Rhizosphere ecological restoration: interactions between nutrient mobilization, core microbial assembly, and phenylalanine metabolism circulation

Abstract

Continuous cropping obstacles (CCOs) constitute a major threat to agricultural productivity and environmental quality. Despite the recognized significance of rhizosphere restoration for CCOs, the mechanisms underlying rhizosphere restoration are not well understood. We conducted a pot experiment by planting Panax notoginseng with the addition of biochar, plant ash, the combination of biochar and plant ash (biochar:plant ash=4:1) or without any addition of biochar and plant ash. We found that rhizosphere soil with planting P. notoginseng, without any addition of biochar and plant ash, had a more homogeneous fungal community structure than soils added either with biochar, plant ash or the combination of biochar and plant ash. Among all treatments, the rhizosphere soil added with the combination of biochar and plant ash had the highest fungal and bacterial alpha-diversity. The combination of biochar and plant ash addition also enriched AMF Rhizophagus (TOP3 diff genus) in the rhizosphere soil compared to that without any biochar and plant ash addition. The co-occurrence network analysis demonstrated that Rhizophagus assembled a core microbial functional circle which helped suppress pathogens by promoting competition for amino acids and improving phenolic acid utilization, nutrient availability, and soil pH. Moreover, the metabolomic analysis revealed that the rhizosphere soil with the combination of biochar and plant ash addition upregulated the phenylalanine-tyrosine-tryptophan biosynthesis pathway, resulting in a decline of phenolic acid production and an increase amino acid accumulation in comparison with that without any biochar and ash addition (OPLS - DA, VIP > 1, FC ≥ 2, FC ≤ 0.5). Our results highlighted the importance of the interplay among keystone microbial species, pH and key metabolites in the rhizosphere soil in mitigating CCOs, building a framework for developing effective management for CCOs.

Keywords

Rhizosphere / Continuous cropping barriers / Biochar / AMF / Phenylalanine pathway

References

[1] BaiB, LiuW, QiuX, ZhangJ, ZhangJ, BaiYJJ. The root microbiome: community assembly and its contributions to plant fitness. J Integr Plant Biol, 2022.

[2] BaiYC, YangCQ, HalitschkeR, PaetzC, KesslerD, BurkardK, GaquerelE, BaldwinIT, LiDP. Natural history-guided omics reveals plant defensive chemistry against leafhopper pests. Science, 2022, 375514.

[3] BaoL, LiuY, DingY, ShangJ, WeiY, TanY, et al.. Interactions between phenolic acids and microorganisms in rhizospheric soil from continuous cropping of Panax notoginseng. Front Microbiol, 2022, 13. 791603

[4] BeneduziA, AmbrosiniA, PassagliaLMPJG, BiologyM. Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Gene Mol Biol, 2012, 35: 1044-1051.

[5] BerendsenRL, VismansG, YuK, SongY, de JongeR, BurgmanWP, et al.. Disease-induced assemblage of a plant-beneficial bacterial consortium. Isme J, 2018, 12: 1496-1507.

[6] CaporasoJG, KuczynskiJ, StombaughJ, BittingerK, BushmanFD, CostelloEK, et al.. QIIME allows analysis of high-throughput community sequencing data. Nat Methods, 2010, 7: 335-336.

[7] ChenYD, DuJF, LiY, TangH, YinZY, YangL, DingXH. Evolution and management of soil microbial community structure under continuous cropping. Front Microbiol, 2022, 13. 839494

[8] DamVNM, BouwmeesterHJ. Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci, 2016, 21: 256-265.

[9] DebrayR, HerbertRA, JaffeAL, Crits-ChristophA, PowerME, KoskellaB. Priority effects in microbiome assembly. Nat Rev Microbiol, 2022, 20: 109-121.

[10] DongL, XuJ, FengG, LiX, ChenS. Soil bacterial and fungal community dynamics associated with Panax notoginseng death rate in a continuous cropping system. Sci Rep, 2016, 631802.

[11] DrorB, AmutuhaireH, FrenkelO, JurkevitchE, CytrynE. Identification of bacterial populations and functional mechanisms involved in biochar-facilitated antagonism against the soilborne pathogen Fusarium oxysporum. Phytobio J, 2022, 6: 139-150.

[12] DuS, TrivediP, WeiZ, FengJ, HuH, BiL, et al.. The proportion of soil-borne fungal pathogens increases with elevated organic carbon in agricultural soils. Msystems, 2022.

[13] EisenhauerN, SchulzW, ScheuS, JoussetA. Niche dimensionality links biodiversity and invasibility of microbial communities. Funct Ecol, 2013, 27: 282-288.

[14] El-SharkawyHHA, RashadYM, ElazabNT. Synergism between Streptomyces viridosporus HH1 and Rhizophagus irregularis effectively induces defense responses against Fusarium wilt of pea and improves plant growth and yield. J Fungi, 2022, 87683.

[15] GaoZZ, LiPW, LiCZ, TangRC, WangMH, ChenJZ, YangY, HeZX, XiaoZH, MaYZ, ChenYZ. Identification, functional annotation, and isolation of phosphorus-solubilizing bacteria in the rhizosphere soil of Glycyrrhiza uralensis (Fisch.) Sojak. Appl Soil Ecol, 2024, 194. 105207

[16] GuerrieriE, RasmannS. Exposing belowground plant communication. Science, 2024, 384: 272-273.

[17] GuptaR, AnandG, GaurR, YadavDJP, PlantsMB. Plant–microbiome interactions for sustainable agriculture: a review. Physiol Mol Biol Plants, 2021, 27: 165-179.

[18] HuL, RobertCAM, CadotS, ZhangX, YeM, LiB, ManzoD, ChervetN, SteingerT, Van Der HeijdenMGA, SchlaeppiK, ErbM. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun, 2018, 92738.

[19] HuangAC, OsbournAJ. Plant terpenes that mediate below-ground interactions: prospects for bioengineering terpenoids for plant protection. Pest Manag Sci, 2019, 75: 2368-2377.

[20] JacobyRP, KoprivaSJ. Metabolic niches in the rhizosphere microbiome: new tools and approaches to analyse metabolic mechanisms of plant–microbe nutrient exchange. J Exp Bot, 2019, 70: 1087-1094.

[21] JaiswalAK, AlkanN, EladY, SelaN, PhilosophAM, GraberER, et al.. Molecular insights into biochar-mediated plant growth promotion and systemic resistance in tomato against Fusarium crown and root rot disease. Sci Rep, 2020, 1013934.

[22] LehmannJ, RilligMC, ThiesJE, MasielloCA, HockadayWC, CrowleyDE. Biochar effects on soil biota—a review. Soil Biol Biochem, 2011, 43: 1812-1836.

[23] LiG, ChenJ, LiZ, WuW, YangHJ. Analysis of patent data of Panax notoginseng and enlightenment of industrial development. J Chin Med Mater, 2020, 45(5): 1011-1022.

[24] LiWT, LuQ, AlharbiSA, SoromotinAV, KuzyakovY, LeiYB. Plant–soil–microbial interactions mediate vegetation succession in retreating glacial forefields. Sci Total Environ, 2023, 873162393.

[25] LiY, FangF, WeiJ, WuX, CuiR, LiG, et al.. Humic acid fertilizer improved soil properties and soil microbial diversity of continuous cropping peanut: a three-year experiment. Sci Rep, 2019, 912014.

[26] LiuC, XiaR, TangM, ChenX, ZhongB, LiuX, et al.. Improved ginseng production under continuous cropping through soil health reinforcement and rhizosphere microbial manipulation with biochar: a field study of Panax ginseng from Northeast China. Hortic Res, 2022, 9uhac108.

[27] MaL, WangWQ, ShiR, ZhangX, LiX, YangYS, et al.. Effects of organic acids on the chemotaxis profiles and biocontrol traits of antagonistic bacterial endophytes against root-rot disease in Panax notoginseng. Antonie van Leeuwenhoek, 2021, 114(11): 1771-1789.

[28] MaX, GengQ, ZhangH, BianC, ChenHYH, JiangD, et al.. Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multi-functionality. New Phytol, 2020, 229(5): 2957-2969.

[29] MulkS, WahabA, YasminH, MumtazS, El-SerehyHA, KhanN, et al.. Prevalence of wheat associated Bacillus spp. and their bio-control efficacy against Fusarium root rot. Front Microbiol, 2022, 12798619.

[30] PervaizZH, IqbalJ, ZhangQ, ChenD, WeiH, SaleemMJ. Continuous cropping alters multiple biotic and abiotic indicators of soil health. Soil Syst, 2020, 4459.

[31] PowellJR, RilligMC. Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol, 2018, 220(4): 1059-1075.

[32] RognesT, FlouriT, NicholsB, QuinceC, MahéF. VSEARCH: a versatile open source tool for metagenomics. PeerJ, 2016, 4e2584.

[33] SaleemM, HuJ, JoussetA. More than the sum of its parts: microbiome biodiversity as a driver of plant growth and soil health. Annu Rev Ecol Evol Syst, 2019, 50: 145-168.

[34] SchindlerDE, ArmstrongJB, ReedTE. The portfolio concept in ecology and evolution. Front Ecol Environ, 2015, 13: 257-263.

[35] ShuX, ZhangKR, ZhangQF, WangWB. Response of soil physico-chemical properties to restoration approaches and submergence in the water level fluctuation zone of the Danjiangkou Reservoir, China. Ecotoxicol Environ Saf, 2017, 145: 119-125.

[36] SpagnolettiFN, CarmonaMA, BalestrasseK, ChiocchioVM, GiacomettiR, LavadoRS. The arbuscular mycorrhizal fungus Rhizophagus intraradices reduces the root rot caused by Fusarium pseudograminearum in wheat. Rhizosphere, 2021, 19. 100369

[37] TanY, CuiY, LiH, KuangA, LiX, WeiY, JiX. Diversity and composition of rhizospheric soil and root endogenous bacteria in Panax notoginseng during continuous cropping practices. J Basic Microbiol, 2017, 57: 337-344.

[38] TanY, CuiY, LiH, KuangA, LiX, WeiY, JiX. Rhizospheric soil and root endogenous fungal diversity and composition in response to continuous Panax notoginseng cropping practices. Microbiol Res, 2017, 194: 10-19.

[39] TrivediP, LeachJE, TringeSG, SaT, SinghBK. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol, 2021, 18: 607-621.

[40] WangRT, LiuJX, JiangWY, JiPS, LiYG. Metabolomics and microbiomics reveal impacts of rhizosphere metabolites on Alfalfa continuous cropping. Front Microbiol, 2022, 13. 833968

[41] XiangW, ChenJ, ZhangF, HuangR, LiL. Autotoxicity in Panax notoginseng of root exudates and their allelochemicals. Front Plant Sci, 2022, 131020626.

[42] XuW, WhitmanWB, GundaleMJ, ChienCC, ChiuCY. Functional response of the soil microbial community to biochar applications. Change Biol Bioenergy, 2021, 13(1): 269-281.

[43] XuW, WuF, WangH, ZhaoL, LiuX, XiangP, GuanH, MaL. Key soil parameters affecting the survival of under continuous cropping. Sci Rep, 2021, 115656.

[44] XuCC, ZhangNF, ZhangKH, LiSH, XiaQ, XiaoJ, LiangMJ, LeiW, HeJ, ChenGP, GeCJ, ZhengXH, ZhuJG, HuSJ, KoideRT, FirestoneMK, ChengL. Large losses of ammonium-nitrogen from a rice ecosystem under elevated CO2. Sci Adv, 2020, 6eabb7433.

[45] XuCC, ZhangNF, ZhangKH, LiSH, XiaQ, XiaoJ, LiangMJ, LeiW, HeJ, ChenGP, GeCJ, ZhengXH, ZhuJG, HuSJ, KoideRT, FirestoneMK, ChengL. Coupled anaerobic methane oxidation and metal reduction in soil under elevated CO2. Global Change Biol, 2023, 29: 670-685.

[46] Yang M, Chuan Y, Guo C, Liao J, Xu Y, Mei X, Liu Y, Huang H, He X, Zhu S (2018) Root cell death caused by the autotoxic ginsenoside Rg1 Is due to over-accumulation of ROS, as revealed by transcriptomic and cellular approaches. Front Plant Sci. 9. https://doi.org/10.3389/fpls.2018.00264.

[47] YuanY, ZuoJ, ZhangH, ZuM, LiuS. The Chinese medicinal plants rhizosphere: metabolites, microorganisms, and interaction. Rhizosphere, 2022.

[48] YuHW, HeYY, ZhangW, ChenL, ZhangJL, ZhangXB, DawsonW, DingJQ. Greater chemical signaling in root exudates enhances soil mutualistic associations in invasive plants compared to natives. New Phytol, 2022, 236: 1140-1153.

Funding

National Natural Science Foundation of China(31760360)

Natural Science Foundation of Yunnan Province of China(202301 AT070007)

Natural Science Agricultural Joint Foundation of Yunnan Province of China(202101BD070001-078)

RIGHTS & PERMISSIONS

The Author(s)