Abstract
Background and aims
Application of organic manure improves strawberry yield, but the underlying physiological and molecular mechanisms remain largely unclear.
Methods
Here, by integrating physio-biochemistry, metabolome and transcriptome analyses, we evaluated the effect of organic manure on the yield and quality of strawberry. Using garden waste and vermicompost as organic manure sources, five fertilization treatments were carried out in strawberry cultivation, including no fertilization, full inorganic nitrogen fertilizer, reduced inorganic nitrogen fertilizer (70% N), 70% N plus garden waste and 70% N plus vermicompost.
Results
The application of organic manure increased the yield, ascorbic acid content, nutrient levels and sugar/acid ratio but decreased the organic acid content in strawberry fruits. Furthermore, the increased organic manure accelerated the synthesis of sugars, amino acids, phenolic volatiles and flavonoids in strawberry fruits by reprogramming the regulatory network of transcripts and metabolites.
Conclusion
This study will help to ascertain the positive effects of the application of organic manure on the quality of strawberry fruits at the molecular level.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be made available on request.
References
Arancon NQ, Edwards CA, Bierman P, Metzger JD, Lee S, Welch C (2003) Effects of vermicompost on growth and marketable fruits of field-grown tomatoes, peppers and strawberries: The 7th international symposium on earthworm ecology. Pedobiologia 47(5):731–735. https://doi.org/10.1078/0031-4056-00251
Baur FJ, Ensminger LG (1977) The association of official analytical chemists (AOAC). Eur Soc Agron 54(4):171–172. https://doi.org/10.1007/BF02670789
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. Agr Ecosyst Environ 260:58–69. https://doi.org/10.1016/j.agee.2018.03.014
Carvalho FP (2017) Pesticides, environment, and food safety. Food Energy Secur 6(2):48–60. https://doi.org/10.1002/fes3.108
Chen M, Huang Y, Liu H, Xie S, Abbas F (2019) Impact of different nitrogen source on the compost quality and greenhouse gas emissions during composting of garden waste. Process Saf Environ Prot 124:326–335. https://doi.org/10.1016/j.psep.2019.03.006
Chen Q, Long Y, Yang M, Wang H, Sun Y, Liu X et al. (2022) FaPKc2.2 negatively modulates strawberry fruit ripening by reprograming the carbon metabolic pathway. Scientia Horticulturae 301, 111114. https://doi.org/10.1016/j.scienta.2022.111114
Chen S, Zhou Y, Chen Y, Gu J (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):884–890. https://doi.org/10.1093/bioinformatics/bty560
Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X et al (2013) A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: Application in the study of rice metabolomics. Mol Plant 6(6):1769–1780. https://doi.org/10.1093/mp/sst080
Cheng M, Wang H, Fan J, Xiang Y, Tang Z, Pei S et al (2021) Effects of nitrogen supply on tomato yield, water use efficiency and fruit quality: A global meta-analysis. Sci Hortic 290:110553. https://doi.org/10.1016/j.scienta.2021.110553
De CU (2020) Agricultural waste recycling in horticultural intensive farming systems by on-farm composting and compost-based tea application improves soil quality and plant health: A review under the perspective of a circular economy. Sci Total Environ 738:139840. https://doi.org/10.1016/j.scitotenv.2020.139840
Deng B, Li Y, Xu D, Ye Q, Liu G (2019) Nitrogen availability alters flavonoid accumulation in Cyclocarya paliurus via the effects on the internal carbon/nitrogen balance. Sci Rep 9(1):1–9. https://doi.org/10.1038/s41598-019-38837-8
Dong NQ, Lin HX (2021) Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol 63(1):180–209. https://doi.org/10.1111/jipb.13054
Fan H, Zhang Y, Li J, Jiang J, Waheed A, Wang S et al (2023) Effects of organic fertilizer supply on soil properties, tomato yield, and fruit quality: A global meta-analysis. Sustainability 15(3):2556. https://doi.org/10.3390/su15032556
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF et al (2010) Significant acidification in major Chinese croplands. Science 327(5968):1008–1010. https://doi.org/10.1126/science.1182570
Guo L, Wu G, Li Y, Li C, Liu W, Meng J et al (2016) Effects of cattle manure compost combined with chemical fertilizer on topsoil organic matter, bulk density and earthworm activity in a wheat-maize rotation system in Eastern China. Soil & Tillage Res 156:140–147. https://doi.org/10.1016/j.still.2015.10.010
Gupta AK, Tripathi VK (2012) Efficacy of Azotobacter and vermicompost alone and in combination on vegetative growth, flowering and yield of strawberry (Fragaria x ananassa Duch.) cv. Chandler. Progressive Horticulture 44, 256–261. https://www.researchgate.net/publication/326247188
Han ML, Lv QY, Zhang J, Wang T, Zhang CX, Tan RJ et al. (2022) Decreasing nitrogen assimilation under drought stress by suppressing DST-mediated activation of Nitrate Reductase 1.2 in rice. Molecular Plant, 15(1), 167–178. https://doi.org/10.1016/j.molp.2021.09.005
Hu H, Fei X, He B, Chen X, Ma L, Han P et al (2022) UPLC-MS/MS profile combined with RNA-Seq reveals the amino acid metabolism in Zanthoxylum bungeanum leaves under drought stress. Front Nutr 9:921742. https://doi.org/10.3389/fnut.2022.921742
Huang H, Yao Q, Xia E, Gao L (2018) Metabolomics and transcriptomics analyses reveal nitrogen influences on the accumulation of flavonoids and amino acids in young shoots of tea plant (Camellia sinensis L.) associated with tea flavor. Journal of Agricultural and Food Chemistry 66(37), 9828–9838. https://doi.org/10.1021/acs.jafc.8b01995
Imran A, Sardar F, Khaliq Z, Nawaz MS, Shehzad A, Ahmad M et al (2021) Tailored bioactive compost from agri-waste improves the growth and yield of chili pepper and tomato. Front Bioeng Biotechnol 9:787764. https://doi.org/10.3389/fbioe.2021.787764
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M et al. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Research 36(suppl_1), 480–484. https://doi.org/10.1093/nar/gkm882
Kim KH, Kabir E, Jahan SA (2017) Exposure to pesticides and the associated human health effects. Sci Total Environ 575:525–535. https://doi.org/10.1016/j.scitotenv.2016.09.009
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9(1):559. https://doi.org/10.1186/1471-2105-9-559
Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of Paraquat. Biochemical Journal 210(3), 899–903. https://doi.org/10.1042/bj2100899
Leonardou VK, Doudoumis E, Tsormpatsidis E, Vysini E, Papanikolopoulos T, Papasotiropoulos V et al (2021) Quality traits, volatile organic compounds, and expression of key flavor genes in strawberry genotypes over harvest period. Int J Mol Sci 22(24):13499. https://doi.org/10.3390/ijms222413499
Li M, Li P, Ma F, Dandekar AM, Cheng L (2018) Sugar metabolism and accumulation in the fruit of transgenic apple trees with decreased sorbitol synthesis. Horticulture Res 5:60. https://doi.org/10.1038/s41438-018-0064-8
Li W, Lu X, Li J (2022) The effect of organic nutrient solution on flavor in ripe cherry tomato fruit-Transcriptome and metabolomic analyses. Environ Exp Bot 194:104721. https://doi.org/10.1016/j.envexpbot.2021.104721
Li Y, Lv Y, Lian M, Peng F, Xiao Y (2021) Effects of combined glycine and urea fertilizer application on the photosynthesis, sucrose metabolism, and fruit development of peach. Sci Hortic 289:110504. https://doi.org/10.1016/j.scienta.2021.110504
Liu J, Shu A, Song W, Shi W, Li M, Zhang W et al (2021) Long-term organic fertilizer substitution increases rice yield by improving soil properties and regulating soil bacteria. Geoderma 404:115287. https://doi.org/10.1016/j.geoderma.2021.115287
Liu S, Zhang P, Wang X, Hakeem A, Niu M, Song S et al (2024) Comparative analysis of different bio-organic fertilizers on growth and rhizosphere environment of grapevine seedlings. Sci Hortic 324:112587. https://doi.org/10.1016/j.scienta.2023.112587
Liu L, Xiao W, Ji ML, Yang C, Li L, Gao DS et al (2017) Effects of molybdenum on nutrition, quality, and flavor compounds of strawberry (Fragaria × ananassa Duch. cv. Akihime) fruit. J Integr Agric 16:1502–1512. https://doi.org/10.1016/S2095-3119(16)61518-6
Liu Y, Li M, Xu J, Liu X, Wang S, Shi L (2019) Physiological and metabolomics analyses of young and old leaves from wild and cultivated soybean seedlings under low-nitrogen conditions. BMC Plant Biol 19(1):389. https://doi.org/10.1186/s12870-019-2005-6
Lu J, Shao G, Gao Y, Zhang K, Wei Q, Cheng J (2021) Effects of water deficit combined with soil texture, soil bulk density and tomato variety on tomato fruit quality: a meta-analysis. Agric Water Manage 243:106427. https://doi.org/10.1016/j.agwat.2020.106427
Marzouk HA, Kassem HA (2011) Improving fruit quality, nutritional value and yield of Zaghloul dates by the application of organic and/or mineral fertilizers. Sci Hortic 127(3):249–254. https://doi.org/10.1016/j.scienta.2010.10.005
Negi YK, Sajwan P, Uniyal S, Mishra AC (2021) Enhancement in yield and nutritive qualities of strawberry fruits by the application of organic manures and biofertilizers. Sci Hortic 283:110038. https://doi.org/10.1016/j.scienta.2021.110038
Ombita SN, Mwendwa SM, Mureithi SM (2024) Influence of organic fertilization on growth and yield of strawberry (Fragaria × ananassa Duch) in Kabete and Mbooni areas. Kenya Heliyon 10(3):e25324. https://doi.org/10.1016/j.heliyon.2024.e25324
Pandey C, Bajpai VK, Negi YK, Rather IA, Maheshwari DK (2018) Effect of plant growth promoting Bacillus spp. On nutritional properties of Amaranthus hypochondriacus grains. Saudi J Biol Sci 25:1066–1071. https://doi.org/10.1016/j.sjbs.2018.03.003
Siti NBBK, Irnis AZ, Tengku NTI (2018) Composting of garden waste using indigenous microorganisms (IMO) as organic additive. Journal of Integrative Agriculture 10, 140–145. https://doi.org/10.30880/ijie.2018.10.09.026
Salvato F, Wilson R, Portilla L, Kiyota E, Lima RK, Boaretto LF et al (2017) Luxurious nitrogen fertilization of two sugar cane genotypes contrasting for lignin composition causes changes in the stem proteome related to carbon, nitrogen, and oxidant metabolism but does not alter lignin content. J Proteome Res 16(10):3688–3703. https://doi.org/10.1021/acs.jproteome.7b00397
Santos FP, Saviani EE, Salgad I, Oliveira HC (2014) The effect of nitrate assimilation deficiency on the carbon and nitrogen status of Arabidopsis thaliana plants. Amino Acids 46(4):1121–1129. https://doi.org/10.1007/s00726-014-1674-6
Song QA, Catlin NS, Brad BW, Li S (2019) Computational analysis of alternative splicing in plant genomes. Gene 685:186–195. https://doi.org/10.1016/j.gene.2018.10.026
Sun R, Dsouza M, Gilbert JA, Guo X, Wang D, Guo Z et al (2016) Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ Microbiol 18(12):5137–5150. https://doi.org/10.1111/1462-2920.13512
Tammam AA, Shehata MR, Pessarakli M, ElAggan WH (2023) Vermicompost and its role in alleviation of salt tress in plants–II. Impact of vermicompost on the physiological responses of salt-stressed plants. Journal of Plant Nutrition 46(7), 1458–1478. https://doi.org/10.1080/01904167.2022.2072742
Tang Q, Cotton A, Wei Z, Xia Y, Daniell T, Yan X (2022) How does partial substitution of chemical fertilizer with organic forms increase sustainability of agricultural production? Sci Total Environ 803:149933. https://doi.org/10.1016/j.scitotenv.2021.149933
Tits M, Elsen A, Bries J, Vandendriessche H (2012) Short-term and long-term effects of vegetable, fruit and garden waste compost applications in an arable crop rotation in Flanders. Plant Soil 376:43–59. https://doi.org/10.1007/s11104-012-1318-0
Wang F, Ge S, Xu X, Xing Y, Du X, Zhang X et al (2021) Multiomics analysis reveals new insights into the apple fruit quality decline under high nitrogen conditions. J Agric Food Chem 69(19):5559–5572. https://doi.org/10.1021/acs.jafc.1c01548
Wang J, Song Y, Ma T, Raza W, Li J, Howland JG et al (2017) Impacts of inorganic and organic fertilization treatments on bacterial and fungal communities in a paddy soil. Appl Soil Ecol 112:42–50. https://doi.org/10.1016/j.apsoil.2017.01.005
Wang M, Wang Y, Li, X., Zhang, Y., Chen, X., Liu, J., et al. (2024). Integration of metabolomics and transcriptomics reveals the regulation mechanism of the phenylpropanoid biosynthesis pathway in insect resistance traits in Solanum habrochaites. Horticult Res, 11(2), uhad277. https://doi.org/10.1093/hr/uhad277
Wei Z, Ying H, Guo X, Zhuang M, Cui Z, Zhang F (2020) Substitution of mineral fertilizer with organic fertilizer in maize systems: s meta-analysis of reduced nitrogen and carbon emissions. Agronomy 10(8):1149. https://doi.org/10.3390/agronomy10081149
Xiao J, Gu C, He S, Zhu D, Huang Y, Zhou Q (2021) Widely targeted metabolomics analysis reveals new biomarkers and mechanistic insights on chestnut (Castanea mollissima BL.) calcification process. Food Res Intl 141, 110128. https://doi.org/10.1016/j.foodres.2021.110128
Xing Y, Zhang F, Wu L, Fan J, Zhang Y, Li J (2015) Determination of optimal amount of irrigation and fertilizer under drip fertigated system based on tomato yield, quality, water and fertilizer use efficiency. Trans Chinese Soc Agric Eng 31:110–121. https://doi.org/10.3969/j.issn.1002-6819.2015.z1.014
Xu F, Liu Y, Du W, Li C, Xu M, Xie T et al (2021) Response of soil bacterial communities, antibiotic residuals, and crop yields to organic fertilizer substitution in North China under wheat-maize rotation. Sci Total Environ 785:147248. https://doi.org/10.1016/j.scitotenv.2021.147248
Xu Y, Luo B, Jia R, Xiao J, Wang X, Yang Y et al (2024) Quantifying synergies and trade-offs in the food-energy-soil-environment nexus under organic fertilization. J Environ Manage 349:119526. https://doi.org/10.1016/j.jenvman.2023.119526
Yang H, Wu Y, Duan Y, Zhang C, Huang Z, Wu W et al (2022) Metabolomics combined with physiological and transcriptomic analyses reveal regulatory features associated with blueberry growth in different soilless substrates. Sci Hortic 302:111145. https://doi.org/10.1016/j.scienta.2022.111145
Zhong C, Jian SF, Chen DL, Huang XJ, Miao JH (2021) Organic nitrogen sources promote andrographolide biosynthesis by reducing nitrogen metabolism and increasing carbon accumulation in Andrographis paniculata. Plant Physiol Biochem 164:82–91. https://doi.org/10.1016/j.plaphy.2021.04.016
Zou C, Lu T, Wang R, Xu P, Jing Y, Wang R, Xu J, Wan J (2022) Comparative physiological and metabolomic analyses reveal that Fe3O4 and ZnO nanoparticles alleviate Cd toxicity in tobacco. J Nanobiotechnology 20:302. https://doi.org/10.1186/s12951-022-01509-3
Zuo Y, Zhang J, Zhao R, Dai H, Zhang Z (2018) Application of vermicompost improves strawberry growth and quality through increased photosynthesis rate, free radical scavenging and soil enzymatic activity. Sci Hortic 233:132–140. https://doi.org/10.1016/j.scienta.2018.01.023
Funding
This work was supported by the ‘1331 Project’ Construction Plan of Shanxi Province (20211331–15) and the Key Research and Development Project of Shanxi Province (201903D211011).
Author information
Authors and Affiliations
Contributions
Min Wu: Investigation, Methodology, Data curation, Roles/Writing -original draft. Panting Zhao: Investigation, Methodology, Data curation. Lizhi Liu: Investigation, Methodology. Qi Zhao: Investigation, Methodology. Qian Li: Investigation, Methodology. Lei Li: Conceptualization, Funding acquisition, Supervision. Jin Xu: Conceptualization, Writing-review & editing, Supervision.
Corresponding authors
Ethics declarations
Competing interest
The authors have no conflict of interest to declare.
Additional information
Responsible Editor: Mian Gu.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wu, M., Zhao, P., Liu, L. et al. The organic manure-improved yield and quality in strawberries is attributed to metabolic reprogramming to increase amino acids, sugar/acid ratio, flavonoids and phenolic volatiles. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06651-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-024-06651-5