

Hernandez D J, David A S, Menges E S, Searcy C A, Afkhami M E. 2021. Environmental stress destabilizes microbial networks. The ISME Journal, 15, 1722–1734.

Huse S M, Dethlefsen L, Huber J A, Welch D M, Relman D A, Sogin M L. 2008. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genetics, 4, e1000255.

Iheshiulo E M A, Larney F J, Hernandez-Ramirez G, St Luce M, Liu K, Chau H W. 2023. Do diversified crop rotations influence soil physical health? A meta-analysis. Soil and Tillage Research, 233, 105781.

IUSS Working Group WRB. 2022. World Reference Base for Soil Resources. International Soil Classification System for Naming Soils and Creating Legends for Soil Maps. 4th edition. International Union of Soil Sciences (IUSS), Vienna, Austria.

Ju X T, Xing G X, Chen X P, Zhang S L, Zhang L J, Liu X J, Cui Z L, Yin B, Christie P, Zhu Z L, Zhang F S. 2009. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proceedings of the National Academy of Sciences of the United States of America, 106, 3041–3046.

Kalburtji K L, Mamolos A P. 2000. Maize, soybean and sunflower litter dynamics in two physicochemically different soils. Nutrient Cycling in Agroecosystems, 57, 195–206.

Kavamura V N, Mendes R, Bargaz A, Mauchline T H. 2021. Defining the wheat microbiome: Towards microbiome-facilitated crop production. Computational and Structural Biotechnology Journal, 19, 1200–1213.

Langfelder P, Horvath S. 2008. Wgcna: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.

Li G, Niu W, Ma L, Du Y, Zhang Q, Sun J, Siddique K H M. 2023. Legacy effects of wheat season organic fertilizer addition on microbial co-occurrence networks, soil function, and yield of the subsequent maize season in a Wheat–maize rotation system. Journal of Environmental Management, 347, 119160.

Li H, Zhang Y, Yang S, Wang Z, Feng X, Liu H, Jiang Y. 2019. Variations in soil bacterial taxonomic profiles and putative functions in response to straw incorporation combined with N fertilization during the maize growing season. Agriculture, Ecosystems & Environment, 283, 106578.

Li T, Li Y, Shi Z, Wang S, Liao Y. 2021. Crop development has more influence on shaping rhizobacteria of wheat than tillage practice and crop rotation pattern in an arid agroecosystem. Applied Soil Ecology, 165, 104016.

Li T, Xie H, Ren Z, Hou Y, Zhao D, Wang W, Wang Z, Liu Y, Wen X, Han J, Mo F, Liao Y. 2023. Soil tillage rather than crop rotation determines assembly of the wheat rhizobacterial communities. Soil and Tillage Research, 226, 105588.

Liang H, Fu L B, Chen H, Zhou G P, Gao S J, Cao W D. 2023. Green manuring facilitates bacterial community dispersal across different compartments of subsequent tobacco. Journal of Integrative Agriculture, 22, 1199–1215.

Liaw A, Wiener M. 2002. Classification and regression by randomforest. R News, 2, 18–22.

Liu C, Feng X, Xu Y, Kumar A, Yan Z, Zhou J, Yang Y, Peixoto L, Zeng Z, Zang H. 2023. Legume-based rotation enhances subsequent wheat yield and maintains soil carbon storage. Agronomy for Sustainable Development, 43, 64.

Liu Z, Ying H, Chen M, Bai J, Xue Y, Yin Y, Batchelor W D, Yang Y, Bai Z, Du M, Guo Y, Zhang Q, Cui Z, Zhang F, Dou Z. 2021. Optimization of china’s maize and soy production can ensure feed sufficiency at lower nitrogen and carbon footprints. Nature Food, 2, 426–433.

Louca S, Parfrey L W, Doebeli M. 2016. Decoupling function and taxonomy in the global ocean microbiome. Science, 353, 1272–1277.

Lozupone C, Lladser M E, Knights D, Stombaugh J, Knight R. 2011. Unifrac: An effective distance metric for microbial community comparison. The ISME Journal, 5, 169–172.

Luo W, Wang J, Li Y, Wang C, Yang S, Jiao S, Wei G, Chen W. 2022. Local domestication of soybean leads to strong root selection and diverse filtration of root-associated bacterial communities. Plant and Soil, 480, 439–455.

Lupwayi N, Fernandez M, Petri R, Brown A H, Kanashiro D. 2023. Alteration of the organic wheat rhizobiome and enzyme activities by reduced tillage and diversified crop rotation. European Journal of Agronomy, 144, 126726.

Mendes L W, Kuramae E E, Navarrete A A, van Veen J A, Tsai S M. 2014. Taxonomical and functional microbial community selection in soybean rhizosphere. The ISME Journal, 8, 1577–1587.

Mhlongo M I, Piater L A, Madala N E, Labuschagne N, Dubery I A. 2018. The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Frontiers in Plant Science, 9, 112.

Nannipieri P, Hannula S E, Pietramellara G, Schloter M, Sizmur T, Pathan S I. 2023. Legacy effects of rhizodeposits on soil microbiomes: A perspective. Soil Biology and Biochemistry, 184, 109107.

NBSC (National Bureau of Statistics of China). 2020. China Statistical Yearbook. China Statistics Press, Beijing. (in Chinese)

Oksanen J, Blanchet F G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P, O’Hara R, Simpson G, Solymos P, Stevens H, Szöcs E, Wagner H. 2018. Vegan: Community ecology package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. R package version 2.5–7.

Peng J, Chen C, Xiong C, Li S, Ge A, Wang E, Liesack W. 2023. Harnessing biological nitrogen fixation in plant leaves. Trends in Plant Science, 28, 1391–1405.

Quiza L, Tremblay J, Pagé A P, Greer C W, Pozniak C J, Li R, Haug B, Hemmingsen S M, St-Arnaud M, Yergeau E. 2023. The effect of wheat genotype on the microbiome is more evident in roots and varies through time. ISME Communications, 3, 32.

Reinhold-Hurek B, Bünger W, Burbano C S, Sabale M, Hurek T. 2015. Roots shaping their microbiome: Global hotspots for microbial activity. Annual Review of Phytopathology, 53, 403–424.

Rezgui C, Trinsoutrot-Gattin I, Benoit M, Laval K, Riah-Anglet W. 2021. Linking changes in the soil microbial community to C and N dynamics during crop residue decomposition. Journal of Integrative Agriculture, 20, 3039–3059.

Robinson M D, McCarthy D J, Smyth G K. 2010. Edger: A bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139–140.

Shi Z, Liu D, Liu M, Hafeez M B, Wen P, Wang X, Wang R, Zhang X, Li J. 2021. Optimized fertilizer recommendation method for nitrate residue control in a wheat–maize double cropping system in dryland farming. Field Crops Research, 271, 108258.

Stegen J C, Fredrickson J K, Wilkins M J, Konopka A E, Nelson W C, Arntzen E V, Chrisler W B, Chu R K, Danczak R E, Fansler S J, Kennedy D W, Resch C T, Tfaily M. 2016. Groundwater–surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover. Nature Communications, 7, 11237.

Sun A, Jiao X Y, Chen Q, Wu A L, Zheng Y, Lin Y X, He J Z, Hu H W. 2021. Microbial communities in crop phyllosphere and root endosphere are more resistant than soil microbiota to fertilization. Soil Biology and Biochemistry, 153, 108113.

Trivedi P, Leach J E, Tringe S G, Sa T, Singh B K. 2020. Plant–microbiome interactions: From community assembly to plant health. Nature Reviews Microbiology, 18, 607–621.

Vives-Peris V, de Ollas C, Gómez-Cadenas A, Pérez-Clemente R M. 2020. Root exudates: From plant to rhizosphere and beyond. Plant Cell Reports, 39, 3–17.

Wang P, Nie J, Yang L, Zhao J, Wang X, Zhang Y, Zang H, Yang Y, Zeng Z. 2023. Plant growth stages covered the legacy effect of rotation systems on microbial community structure and function in wheat rhizosphere. Environmental Science and Pollution Research, 30, 59632–59644.

Wang Y, Liu L, Yang J, Duan Y, Luo Y, Taherzadeh M J, Li Y, Li H, Awasthi M K, Zhao Z. 2020. The diversity of microbial community and function varied in response to different agricultural residues composting. Science of the Total Environment, 715, 136983.

Xie Z, Yu Z, Li Y, Wang G, Liu X, Tang C, Lian T, Adams J, Liu J, Liu J, Herbert S J, Jin J. 2022. Soil microbial metabolism on carbon and nitrogen transformation links the crop-residue contribution to soil organic carbon. NPJ Biofilms and Microbiomes, 8, 14.

Xiong C, Lu Y. 2022. Microbiomes in agroecosystem: Diversity, function and assembly mechanisms. Environmental Microbiology Reports, 14, 833–849.

Xiong C, Singh B K, He J Z, Han Y L, Li P P, Wan L H, Meng G Z, Liu S Y, Wang J T, Wu C F, Ge A H, Zhang L M. 2021a. Plant developmental stage drives the differentiation in ecological role of the maize microbiome. Microbiome, 9, 171.

Xiong C, Zhu Y G, Wang J T, Singh B, Han L L, Shen J P, Li P P, Wang G B, Wu C F, Ge A H, Zhang L M, He J Z. 2021b. Host selection shapes crop microbiome assembly and network complexity. New Phytologist, 229, 1091–1104.

Ye Z, Li J, Wang J, Zhang C, Liu G, Dong Q G. 2021. Diversity and co-occurrence network modularization of bacterial communities determine soil fertility and crop yields in arid fertigation agroecosystems. Biology and Fertility of Soils, 57, 809–824.

Yin C, Hulbert S H, Schroeder K L, Mavrodi O, Mavrodi D, Dhingra A, Schillinger W F, Paulitz T C. 2013. Role of bacterial communities in the natural suppression of rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.). Applied and Environmental Microbiology Journal, 79, 7428–7438.

Yu S, Wang T, Meng Y, Yao S, Wang L, Zheng H, Zhou Y, Song Z, Zhang B. 2022. Leguminous cover crops and soya increased soil fungal diversity and suppressed pathotrophs caused by continuous cereal cropping. Frontiers in Microbiology, 13, 993214.

Zhalnina K, Louie K B, Hao Z, Mansoori N, da Rocha U N, Shi S, Cho H, Karaoz U, Loqué D, Bowen B P, Firestone M K, Northen T R, Brodie E L. 2018. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nature Microbiology, 3, 470–480.

Zhang B, Zhang J, Liu Y, Shi P, Wei G. 2018. Co-occurrence patterns of soybean rhizosphere microbiome at a continental scale. Soil Biology & Biochemistry, 118, 178–186.

Zhang H, Luo G, Wang Y, Fei J, Xiangmin R, Peng J, Tian C, Zhang Y. 2023. Crop rotation-driven change in physicochemical properties regulates microbial diversity, dominant components, and community complexity in paddy soils. Agriculture, Ecosystems & Environment, 343, 108278.

Zhang J, Liu Y X, Zhang N, Hu B, Jin T, Xu H, Qin Y, Yan P, Zhang X, Guo X, Hui J, Cao S, Wang X, Wang C, Wang H, Qu B, Fan G, Yuan L, Garrido-Oter R, Chu C, Bai Y. 2019. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nature Biotechnology, 37, 676–684.

Zhang L, Ge A H, Tóth T, An F, Guo L, Nie Z, Liu J, Yang F, Wang Z. 2021. Soil bacterial microbiota predetermines rice yield in reclaiming saline-sodic soils leached with brackish ice. Journal of the Science of Food and Agriculture, 101, 6472–6483.

编辑推荐 0

Metrics

阅读次数

全文

HTML			PDF

最新录用	在线预览	正式出版	最新录用	在线预览	正式出版
0	0	0	2	0	0

	来源	本网站

	次数	2
	比例	100%

摘要

最新录用	在线预览	正式出版

21	0	32

	来源	本网站

	次数	53
	比例	100%