Plant Soil Environ., 2024, 70(6):342-355 | DOI: 10.17221/498/2023-PSE

Partitioned nitrogen fertilisation in peanut rhizosphere and geocarposphere drives specific variation soil microbiomesOriginal Paper

Haiyan Liang1, Qi Wu1, Liyu Yang1, Dianxu Chen1, Pu Shen1
1 Shandong Peanut Research Institute/Chinese National Peanut Engineering Research Center, Qingdao, P.R. China

Peanut is a plant characterised by belowground fruiting that absorbs nutrients not only through its roots but also through its pods. However, little is currently known regarding the species of bacteria that contribute to nutrient absorption and utilisation in this plant’s pod and root zones. This study examined the effects of root and pod area nitrogen (N) fertiliser application on peanut rhizosphere and geocarposphere microbial communities and functions. Using two peanut cultivars [nodulated Huayu 22 (H) and non-nodulated NN-1 (B)], we applied the following four treatments: no N fertiliser (HT1, BH1); N applied to geocarposphere soil (HT2, BT2); N applied to rhizosphere soil (HT3, BT3), and N applied to both rhizosphere and geocarposphere soil (HT4, BT4). The results revealed that compared with HT1 and BT1, the HT3, HT4, BT3, and BT4 treatments promoted increases in total plant accumulated N of 11.2, 30.1, 38.5, and 9.9%, respectively. Moreover, N input contributed to an increase in the abundance of bacteria colonising the surrounding pods, which differed significantly from bacteria colonising the rhizosphere. Among the top four bacterial phyla detected, we recorded a significant increase in the relative abundances of Proteobacteria and Gemmatimonadetes in response to treatments HT2 and HT4, whereas the highest relative abundances of Acidobacteria and Actinobacteria were detected in HT3 plants. Regarding cultivar B, we detected increases in the relative abundances of Bacteroidetes and Gemmatimonadetes in response to the BT2 and BT4 treatments, and in the relative abundance of Actinobacteria in BT3 treated soil. The findings of FAPROTAX functional analysis revealed clear differences among the T2, T4, and T3 treatments of two peanut cultivars concerning the functional groups with the highest relative abundances. These findings will make a considerable contribution to enhancing our understanding of the effects of N fertilisation on soil microbial structure and function in the rhizosphere and geocarposphere of peanuts and can provide a basis for identifying beneficial bacteria for promoting N utilisation and yield enhancement.

Keywords: Arachis hypogaea L.; pod zone; zoot zone; bacterial composition and diversity; nitrogen application

Received: December 21, 2023; Revised: April 8, 2024; Accepted: April 10, 2024; Prepublished online: April 10, 2024; Published: May 24, 2024  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Liang H, Wu Q, Yang L, Chen D, Shen P. Partitioned nitrogen fertilisation in peanut rhizosphere and geocarposphere drives specific variation soil microbiomes. Plant Soil Environ. 2024;70(6):342-355. doi: 10.17221/498/2023-PSE.
Download citation

References

  1. Abdel-Gayed M.A., Abo-Zaid G.A., Matar S.M., Hafez E.E. (2019): Fermentation, formulation and evaluation of PGPR Bacillus subtilis isolate as a bioagent for reducing the occurrence of peanut soil-borne diseases. Journal of Integrative Agriculture, 18: 2080-2092. Go to original source...
  2. Arafa R.A.M., El-Rahmany T.A., El-Ghany B.F.A., El-Shazly M.M. (2010): Role of some effective microorganisms in improving soil properties and peanut productivity under North Sinai conditions. Research Journal of Agriculture and Biological Sciences, 6: 228-246.
  3. Arya S.S., Salve A.R., Chauhan S. (2016): Peanuts as functional food: a review. Journal of Food Science and Technology, 53: 31-41. Go to original source... Go to PubMed...
  4. Bai Y., Muller D.B., Srinivas G., Garrido-Oter R., Potthoff E., Rott M., Dombrowski N., Munch P.C., Spaepen S., Remus-Emsermann M., Huttel B., McHardy A.C., Vorholt J.A., Schulze-Lefert P. (2015): Functional overlap of the Arabidopsis leaf and root microbiota. Nature, 528: 364-369. Go to original source... Go to PubMed...
  5. Beringer H., Taha H.A. (1976): 45Calcium absorption by two cultivars of groundnut (Arachis hypogea). Experimental Agriculture, 12: 1-7. Go to original source...
  6. Bobbink R., Hicks K., Galloway J., Spranger T., Alkemade R., Ashmore M., Bustamante M., Cinderby S., Davidson E., Dentener F. (2010): Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications, 20: 30-59. Go to original source... Go to PubMed...
  7. Fuke P.T.M.M., Kumar M., Sawarkar A.D., Pandey A., Singh L. (2021): Role of microbial diversity to influence the growth and environmental remediation capacity of bamboo: a review. Industrial Crops and Products, 167: 113567. Go to original source...
  8. Garren K.H. (1966): Peanut (groundnut) microfloras and pathogenesis in peanut pod rot. Journal of Phytopathology, 55: 359-367. Go to original source...
  9. Geisseler D., Scow K.M. (2014): Long-term effects of mineral fertilizers on soil microorganisms - a review. Soil Biology and Biochemistry, 75: 54-63. Go to original source...
  10. Gyaneshwar P., Hirsch A.M., Moulin L., Chen W.M., Elliott G.N., Bontemps C., Estrada-de los Santos P., Gross E., dos Reis F.B., Sprent J.I., Young J.P.W., James E.K. (2011): Legume-nodulating betaproteobacteria diversity, host range, and future prospects. Molecular Plant-Microbe Interac-tions, 24: 1276-1288. Go to original source... Go to PubMed...
  11. Hou L., Lin R.X., Wang X.J., Li H., Zhao C.Z., Zhu X.J., Li C.S., Li G.H. (2022): The mechanisms of pod zone nitrogen application on peanut pod yield. Russian Journal of Plant Physiology, 69: 51. Go to original source...
  12. Inanaga S., Utunomiya M., Horiguchi T., Nishihara T. (1990): Behaviour of fertilizer-N absorbed through root and fruit in peanut. Plant and Soil, 122: 85-89. Go to original source...
  13. Kloepper J.W., Bowen K.L. (1991): Quantification of the geocarposphere and rhizosphere effect of peanut (Arachis hypogaea L.). Plant and Soil, 136: 103-109. Go to original source...
  14. Kloepper J.W., McInroy J.A., Bowen K.L. (1992): Comparative identification by fatty acid analysis of soil, rhizosphere, and geocarposphere bacte-ria of peanut (Arachis hypogaea L.). Plant and Soil, 139: 85-90. Go to original source...
  15. Li F., Hao Z., Chen B. (2019): Molecular mechanism for the adaption of arbuscular mycorrhizal symbiosis to phosphorus deficiency. Journal of Plant Nutrition and Fertilizers, 25: 1989-1997.
  16. Li Y., Pan F., Yao H. (2019): Response of symbiotic and asymbiotic nitrogen-fixing microorganisms to nitrogen fertilizer application. Journal of Soils and Sediments, 19: 1948-1958. Go to original source...
  17. Li G.H., Guo X., Sun W., Hou L., Wang G.H., Tian R.Z., Wang X.J., Qu C.J., Zhao C.Z. (2024): Nitrogen application in pod zone improves yield and quality of two peanut cultivars by modulating nitrogen accumulation and metabolism. BMC Plant Biology, 24: 48. Go to original source... Go to PubMed...
  18. Liang H.Y., Yang L.Y., Wu Q., Meng C.P., Zhang J.C., Shen P. (2023): Regulation of the C:N ratio improves the N-fixing bacteria activity, root growth, and nodule formation of peanut. Journal of Soil Science and Plant Nutrition, 23: 4596-4608. Go to original source...
  19. Liang H.Y., Yang L.Y., Wu Q., Yin L., Meng C.P., Shen P. (2022): Exogenous glucose modulated the diversity of soil nitrogen-related bacteria and promoted the nitrogen absorption and utilisation of peanut. Plant, Soil and Environment, 68: 560-571. Go to original source...
  20. Louca S., Parfrey L.W., Doebeli M. (2016): Decoupling function and taxonomy in the global ocean microbiome. Science, 353: 1272-1277. Go to original source... Go to PubMed...
  21. Lu M., Yang Y.H., Luo Y.Q., Fang C.M., Zhou X.H., Chen J.K., Yang X., Li B. (2011): Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis. New Phytologist, 189: 1040-1050. Go to original source... Go to PubMed...
  22. Michalczyk A., Kersebaum K.C., Dauck H.P., Roelcke M., Yue S.C., Chen X.P., Zhang F.S. (2020): Quantifying nitrogen loss and water use via regionalization and multiple-year scenario simulations in the North China Plain. Journal of Plant Nutrition and Soil Science, 183: 718-733. Go to original source...
  23. Moreau D., Bardgett R.D., Finlay R.D., Jones D.L., Philippot L. (2019): A plant perspective on nitrogen cycling in the rhizosphere. Functional Ecology, 33: 540-552. Go to original source...
  24. Qu Q., Zhang Z.Y., Peijnenburg W.J.G.M., Liu W.Y., Lu T., Hu B.L., Chen J.M., Chen J., Lin Z.F., Qian H.F. (2020): Rhizosphere microbiome assembly and its impact on plant growth. Journal of Agricultural and Food Chemistry, 68: 5024-5038. Go to original source... Go to PubMed...
  25. 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. Go to original source... Go to PubMed...
  26. Sahib M.R., Pervaiz Z.H., Williams M.A., Saleem M., DeBolt S. (2020): Rhizobacterial species richness improves sorghum growth and soil nutrient synergism in a nutrient-poor greenhouse soil. Scientific Reports, 10: 15454. Go to original source... Go to PubMed...
  27. Selamat A., Gardner F.P. (1985): Nitrogen partitioning and redistribution in nonnodulating peanut related to nitrogen stress. Agronomy Journal, 77: 859-862. Go to original source...
  28. Shi H., Miao S.J., Liu J.D., Zhou K.Q. (2012): Effect of nitrogen application on growth and nitrogen fixation in nodulation and non-nodulation soybean isolines. Soybean Science, 31: 961-965. (In Chinese)
  29. Shi X.L., Zhou Y.F., Guo P., Ren J.Y., Zhang H., Dong Q.Q., Jiang C.J., Zhong C., Zhang Z., Wan S.B., Zhao X.H., Yu H.Q. (2022): Peanut/sorghum intercropping drives specific variation in peanut rhizosphere soil properties and microbiomes under salt stress. Land Degradation and Devel-opment, 34: 736-750. Go to original source...
  30. Treseder K.K. (2008): Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters, 11: 1111-1120. Go to original source... Go to PubMed...
  31. Weiss A., Shaw L.N. (2015): Small things considered: the small accessory subunits of RNA polymerase in gram-positive bacteria. FEMS Microbiol-ogy Reviews, 39: 541-554. Go to original source... Go to PubMed...
  32. Xiao W., Yan P.S., Wu H.Q., Lin F. (2014): Antagonizing Aspergillus parasiticus and promoting peanut growth of Bacillus isolated from peanut geocarposphere soil. Journal of Integrative Agriculture, 13: 2445-2451. Go to original source...
  33. Xu W.Y., Wang M.L., Sun X.X., Shu C.L., Zhang J., Geng L.L. (2021): Peanut (Arachis hypogaea L.) pod and rhizosphere harbored different bacte-rial communities. Rhizosphere, 19: 100373. Go to original source...
  34. Yang Z., Li L., Zhu W.J., Xiao S.Y., Chen S.Y., Liu J., Xu Q., Guo F., Lan S.L. (2022): Nitrogen fertilizer amount has minimal effect on rhizosphere bacterial diversity during different growth stages of peanut. PeerJ, 10: e13962. Go to original source... Go to PubMed...
  35. Zhang M., Wang L.F., Wan Y.S., Liu F.Z., Zhang K. (2017): Rational nitrogen strategies can improve peanut source supply capacity and pod yield. Agronomy Journal, 109: 2927. Go to original source...
  36. Zhao C.Z., Zhao S.Z., Hou L., Xia H., Wang J.S., Li C.S., Li A.Q., Li T.T., Zhang X.Y., Wang X.J. (2015): Proteomics analysis reveals differentially activated pathways that operate in peanut gynophores at different developmental stages. BMC Plant Biology, 15: 188. Go to original source... Go to PubMed...
  37. Zhao Y.H., Ma J.J., Li M., Deng L., Li G.H., Xia H., Zhao S.Z., Hou L., Li P.C., Ma C.L., Yuan M., Ren L., Gu J.Z., Guo B.Z., Zhao C.Z., Wang X.J. (2020): Whole-genome resequencing-based QTL-seq identified AhTc1 gene encoding a R2R3-MYB transcription factor controlling peanut purple testa colour. Plant Biotechnology Journal, 18: 96-105. Go to original source... Go to PubMed...
  38. Zharare G.E., Asher C.J., Blamey F.P.C. (2010): Magnesium antagonizes pod-zone calcium and zinc uptake by developing peanut pods. Journal of Plant Nutrition, 34: 1-11. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.