journal article Open Access Nov 28, 2024

Synthetic Microbial Community Isolated from Intercropping System Enhances P Uptake in Rice

View at Publisher Save 10.3390/ijms252312819
Abstract
Changes in root traits and rhizosphere microbiome are important ways to optimize plant phosphorus (P) efficiency and promote multifunctionality in intercropping. However, whether and how synthetic microbial communities isolated from polyculture systems can facilitate plant growth and P uptake are still largely unknown. A field experiment was first carried out to assess the rice yield and P uptake in the rice/soybean intercropping systems, and a synthetic microbial community (SynCom) isolated from intercropped rice was then constructed to elucidate the potential mechanisms of growth-promoting effects on rice growth and P uptake in a series of pot experiments. Our results showed that the yield and P uptake of intercropped rice were lower than those of rice grown in monoculture. However, bacterial networks in the rice rhizosphere were more stable in polyculture, exhibiting more hub nodes and greater modularity compared to the rice monoculture. A bacterial synthetic community (SynCom) composed of four bacterial strains (Variovorax paradoxus, Novosphingobium subterraneum, Hydrogenophaga pseudoflava, Acidovorax sp.) significantly enhanced the biomass and P uptake of potted rice plants. These growth-promoting effects are underpinned by multiple pathways, including the direct activation of soil available P, increased root surface area and root tip number, reduced root diameter, and promotion of root-to-shoot P translocation through up-regulation of Pi transporter genes (OsPht1;1, OsPht1;2, OsPht1;4, OsPht1;6). This study highlights the potential of harnessing synthetic microbial communities to enhance nutrient acquisition and improve crop production.
Topics

No keywords indexed for this article. Browse by subject →

References
62
[1]
Crusciol "Upland rice intercropped with forage grasses in an integrated crop-livestock system: Optimizing nitrogen management and food production" Field Crops Res. (2021) 10.1016/j.fcr.2020.108008
[2]
Yadav "Impact of no-till and mulching on soil carbon sequestration under rice (Oryza sativa L.)-rapeseed (Brassica campestris L. var. rapeseed) cropping system in hilly agro-ecosystem of the Eastern Himalayas, India" Agric. Ecosyst. Environ. (2019) 10.1016/j.agee.2019.02.001
[3]
Caine "Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions" New Phytol. (2019) 10.1111/nph.15344
[4]
Surendran "Use of efficient water saving techniques for production of rice in India under climate change scenario: A critical review" J. Clean. Prod. (2021) 10.1016/j.jclepro.2021.127272
[5]
Singh "Growing more rice with less water" Curr. Sci. (2021)
[6]
Fukai "Factors determining water use efficiency in aerobic rice" Crop Environ. (2022) 10.1016/j.crope.2022.03.008
[7]
Girsang "Soil aeration and relationship to inorganic nitrogen during aerobic cultivation of irrigated rice on a consolidated land parcel" Soil Tillage Res. (2020) 10.1016/j.still.2020.104647
[8]
Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology

Rob W. Brooker, Alison E. Bennett, Wen‐Feng Cong et al.

New Phytologist 2015 10.1111/nph.13132
[9]
Betencourt "Intercropping promotes the ability of durum wheat and chickpea to increase rhizosphere phosphorus availability in a low P soil" Soil Biol. Biochem. (2012) 10.1016/j.soilbio.2011.11.015
[10]
Xiao "Wheat growth is stimulated by interspecific competition after faba bean attains its maximum growth rate" Crop Sci. (2019) 10.2135/cropsci2018.03.0155
[11]
Ma "Maize/alfalfa intercropping enhances yield and phosphorus acquisition" Field Crops Res. (2023) 10.1016/j.fcr.2023.109136
[12]
P for Two, Sharing a Scarce Resource: Soil Phosphorus Acquisition in the Rhizosphere of Intercropped Species

Philippe Hinsinger, Elodie Betencourt, Laetitia Bernard et al.

Plant Physiology 2011 10.1104/pp.111.175331
[13]
Sun "The relative contributions of pH, organic anions, and phosphatase to rhizosphere soil phosphorus mobilization and crop phosphorus uptake in maize/alfalfa polyculture" Plant Soil (2020) 10.1007/s11104-019-04110-0
[14]
Devau "A mechanistic model for understanding root-induced chemical changes controlling phosphorus availability" Ann. Bot. (2010) 10.1093/aob/mcq098
[15]
Root exudates drive interspecific facilitation by enhancing nodulation and N 2 fixation

Bai Li, Yu-Ying Li, Hua-Mao Wu et al.

Proceedings of the National Academy of Sciences 2016 10.1073/pnas.1523580113
[16]
Liu, X., Jiao, Y., Zhao, X., Yu, X., Zhang, Q., Li, S., Ma, L., Tang, W., Yang, C., and Yang, G. (2023). Root architecture of forage species varies with intercropping combinations. Agronomy, 13. 10.3390/agronomy13092223
[17]
Li "Plant diversity and overyielding: Insights from belowground facilitation of intercropping in agriculture" New Phytol. (2014) 10.1111/nph.12778
[18]
Homulle "Root traits with team benefits: Understanding belowground interactions in intercropping systems" Plant Soil (2021) 10.1007/s11104-021-05165-8
[19]
Song "Growth promotion ability of phosphate-solubilizing bacteria from the soybean rhizosphere under maize–soybean intercropping systems" J. Sci. Food Agric. (2022) 10.1002/jsfa.11477
[20]
Signal communication during microbial modulation of root system architecture

Yucong Li, Yu Chen, Yansong Fu et al.

Journal of Experimental Botany 2024 10.1093/jxb/erad263
[21]
Verbon "Beneficial microbes affect endogenous mechanisms controlling root development" Trends Plant Sci. (2016) 10.1016/j.tplants.2016.01.013
[22]
Zhang "Soil phosphorus fractionation and its association with soil phosphate-solubilizing bacteria in a chronosequence of vegetation restoration" Ecol. Eng. (2021) 10.1016/j.ecoleng.2021.106208
[23]
The Role of Synthetic Microbial Communities (SynCom) in Sustainable Agriculture

Ambihai Shayanthan, Patricia Ann C. Ordoñez, Ivan John Oresnik

Frontiers in Agronomy 10.3389/fagro.2022.896307
[24]
Evaluation of ready-to-use freezer stocks of a synthetic microbial community for maize root colonization

J. Jacob Parnell, Simina Vintila, Clara Tang et al.

Microbiology Spectrum 2024 10.1128/spectrum.02401-23
[25]
De Souza, R.S.C., Armanhi, J.S.L., and Arruda, P. (2020). From microbiome to traits: Designing synthetic microbial communities for improved crop resiliency. Front. Plant Sci., 11. 10.3389/fpls.2020.01179
[26]
Harnessing the plant microbiome for environmental sustainability: From ecological foundations to novel applications

Jing-Ru Hao, Yan Li, Yuan Ge

Science of The Total Environment 2024 10.1016/j.scitotenv.2024.175766
[27]
Li "Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils" Proc. Natl. Acad. Sci. USA (2007) 10.1073/pnas.0704591104
[28]
Jadhav "Weed management in rice–soybean intercropping system under rainfed condition of Marathwada region of Maharshtra" J. Crop Weed (2014)
[29]
Jin "Fusaric acid mediates the assembly of disease-suppressive rhizosphere microbiota via induced shifts in plant root exudates" Nat. Commun. (2024) 10.1038/s41467-024-49218-9
[30]
Root microbiota confers rice resistance to aluminium toxicity and phosphorus deficiency in acidic soils

Chaoyang Liu, Meitong Jiang, Mengting Maggie Yuan et al.

Nature Food 2023 10.1038/s43016-023-00848-0
[31]
Li "Salt-induced recruitment of specific root-associated bacterial consortium capable of enhancing plant adaptability to salt stress" Int. J. Syst. Evol. Microbiol. (2021)
[32]
Li, S., and Wu, F. (2018). Diversity and co-occurrence patterns of soil bacterial and fungal communities in seven intercropping systems. Front. Microbiol., 9. 10.3389/fmicb.2018.01521
[33]
Pang, Z., Fallah, N., Weng, P., Zhou, Y., Tang, X., Tayyab, M., Liu, Y., Liu, Q., Xiao, Y., and Hu, C. (2022). Sugarcane–peanut intercropping system enhances bacteria abundance, diversity, and sugarcane parameters in rhizospheric and bulk soils. Front. Microbiol., 12. 10.3389/fmicb.2021.815129
[34]
Jain "The flavonoid naringenin enhances intercellular colonization of rice roots by Azorhizobium caulinodans" Biol. Fertil. Soils (2003) 10.1007/s00374-003-0599-0
[35]
Makrushin "Changes in motility of the rhizobacterium Azospirillum brasilense in the presence of plant lectins" Microbiol. Res. (2009) 10.1016/j.micres.2006.11.008
[36]
Morris "Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates" Plant Physiol. (1998) 10.1104/pp.117.4.1171
[37]
Wang, Z.G., Jin, X., Bao, X.G., Li, X.F., Zhao, J.H., Sun, J.H., Christie, P., and Li, L. (2014). Intercropping enhances productivity and maintains the most soil fertility properties relative to sole cropping. PLoS ONE, 9. 10.1371/journal.pone.0113984
[38]
Root Structure and Functioning for Efficient Acquisition of Phosphorus: Matching Morphological and Physiological Traits

Hans Lambers, MICHAEL W. SHANE, MICHAEL D. CRAMER et al.

Annals of Botany 2006 10.1093/aob/mcl114
[39]
Lambers "Phosphorus acquisition and utilization in plants" Annu. Rev. Plant Biol. (2022) 10.1146/annurev-arplant-102720-125738
[40]
Magadlela "The metabolic potential of soil microorganisms and enzymes in phosphorus-deficient KwaZulu-Natal grassland ecosystem soils" Appl. Soil Ecol. (2023) 10.1016/j.apsoil.2022.104647
[42]
Moreira "Phosphorus recovery from phosphate rocks using phosphate-solubilizing bacteria" Geomicrobiol. J. (2019) 10.1080/01490451.2018.1534901
[43]
Sitlaothaworn, K., Yukphan, P., Budsabun, T., Charoenyingcharoen, P., Phongsopitanun, W., Savarajara, A., and Tanasupawat, S. (2023). Novosphingobium kaempferiae sp. nov., a phosphate-solubilizing bacterium isolated from stem of Kaempferia marginata Carey. Int. J. Syst. Evol. Microbiol., 73. 10.1099/ijsem.0.005746
[44]
Rott "Organophosphonates: A review on environmental relevance, biodegradability and removal in wastewater treatment plants" Sci. Total Environ. (2018) 10.1016/j.scitotenv.2017.09.223
[45]
Sukumar "Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions" Plant Cell Env. (2013) 10.1111/pce.12036
[46]
Pereira "Prospecting plant growth-promoting bacteria isolated from the rhizosphere of sugarcane under drought stress" Curr. Microbiol. (2019) 10.1007/s00284-019-01749-x
[47]
Ilangumaran, G., Subramanian, S., and Smith, D.L. (2024). Complete genome sequences of Rhizobium sp. strain SL42 and Hydrogenophaga sp. strain SL48, microsymbionts of Amphicarpaea bracteata. Front. Microbiomes, 3. 10.3389/frmbi.2024.1309947
[48]
Lee "Effect of Novosphingobium sp. CuT1 inoculation on the rhizoremediation of heavy metal-and diesel-contaminated soil planted with tall fescue" Environ. Sci. Pollut. Res. (2023) 10.1007/s11356-022-23339-4
[49]
Lu "Molecular mechanisms and genetic improvement of low-phosphorus tolerance in rice" Plant Cell Environ. (2023) 10.1111/pce.14457
[50]
Ai "Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation" Plant J. (2009) 10.1111/j.1365-313x.2008.03726.x

Showing 50 of 62 references

Metrics
11
Citations
62
References
Details
Published
Nov 28, 2024
Vol/Issue
25(23)
Pages
12819
License
View
Funding
National Natural Science Foundation of China Award: 32101398
Jilin Science and Technology Development Plan Project Award: 32101398
Cite This Article
Huimin Ma, Hongcheng Zhang, Congcong Zheng, et al. (2024). Synthetic Microbial Community Isolated from Intercropping System Enhances P Uptake in Rice. International Journal of Molecular Sciences, 25(23), 12819. https://doi.org/10.3390/ijms252312819
Related

You May Also Like