OpenLB
Open Library of Bioscience
Advanced Search
Environmental microbiology
Apr, 2025;27 (4): e70085.

Continuous Rice Cultivation Increases Celery Yield by Enhancing Plant Beneficial Bacteria in Rice-Celery Rotations.

Danyan Qiu, Mingjing Ke, Nuohan Xu, Hang Hu, Yuke Zhu, Tao Lu, MingKang Jin, Zhenyan Zhang, Qi Zhang, Josep Penuelas, Michael Gillings, Haifeng Qian
Author Information
  1. Danyan Qiu: College of Environment, Zhejiang University of Technology, Hangzhou, People's Republic of China.
  2. Mingjing Ke: College of Environment, Zhejiang University of Technology, Hangzhou, People's Republic of China.
  3. Nuohan Xu: Institute for Advanced Study, Shaoxing University, Shaoxing, People's Republic of China.
  4. Hang Hu: College of Environment, Zhejiang University of Technology, Hangzhou, People's Republic of China.
  5. Yuke Zhu: College of Environment, Zhejiang University of Technology, Hangzhou, People's Republic of China.
  6. Tao Lu: College of Environment, Zhejiang University of Technology, Hangzhou, People's Republic of China. ORCID
  7. MingKang Jin: Research Center for eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, People's Republic of China.
  8. Zhenyan Zhang: College of Environment, Zhejiang University of Technology, Hangzhou, People's Republic of China. ORCID
  9. Qi Zhang: Institute for Advanced Study, Shaoxing University, Shaoxing, People's Republic of China.
  10. Josep Penuelas: CSIC, Global Ecology Unit CREAF-CSIC-UAB, Barcelona, Catalonia, Spain.
  11. Michael Gillings: ARC Centre of Excellence in Synthetic Biology, Faculty of Science and Engineering, Macquarie University, New South Wales, Australia.
  12. Haifeng Qian: College of Environment, Zhejiang University of Technology, Hangzhou, People's Republic of China. ORCID
PMID: 40151905 DOI: 10.1111/1462-2920.70085

Abstract

The sustainable management of crops is a fundamental challenge as the human population and demand for food increase. Crop rotation, a practice that has been used for centuries, offers a sustainable solution with minimal environmental impact. However, our understanding of how microbial diversity changes during rotation and how microbially mediated functions enhance plant production remains limited. In our study, we combined field surveys of rice-celery rotations with greenhouse experiments. We found that crop rotation increased yield by increasing the presence of plant-beneficial bacteria, including a novel strain named Acinetobacter bohemicus HfQ1. Bacteria that promote plant growth are enriched under crop rotation, leading to increased ammonia oxidation, siderophore production and indole-3-acetic acid synthesis. These beneficial ecological consequences of crop rotation were consistent across various crops during our metadata analysis. Our study provides new insights into the development of innovative crop rotation models and effective strategies to safeguard food production and advance sustainable agriculture. Additionally, the Acinetobacter strain may serve as a potential microbial agent to replace chemical fertilisers, further supporting sustainable agricultural practices.

Keywords

crop yield plant beneficial bacteria plant growth promotion rotation

References

  1. Andersen, S. B., R. L. Marvig, S. Molin, H. K. Johansen, and A. S. Griffin. 2015. “Long‐Term Social Dynamics Drive Loss of Function in Pathogenic Bacteria.” Proceedings. National Academy of Sciences. United States of America 112: 10756–10761.
  2. Barber, M. F., and N. C. Elde. 2015. “Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy.” Trends in Genetics 31: 627–636.
  3. Bolger, A. M., M. Lohse, and B. Usadel. 2014. “Trimmomatic: A Flexible Trimmer for Illumina Sequence Data.” Bioinformatics 30: 2114–2120.
  4. Bolyen, E., J. R. Rideout, M. R. Dillon, et al. 2019. “Reproducible, Interactive, Scalable and Extensible Microbiome Data Science Using QIIME 2.” Nature Biotechnology 37: 852–857.
  5. Braun‐Kiewnick, A., A. Giongo, P. M. Zamberlan, et al. 2024. “The Microbiome of Continuous Wheat Rotations: Minor Shifts in Bacterial and Archaeal Communities but a Source for Functionally Active Plant‐Beneficial Bacteria.” Phytobiomes Journal: 1–99.
  6. Callahan, B. J., P. J. McMurdie, M. J. Rosen, A. W. Han, A. J. A. Johnson, and S. P. Holmes. 2016. “DADA2: High‐Resolution Sample Inference From Illumina Amplicon Data.” Nature Methods 13: 581–583.
  7. Carrión, V. J., J. Perez‐Jaramillo, V. Cordovez, et al. 2019. “Pathogen‐Induced Activation of Disease‐Suppressive Functions in the Endophytic Root Microbiome.” Science 366: 606–612.
  8. Cernay, C., D. Makowski, and E. Pelzer. 2018. “Preceding Cultivation of Grain Legumes Increases Cereal Yields Under Low Nitrogen Input Conditions.” Environmental Chemistry Letters 16: 631–636.
  9. Cordero, O. X., L. A. Ventouras, E. F. DeLong, and M. F. Polz. 2012. “Public Good Dynamics Drive Evolution of Iron Acquisition Strategies in Natural Bacterioplankton Populations.” Proceedings. National Academy of Sciences. United States of America 109: 20059–20064.
  10. Deng, X., N. Zhang, Y. Li, et al. 2022. “Bio‐Organic Soil Amendment Promotes the Suppression of Ralstonia solanacearum by Inducing Changes in the Functionality and Composition of Rhizosphere Bacterial Communities.” New Phytologist 235: 1558–1574.
  11. Dirzo, R., and P. H. Raven. 2003. “Global State of Biodiversity and Loss.” Annual Review of Environment and Resources 28: 137–167.
  12. Dixon, P. 2003. “VEGAN, a Package of R Functions for Community Ecology.” Journal of Vegetation Science 14: 927–930.
  13. Douglas, G. M., V. J. Maffei, J. Zaneveld, et al. 2019. PICRUSt2: An Improved and Extensible Approach for Metagenome Inference. Cold Spring Harbor Laboratory.
  14. Droux, M. 2004. “Sulfur Assimilation and the Role of Sulfur in Plant Metabolism: A Survey.” Photosynthesis Research 79: 331–348.
  15. Duca, D., J. Lorv, C. L. Patten, D. Rose, and B. R. Glick. 2014. “Indole‐3‐Acetic Acid in Plant–Microbe Interactions.” Antonie Van Leeuwenhoek International Journal of General and Molecular 106: 85–125.
  16. Fu, L. M., B. F. Niu, Z. W. Zhu, S. T. Wu, and W. Z. Li. 2012. “CD‐HIT: Accelerated for Clustering the Next‐Generation Sequencing Data.” Bioinformatics 28: 3150–3152.
  17. Gandhi, A., and G. Muralidharan. 2016. “Assessment of Zinc Solubilizing Potentiality of Acinetobacter Sp. Isolated From Rice Rhizosphere.” European Journal of Soil Biology 76: 1–8.
  18. Gu, S. H., Z. Wei, Z. Y. Shao, et al. 2020. “Competition for Iron Drives Phytopathogen Control by Natural Rhizosphere Microbiomes.” Nature Microbiology 5: 1002–1010.
  19. Hayashi, K., K. Arai, Y. Aoi, et al. 2021. “The Main Oxidative Inactivation Pathway of the Plant Hormone Auxin.” Nature Communications 12: 6752.
  20. Hofte, M., S. Buysens, N. Koedam, and P. Cornelis. 1993. “Zinc Affects Siderophore‐Mediated High‐Affinity Iron Uptake Systems in the Rhizosphere Pseudomonas‐Aeruginosa 7NSK2.” BioMetals 6: 85–91.
  21. Hong, S., X. F. Yuan, J. M. Yang, et al. 2023. “Selection of Rhizosphere Communities of Diverse Rotation Crops Reveals Unique Core Microbiome Associated With Reduced Banana Fusarium Wilt Disease.” New Phytologist 238: 2194–2209.
  22. Hoysrijan, B., and A. Sirikulkajorn. 2023. “Colorimetric and Fluorogenic Detection of Nitrite Anion in Water and Food Based on Griess Reaction of Fluorene Derivatives.” Journal of Food Composition and Analysis 117: 105123.
  23. Hu, L. G., X. G. Lin, H. Y. Chu, et al. 2005. “Isolation of Soil Ammonia‐Oxidizing Bacteria.” Soils 37: 3.
  24. Huang, Y. S., T. Shi, X. Luo, et al. 2019. “Determination of Multipesticide Residues in Green Tea With a Modified QuEChERS Protocol Coupled to HPLC‐MS/MS.” Food Chemistry 275: 255–264.
  25. Kaloterakis, N., M. Rashtbari, B. S. Razavi, et al. 2024. “Preceding Crop Legacy Modulates the Early Growth of Winter Wheat by Influencing Root Growth Dynamics, Rhizosphere Processes, and Microbial Interactions.” Soil Biology and Biochemistry 191: 109343.
  26. Kümmerli, R., K. T. Schiessl, T. Waldvogel, K. McNeill, and M. Ackermann. 2014. “Habitat Structure and the Evolution of Diffusible Siderophores in Bacteria.” Ecology Letters 17: 1536–1544.
  27. Larkin, R. P., and C. W. Honeycutt. 2006. “Effects of Different 3‐Year Cropping Systems on Soil Microbial Communities and Rhizoctonia Diseases of Potato.” Phytopathology 96: 68–79.
  28. Li, D. H., C. M. Liu, R. B. Luo, K. Sadakane, and T. W. Lam. 2015. “MEGAHIT: An Ultra‐Fast Single‐Node Solution for Large and Complex Metagenomics Assembly via Succinct de Bruijn Graph.” Bioinformatics 31: 1674–1676.
  29. Li, Y., S. A. Lei, Z. Q. Cheng, et al. 2023. “Microbiota and Functional Analyses of Nitrogen‐Fixing Bacteria in Root‐Knot Nematode Parasitism of Plants.” Microbiome 11: 48.
  30. Li, Y., Z. Li, S. X. Chang, et al. 2020. “Residue Retention Promotes Soil Carbon Accumulation in Minimum Tillage Systems: Implications for Conservation Agriculture.” Science of the Total Environment 740: 140147.
  31. Liu, W. J., E. B. Graham, Y. Dong, et al. 2021. “Balanced Stochastic Versus Deterministic Assembly Processes Benefit Diverse Yet Uneven Ecosystem Functions in Representative Agroecosystems.” Environmental Microbiology 23: 391–404.
  32. Liu, X. T., S. W. Tan, X. J. Song, et al. 2022. “Response of Soil Organic Carbon Content to Crop Rotation and Its Controls: A Global Synthesis.” Agriculture, Ecosystems & Environment 335: 108017.
  33. Lu, T., M. J. Ke, M. Lavoie, et al. 2018. “Rhizosphere Microorganisms Can Influence the Timing of Plant Flowering.” Microbiome 6: 231.
  34. McDaniel, M. D., A. S. Grandy, L. K. Tiemann, and M. N. Weintraub. 2014. “Crop Rotation Complexity Regulates the Decomposition of High and Low Quality Residues.” Soil Biology and Biochemistry 78: 243–254.
  35. Meier, M. A., M. G. Lopez‐Guerrero, M. Guo, et al. 2021. “Rhizosphere Microbiomes in a Historical Maize–Soybean Rotation System Respond to Host Species and Nitrogen Fertilization at the Genus and Subgenus Levels.” Applied and Environmental Microbiology 87, no. 12: e03132‐20.
  36. Muscatt, G., S. Hilton, S. Raguideau, et al. 2022. “Crop Management Shapes the Diversity and Activity of DNA and RNA Viruses in the Rhizosphere.” Microbiome 10: 181.
  37. Ouda, S., A. Zohry, and T. Noreldin. 2018. “Crop Rotation Maintains Soil Sustainability.” In Crop Rotation: An Approach to Secure Future Food, edited by S. Ouda, A. E.‐H. Zohry, and T. Noreldin. Springer International Publishing.
  38. Palma‐Guerrero, J., T. Chancellor, J. Spong, et al. 2021. “Take‐All Disease: New Insights Into an Important Wheat Root Pathogen.” Trends in Plant Science 26, no. 8: 836–848.
  39. Peñuelas, J., B. Poulter, J. Sardans, et al. 2013. “Human‐Induced Nitrogen–Phosphorus Imbalances Alter Natural and Managed Ecosystems Across the Globe.” Nature Communications 4: 2934.
  40. Peralta, A. L., Y. M. Sun, M. D. McDaniel, and J. T. Lennon. 2018. “Crop Rotational Diversity Increases Disease Suppressive Capacity of Soil Microbiomes.” Ecosphere 9: e02235.
  41. Rolli, E., R. Marasco, G. Vigani, et al. 2015. “Improved Plant Resistance to Drought Is Promoted by the Root‐Associated Microbiome as a Water Stress‐Dependent Trait.” Environmental Microbiology 17: 316–331.
  42. Schwyn, B., and J. B. Neilands. 1987. “Universal Chemical Assay for the Detection and Determination of Siderophores.” Analytical Biochemistry 160: 47–56.
  43. Smith, M. E., G. Vico, A. Costa, et al. 2023. “Increasing Crop Rotational Diversity Can Enhance Cereal Yields.” Communications Earth & Environment 4: 89.
  44. Soman, C., D. F. Li, M. M. Wander, and A. D. Kent. 2017. “Long‐Term Fertilizer and Crop‐Rotation Treatments Differentially Affect Soil Bacterial Community Structure.” Plant and Soil 413: 145–159.
  45. Suzuki, W., M. Sugawara, K. Miwa, and M. Morikawa. 2014. “Plant Growth‐Promoting Bacterium Acinetobacter calcoaceticus P23 Increases the Chlorophyll Content of the Monocot Lemna minor (Duckweed) and the Dicot Lactuca sativa (Lettuce).” Journal of Bioscience and Bioengineering 118: 41–44.
  46. Tiemann, L. K., A. S. Grandy, E. E. Atkinson, E. Marin‐Spiotta, and M. D. McDaniel. 2015. “Crop Rotational Diversity Enhances Belowground Communities and Functions in an Agroecosystem.” Ecology Letters 18: 761–771.
  47. Tilman, D., C. Balzer, J. Hill, and B. L. Befort. 2011. “Global Food Demand and the Sustainable Intensification of Agriculture.” Proceedings. National Academy of Sciences. United States of America 108: 20260–20264.
  48. Venter, Z. S., K. Jacobs, and H.‐J. Hawkins. 2016. “The Impact of Crop Rotation on Soil Microbial Diversity: A Meta‐Analysis.” Pedobiologia 59: 215–223.
  49. Wang, C., M. M. Zheng, W. F. Song, et al. 2017. “Impact of 25 Years of Inorganic Fertilization on Diazotrophic Abundance and Community Structure in an Acidic Soil in Southern China.” Soil Biology and Biochemistry 113: 240–249.
  50. Wang, S. L., Y. P. Zhao, Z. H. Wang, X. L. Lv, A. L. Wright, and X. J. Jiang. 2022. “Contrasting Seasonal Response of Comammox Nitrospira and Canonical Ammonia Oxidizers in Two Paddy Soils.” Soil Biology and Biochemistry 168: 108641.
  51. Xia, L. L., S. K. Lam, B. Wolf, R. Kiese, D. L. Chen, and K. Butterbach‐Bahl. 2018. “Trade‐Offs Between Soil Carbon Sequestration and Reactive Nitrogen Losses Under Straw Return in Global Agroecosystems.” Global Change Biology 24: 5919–5932.
  52. Xuan, D. T., V. T. Guong, A. Rosling, S. Alström, B. L. Chai, and N. Högberg. 2012. “Different Crop Rotation Systems as Drivers of Change in Soil Bacterial Community Structure and Yield of Rice, Oryza Sativa.” Biology and Fertility of Soils 48: 217–225.
  53. Yang, X., J. Xiong, T. Du, et al. 2024. “Diversifying Crop Rotation Increases Food Production, Reduces Net Greenhouse Gas Emissions and Improves Soil Health.” Nature Communications 15: 198.
  54. Yu, T., J. Nie, H. Zang, Z. Zeng, and Y. Yang. 2023. “Peanut‐Based Rotation Stabilized Diazotrophic Communities and Increased Subsequent Wheat Yield.” Microbial Ecology 86: 2447–2460.
  55. Yue, J., X. Hu, and J. Huang. 2014. “Origin of Plant Auxin Biosynthesis.” Trends in Plant Science 19: 764–770.
  56. Zhang, Q., Z. Y. Zhang, T. Lu, et al. 2020. “Cyanobacterial Blooms Contribute to the Diversity of Antibiotic‐Resistance Genes in Aquatic Ecosystems.” Communications Biology 3: 737.
  57. Zhang, X. X., R. J. Zhang, J. S. Gao, et al. 2017. “Thirty‐One Years of Rice–Rice‐Green Manure Rotations Shape the Rhizosphere Microbial Community and Enrich Beneficial Bacteria.” Soil Biology and Biochemistry 104: 208–217.
  58. Zhao, J., J. Chen, D. Beillouin, et al. 2022. “Global Systematic Review With Meta‐Analysis Reveals Yield Advantage of Legume‐Based Rotations and Its Drivers.” Nature Communications 13: 4926.
  59. Zhao, J., Y. D. Yang, K. Zhang, J. Jeong, Z. H. Zeng, and H. D. Zang. 2020. “Does Crop Rotation Yield More in China? A Meta‐Analysis.” Field Crops Research 245: 107659.
  60. Zhu, C. K., S. L. Qi, H. van Triest, S. J. Wang, Y. Kang, and Y. Yue. 2004. “Automatic 3D Segmentation of Human Airway Tree in CT Image.” In In: 2010 3rd International Conference on Biomedical Engineering and Informatics.
  61. Zhu, G. B., X. M. Wang, S. Y. Wang, et al. 2022. “Toward a More Labor‐Saving Way in Microbial Ammonium Oxidation: A Review on Complete Ammonia Oxidization (Comammox).” Science of the Total Environment 829: 154590.

Grants

  1. ZJ2023058/Zhejiang Provincial Postdoctoral Science Foundation
  2. CIVP20A6621/Fundación Ramón Areces Grant
  3. SGR2021-1333/Catalan Government Grants
  4. AGAUR2023CLIMA00118/Catalan Government Grants
  5. TED2021-132627 B-I00/Spanish Government Grants
  6. PID2022-140808NB-I00/Spanish Government Grants
  7. 2022C02029/Key Research and Development Program of Zhejiang Province
  8. LZ23B070001/Zhejiang Provincial Natural Science Foundation of China
  9. 22376187/National Natural Science Foundation of China
  10. 42307158/National Natural Science Foundation of China
  11. 42377107/National Natural Science Foundation of China
  12. 2023M743100/China Postdoctoral Science Foundation

MeSH Term

Oryza
Crops, Agricultural
Agriculture
Bacteria
Acinetobacter
Soil Microbiology
Indoleacetic Acids
Siderophores

Chemicals

Indoleacetic Acids
indoleacetic acid
Siderophores
Journal Article

Word Cloud

Created with Highcharts 10.0.0rotationcropsustainableplantproductioncropsfoodmicrobialstudyincreasedyieldbacteriastrainAcinetobacterBacteriagrowthbeneficialmanagementfundamentalchallengehumanpopulationdemandincreaseCroppracticeusedcenturiesofferssolutionminimalenvironmentalimpactHoweverunderstandingdiversitychangesmicrobiallymediatedfunctionsenhanceremainslimitedcombinedfieldsurveysrice-celeryrotationsgreenhouseexperimentsfoundincreasingpresenceplant-beneficialincludingnovelnamedbohemicusHfQ1promoteenrichedleadingammoniaoxidationsiderophoreindole-3-aceticacidsynthesisecologicalconsequencesconsistentacrossvariousmetadataanalysisprovidesnewinsightsdevelopmentinnovativemodelseffectivestrategiessafeguardadvanceagricultureAdditionallymayservepotentialagentreplacechemicalfertiliserssupportingagriculturalpracticesContinuousRiceCultivationIncreasesCeleryYieldEnhancingPlantBeneficialRice-CeleryRotationspromotion

Similar Articles

Cited By

No available data.