Unveiling the hidden allies of industrial chicory-a metagenomic exploration of rhizosphere microbiota and their impact on productivity and plant health
[en] Background: As industrial chicory is significant for food, fodder, and medicinal purposes, its cultivation is increasingly crucial for producers. To enhance productivity, resistance, and the nutritional and functional values of this plant, we aimed to investigate its interactions with the microbial environment. We performed the first comprehensive taxonomic and functional characterization of the rhizosphere microbiota associated with industrial chicory, investigating how environmental factors influence its composition. Methods: Six different land plots were simultaneously cultivated with the same chicory genotype in northern France. Using soil analyses and metagenomic approaches, we characterized the diversity of bacterial and fungal communities in the soil microbiome associated with chicory plants and discussed their functional traits. Results: We observed significant taxonomic variability, influenced by soil composition and cultivation history across each plot. The presence of chicory plants distinctly shaped the microbial community. Specifically, chicory was found to recruit Streptomyces species that produce plant hormones and Penicillium species that facilitate phosphate solubilization and promote plant growth. Moreover, the plant demonstrated an ability to repel pathogens and adapt to local microbial communities by selectively favoring beneficial microorganisms according to local stresses and nutritional needs. Discussion: Our study represents a comprehensive taxonomic and functional analysis of the Cichorium intybus rhizosphere microbiome, underscoring the pivotal role of soil composition and land-use history. The specific microbial recruitment by chicory was also addressed.
Leclercq, Lalie; UMRt BioEcoAgro 1158, University of Lille, JUNIA, INRAE, Univ. Liège, UPJV, Univ. Artois, Univ. Littoral Côte d'Opale, Villeneuve d'Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond Desprez, Villeneuve d'Ascq, France
Debarre, Sony; UMRt BioEcoAgro 1158, University of Lille, JUNIA, INRAE, Univ. Liège, UPJV, Univ. Artois, Univ. Littoral Côte d'Opale, Villeneuve d'Ascq, France
Lloret, Emily; Laboratoire de Génie Civil et géo-Environnement, University of Lille, IMT Lille Douai, University Artois, Lille, France
Taminiau, Bernard ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Rambaud, Caroline; UMRt BioEcoAgro 1158, University of Lille, JUNIA, INRAE, Univ. Liège, UPJV, Univ. Artois, Univ. Littoral Côte d'Opale, Villeneuve d'Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond Desprez, Villeneuve d'Ascq, France
Drider, Djamel; UMRt BioEcoAgro 1158, University of Lille, JUNIA, INRAE, Univ. Liège, UPJV, Univ. Artois, Univ. Littoral Côte d'Opale, Villeneuve d'Ascq, France
Siah, Ali; UMRt BioEcoAgro 1158, University of Lille, JUNIA, INRAE, Univ. Liège, UPJV, Univ. Artois, Univ. Littoral Côte d'Opale, Villeneuve d'Ascq, France
Bruno Desprez; Joint Laboratory CHIC41H, University of Lille-Florimond Desprez, Villeneuve d'Ascq, France ; Florimond Desprez Veuve & Fils, Cappelle-en-Pévèle, France
Hilbert, Jean-Louis; UMRt BioEcoAgro 1158, University of Lille, JUNIA, INRAE, Univ. Liège, UPJV, Univ. Artois, Univ. Littoral Côte d'Opale, Villeneuve d'Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond Desprez, Villeneuve d'Ascq, France
Lucau-Danila, Anca; UMRt BioEcoAgro 1158, University of Lille, JUNIA, INRAE, Univ. Liège, UPJV, Univ. Artois, Univ. Littoral Côte d'Opale, Villeneuve d'Ascq, France ; Joint Laboratory CHIC41H, University of Lille-Florimond Desprez, Villeneuve d'Ascq, France ; CORRESPONDENCE Anca Lucau-Danila
Unveiling the hidden allies of industrial chicory-a metagenomic exploration of rhizosphere microbiota and their impact on productivity and plant health
Ali A. Iftikhar Y. Mubeen M. Ali H. Zeshan M. A. Asad Z. et al. (2022). Antagonistic potential of bacterial species against fungal plant pathogens (FPP) and their role in plant growth promotion (PGP): a review. Phyton Int. J. Exp. Bot. 91, 1859–1877. doi: 10.32604/phyton.2022.021734
Alori E. T. Glick B. R. Babalola O. O. (2017). Microbial phosphorus Solubilization and its potential for use in sustainable agriculture. Front. Microbiol. 8:971. doi: 10.3389/fmicb.2017.00971, PMID: 28626450
Amara U. Khalid R. Hayat R. (2015). “Soil bacteria and phytohormones for sustainable crop production” in Bacterial metabolites in sustainable agroecosystem. Sustainable development and biodiversity. ed. Maheshwari D., vol. 12 (Cham: Springer).
Badri D. V. Vivanco J. M. (2009). Regulation and function of root exudates. Plant Cell Environ. 32, 666–681. doi: 10.1111/j.1365-3040.2009.01926.x
Bargaz A. Elhaissoufi W. Khourchi S. Benmrid B. Borden K. A. Rchiad Z. (2021). Benefits of phosphate solubilizing bacteria on belowground crop performance for improved crop acquisition of phosphorus. Microbiol. Res. 252:126842. doi: 10.1016/j.micres.2021.126842, PMID: 34438221
Berendsen R. L. Pieterse C. M. J. Bakker P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486. doi: 10.1038/s41396-018-0093-1
Berendsen R. L. Vismans G. Yu K. Song Y. de Jonge R. Burgman W. P. et al. (2018). Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 12, 1496–1507. doi: 10.1016/j.tplants.2012.04.001, PMID: 29520025
Calvo P. Nelson L. Kloepper J. W. (2014). Agricultural uses of plant biostimulants. Plant Soil 383, 3–41. doi: 10.1007/s11104-014-2131-8
Castillo C. Morales A. Rubio R. Barea J. M. Borie F. (2013). Interactions between native arbuscular mycorrhizal fungi and phosphate solubilizing fungi and their effect to improve plant development and fruit production by Capsicum annuum L. AJMR 7, 3331–3340. doi: 10.5897/AJMR2012.2363, PMID: 38147025
Chamkhi I. El Omari N. Balahbib A. El Menyiy N. Benali T. Ghoulam C. (2022). Is the rhizosphere a source of applicable multi-beneficial microorganisms for plant enhancement? Saudi J. Biol. Sci. 29, 1246–1259. doi: 10.1016/j.sjbs.2021.09.032, PMID: 35241967
Chang P.-C. Liu S.-C. Ho M.-C. Huang T.-W. Huang C.-H. (2022). A soil-isolated Streptomyces spororaveus species produces a high-molecular-weight antibiotic AF1 against Fungi and gram-positive bacteria. Antibiotics 11:679. doi: 10.3390/antibiotics11050679, PMID: 35625324
Cho S.-E. Oh J. Y. Lee D.-H. (2023). The complete mitochondrial genome of Cladosporium anthropophilum (cladosporiaceae, dothideomycetes). Mitochondrial DNA Part B 8, 164–166. doi: 10.1080/23802359.2023.2167474, PMID: 36713294
Cotrufo M. F. Lavallee J. M. Zhang Y. Hansen P. M. Paustian K. H. Schipanski M. et al. (2021). In-N-out: a hierarchical framework to understand and predict soil carbon storage and nitrogen recycling. Glob. Chang. Biol. 27, 4465–4468. doi: 10.1111/gcb.15782, PMID: 34480393
Delisle-Houde M. Dionne A. Demers F. Tweddell R. J. (2024). Cladosporium fruit rot of raspberry caused by Cladosporium pseudocladosporioides in the Québec Province. Plant Dis. 108:526. doi: 10.1094/PDIS-08-23-1657-PDN
Edwards J. Santos-Medellín C. Nguyen B. Kilmer J. Liechty Z. Veliz E. et al. (2019). Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota. Genome Biol. 20:221. doi: 10.1186/s13059-019-1825-x
Estendorfer J. Stempfhuber B. Haury P. Vestergaard G. Rillig M. C. Joshi J. et al. (2017). The influence of land use intensity on the plant-associated microbiome of Dactylis glomerata L. Front. Plant Sci. 8:930. doi: 10.3389/fpls.2017.00930, PMID: 28680426
FAO (2021). Standard operating procedure for soil pH determination. Rome: Food and Agriculture Organisation of the United Nations, 23.
Fouré M. Dugardin C. Foligné B. Hance P. Cadalen T. Delcourt A. et al. (2018). Chicory roots for prebiotics and appetite regulation: a pilot study in mice. J. Agric. Food Chem. 66, 6439–6449. doi: 10.1021/acs.jafc.8b01055, PMID: 29873488
Galloway J. N. Townsend A. R. Erisman J. W. Bekunda M. Cai Z. Freney J. R. et al. (2008). Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892. doi: 10.1126/science.1136674, PMID: 18487183
Gérard A. El-Hajjaji S. Burteau S. Fall P. A. Pirard B. Taminiau B. et al. (2021). Study of the microbial diversity of a panel of Belgian artisanal cheeses associated with challenge studies for Listeria monocytogenes. Food Microbiol. 100:103861. doi: 10.1016/j.fm.2021.103861, PMID: 34416961
Gower J. R. (1966). Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53, 325–338. doi: 10.1093/biomet/53.3-4.325, PMID: 36970824
Guertal E. A. Green B. D. (2012). Evaluation of organic fertilizer sources for south-eastern (USA) turfgrass maintenance. Acta Agric. Scand. Sect. B Soil Plant Sci. 62, 130–138. doi: 10.1080/09064710.2012.683201, PMID: 40101104
Hartman K. van der Heijden M. G. A. Wittwer R. A. Banerjee S. Walser J.-C. Schlaeppi K. (2018). Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming. Microbiome 6:14. doi: 10.1186/s40168-017-0389-9, PMID: 29338764
Havlin J. L. Tisdale S. L. Nelson W. L. Beaton J. D. (2014). Soil fertility and fertilizers: an introduction to nutrient management. 8th Edn. Pearson, London, UK:Pearson, 499.
Heiri O. Lotter A. F. Lemcke G. (2001). Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J. Paleolimnol. 25, 101–110. doi: 10.1023/A:1008119611481
Henao L. Zade R. S. H. Restrepo S. Husserl J. Abeel T. (2023). Genomes of four Streptomyces strains reveal insights into putative new species and pathogenicity of scab-causing organisms. BMC Genomics 24:143. doi: 10.1186/s12864-023-09190-y, PMID: 36959546
Hinsinger P. Plassard C. Tang C. Jaillard B. (2003). Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248, 43–59. doi: 10.1023/A:1022371130939
Hu L. Jia R. Sun Y. Chen J. Chen N. Zhang J. et al. (2023). Streptomyces pratensis S10 controls fusarium head blight by suppressing different stages of the life cycle and ATP production. Plant Dis. 107, 1442–1451. doi: 10.1094/PDIS-09-22-2063-RE, PMID: 36269586
Islam W. Noman A. Naveed H. Huang Z. Chen H. Y. H. (2020). Role of environmental factors in shaping the soil microbiome. Environ. Sci. Pollut. Res. 27, 41225–41247. doi: 10.1007/s11356-020-10471-2
Jeon B. J. Yoo N. Kim J. D. Choi J. (2023). A peptide encoded by a highly conserved gene belonging to the genus Streptomyces shows antimicrobial activity against plant pathogens. Front. Plant Sci. 14:1250906. doi: 10.3389/fpls.2023.1250906, PMID: 37868322
Jha V. Jain T. Nikumb D. Gharat Y. Koli J. Jadhav N. et al. (2022). Streptomyces peucetius M1 and Streptomyces lavendulae M3 soil isolates as a promising source for antimicrobials discovery. J. Pharm. Res. Int. 7–19, 7–19. doi: 10.9734/jpri/2022/v34i50B36438
Joshi M. V. Loria R. (2007). Streptomyces turgidiscabies possesses a functional Cytokinin biosynthetic pathway and produces leafy galls. MPMI 20, 751–758. doi: 10.1094/MPMI-20-7-0751, PMID: 17601163
Kumar M. Tiwari P. Zeyad M. T. Ansari W. A. Kumar S. C. Chakdar H. et al. (2023). Genetic diversity and antifungal activities of the genera streptomyces and nocardiopsis inhabiting agricultural fields of Tamil Nadu, India. J. King Saud Univ. Sci. 35:102619. doi: 10.1016/j.jksus.2023.102619
Lang M. E. Sibanda T. Louw S. Uzabakiriho J. D. (2023). Antimicrobial potential of the endophytic actinobacteria isolated from Harpagophytum procumbens: a southern African medicinal plant. S. Afr. J. Bot. 156, 268–277. doi: 10.1016/j.sajb.2023.03.030
Li H. Penttinen P. Mikkonen A. Stoddard F. L. Lindström K. (2020). Response of soil bacterial community diversity and composition to time, fertilization, and plant species in a sub-boreal climate. Front. Microbiol. 11:1780. doi: 10.3389/fmicb.2020.01780, PMID: 32849399
Li P. Zhang Z. J. Guo Y. T. Guan J. Wen Xi L. B. Lin L.-P. (2024). Isolation of undescribed cladosporols and spirobisnaphthalenes from a plant pathogen Cladosporium cladosporioides F-10-2-A. Phytochemistry 222:114073. doi: 10.1016/j.phytochem.2024.114073, PMID: 38565420
Liang B. Lehmann J. Solomon D. Kinyangi J. Grossman J. O'Neill B. et al. (2006). Black carbon increases cation exchange capacity in soils. Soil Sci. Soc. Am. J. 70, 1719–1730. doi: 10.2136/sssaj2005.0383
Liu M. Ussiri D. A. N. Lal R. (2016). Soil organic carbon and nitrogen fractions under different land uses and tillage practices. Commun. Soil Sci. Plant Anal. 47, 1528–1541. doi: 10.1080/00103624.2016.1194993
Lugtenberg B. Kamilova F. (2009). Plant-growth-promoting Rhizobacteria. Ann. Rev. Microbiol. 63, 541–556. doi: 10.1146/annurev.micro.62.081307.162918, PMID: 19575558
Mäder P. Fließbach A. Dubois D. Gunst L. Fried P. Niggli U. (2002). Soil fertility and biodiversity in organic farming. Science 296, 1694–1697. doi: 10.1126/science.1071148, PMID: 12040197
Marchesi J. R. Ravel J. (2015). The vocabulary of microbiome research: a proposal. Microbiome 3:31. doi: 10.1186/s40168-015-0094-5, PMID: 26229597
Martins L. F. Kolling D. Camassola M. Dillon A. J. P. Ramos L. P. (2008). Comparison of Penicillium echinulatum and Trichoderma reesei cellulases in relation to their activity against various cellulosic substrates. Bioresour. Technol. 99, 1417–1424. doi: 10.1016/j.biortech.2007.01.060, PMID: 17408952
Mayer Z. Sasvári Z. Szentpéteri V. Pethőné Rétháti B. Vajna B. Posta K. (2019). Effect of long-term cropping systems on the diversity of the soil bacterial communities. Agronomy 9:878. doi: 10.3390/agronomy9120878
Mehta P. Sharma R. Putatunda C. Walia A. (2019). “Endophytic fungi: role in phosphate solubilization” in Advances in endophytic fungal research: present status and future challenges. ed. Singh B. P. (Cham: Springer International Publishing), 183–209.
Mendes R. Garbeva P. Raaijmakers J. M. (2013). The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37, 634–663. doi: 10.1111/1574-6976.12028, PMID: 23790204
Molefe R. R. Amoo A. E. Babalola O. O. (2023). Communication between plant roots and the soil microbiome; involvement in plant growth and development. Symbiosis 90, 231–239. doi: 10.1007/s13199-023-00941-9
Murali M. Naziya B. Ansari M. A. Alomary M. N. AlYahya S. Almatroudi A. et al. (2021). Bioprospecting of rhizosphere-resident fungi: their role and importance in sustainable agriculture. J. Fungi 7:314. doi: 10.3390/jof7040314, PMID: 33919629
Murphy B. W. (2015). Impact of soil organic matter on soil properties—a review with emphasis on Australian soils. Soil Res. 53, 605–635. doi: 10.1071/SR14246
Negi R. Sharma B. Kaur S. (2023). Microbial antagonists: diversity, formulation, and applications for management of pest–pathogens. Egypt. J. Biol. Pest Control 33:105. doi: 10.1186/s41938-023-00748-2
Nye P. H. (1981). Changes of pH across the rhizosphere induced by roots. Plant Soil 61, 7–26. doi: 10.1007/BF02277359
Odo K. E. Agbo M. O. Osadebe P. O. (2022). Extract and fractions from soil Bacteria (Streptomyces canus ATCC 12647) possess antimicrobial and anti-oxidative potential in vitro. Jordan J. Pharm. Sci. 15, 405–412. doi: 10.35516/jjps.v15i3.416
Outryve M. F. V. Gosselé F. Kersters K. Swings J. (1988). The composition of the rhizosphere of chicory (Cichorium intybus L. var. foliosum Hegi). Can. J. Microbiol. 34, 1203–1208. doi: 10.1139/m88-211
Pepe A. Di Baccio D. Magnani E. Giovannetti M. Sbrana C. (2022). Zinc and Iron biofortification and accumulation of health-promoting compounds in mycorrhizal Cichorium intybus L. J. Soil Sci. Plant Nutr. 22, 4703–4716. doi: 10.1007/s42729-022-00953-2
Philippot L. Raaijmakers J. M. Lemanceau P. van der Putten W. H. (2013). Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799. doi: 10.1038/nrmicro3109, PMID: 24056930
Pouille C. L. Jegou D. Dugardin C. Cudennec B. Ravallec R. Hance P. et al. (2020). Chicory root flour – a functional food with potential multiple health benefits evaluated in a mice model. J. Funct. Foods 74:104174. doi: 10.1016/j.jff.2020.104174
Pouille C. L. Ouaza S. Roels E. Behra J. Tourret M. Molinié R. et al. (2022). Chicory: understanding the effects and effectors of this functional food. Nutrients 14:957. doi: 10.3390/nu14050957, PMID: 35267932
Pouralibaba H. R. Amirmijani A. R. (2021). Pathogenicity of Cladosporium halotolerans on some legumes. Iranian J Plant Pathol 57:153. doi: 10.22034/ijpp.2021.541950.370
Prasannath K. Galea V. J. Akinsanmi O. A. (2023). Diversity and pathogenicity of species of Botrytis, Cladosporium, Neopestalotiopsis and Pestalotiopsis causing flower diseases of macadamia in Australia. Plant Pathol. 72, 881–899. doi: 10.1111/ppa.13707
Ramos-García B. Shagarodsky T. Sandoval-Denis M. Ortiz Y. Malosso E. Costa P. M. O. et al. (2016). Morphology and phylogeny of Cladosporium subuliforme, causing yellow leaf spot of pepper in Cuba. Mycotaxon 131, 693–702. doi: 10.5248/131.693
Référentiel pédologique (2008). Association française pour l’étude du sol. Quae, Versailles, France: Edt, 435.
Riascos D. Quiroga I. Gómez R. Hoyos-Carvajal L. (2012). Cladosporium: causal agent of scab in purple passion fruit or gulupa (Passiflora edulis Sims.). Agric. Sci. 3, 299–305. doi: 10.4236/as.2012.32034
Rognes T. Flouri T. Nichols B. Quince C. Mahé F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. doi: 10.7717/peerj.2584, PMID: 27781170
Sandoval-Denis M. Sutton D. A. Martin-Vicente A. Cano-Lira J. F. Wiederhold N. Guarro J. et al. (2015). Cladosporium species recovered from clinical samples in the United States. J. Clin. Microbiol. 53, 2990–3000. doi: 10.1128/JCM.01482-15, PMID: 26179305
Schlatter D. C. Yin C. Hulbert S. Paulitz T. C. (2020). Core rhizosphere microbiomes of dryland wheat are influenced by location and land use history. Appl. Environ. Microbiol. 86, e02135–e02119. doi: 10.1128/AEM.02135-19, PMID: 31862727
Schmidt H. Eickhorst T. Tippkötter R. (2011). Monitoring of root growth and redox conditions in paddy soil rhizotrons by redox electrodes and image analysis. Plant Soil 341, 221–232. doi: 10.1007/s11104-010-0637-2
Schreiter S. Ding G.-C. Heuer H. Neumann G. Sandmann M. Grosch R. et al. (2014). Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front. Microbiol. 5:144. doi: 10.3389/fmicb.2014.00144, PMID: 24782839
Shannon C. E. (1948). A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423. doi: 10.1002/j.1538-7305.1948.tb01338.x
Shannon C. E. Weaver W. (1949). The mathematical theory of communication. Urbana, IL: The University of Illinois Press, 1–117.
Smith S. E. Read D. (2008). Mycorrhizal symbiosis. 3rd Edn. Cambridge, MA:Academic Press.
Spinelli V. Brasili E. Sciubba F. Ceci A. Giampaoli O. Miccheli A. et al. (2022). Biostimulant effects of Chaetomium globosum and Minimedusa polyspora culture filtrates on Cichorium intybus plant: growth performance and metabolomic traits. Front. Plant Sci. 13:879076. doi: 10.3389/fpls.2022.879076, PMID: 35646045
Teregulova G. A. Sineva O. N. Markelova N. N. Sadikova V. S. Uvarov G. V. Kovalenko M. A. et al. (2023). Evaluation of Chitinolytic and antibiotic activity of Streptomyces avidinii Ina 01467 and Micromonospora aurantiaca INA 01468. Eurasian Soil Sci. 56, 611–618. doi: 10.1134/S1064229323600094
Usman M. Shah I. H. Sabir I. A. Malik M. S. Rehman A. Murtaza G. et al. (2024). Synergistic partnerships of endophytic fungi for bioactive compound production and biotic stress management in medicinal plants. Plant Stress 11:100425. doi: 10.1016/j.stress.2024.100425
Venturi V. Keel C. (2016). Signaling in the rhizosphere. Trends Plant Sci. 21, 187–198. doi: 10.1016/j.tplants.2016.01.005, PMID: 26832945
Wei X. Xie B. Wan C. Song R. Zhong W. Xin S. et al. (2024). Enhancing soil health and plant growth through microbial fertilizers: mechanisms, benefits, and sustainable agricultural practices. Agronomy 14:609. doi: 10.3390/agronomy14030609
White J. F. Kingsley K. L. Zhang Q. Verma R. Obi N. Dvinskikh S. et al. (2019). Review: endophytic microbes and their potential applications in crop management. Pest Manag. Sci. 75, 2558–2565. doi: 10.1002/ps.5527, PMID: 31228333
Yang C. Xu X. Zeng Q. Lv Y. Deng Y. Liu Y. (2021). First report of leaf blight caused by Cladosporium perangustum on Livistona chinensis in China. Plant Dis. 105:223. doi: 10.1094/PDIS-05-20-1118-PDN, PMID: 32729801
Yum S.-J. Lee H.-R. Yu S. Y. Seo D. W. Kwon J. H. Kim S. M. et al. (2023). Characterization of the bacterial communities in Cichorium intybus according to cultivation and storage conditions. Microorganisms 11:1560. doi: 10.3390/microorganisms11061560, PMID: 37375061
Żarczyński P. J. Krzebietke S. J. Sienkiewicz S. Wierzbowska J. (2023). The role of fallows in sustainable development. Agriculture 13:2174. doi: 10.3390/agriculture13122174
Zeng X. Yang Y. Zhang Q. Zeng C. Deng X. Yuan H. et al. (2023). Field-scale differences in rhizosphere micro-characteristics of Cichorium intybus, Ixeris polycephala, sunflower, and Sedum alfredii in the phytoremediation of cd-contaminated soil. Ecotoxicol. Environ. Saf. 262:115137. doi: 10.1016/j.ecoenv.2023.115137, PMID: 37320919
Zhong R. Zi Z. Wang P. Noor H. Ren A. Ren Y. et al. (2023). Effects of five consecutive years of fallow tillage on soil microbial community structure and winter wheat yield. Agronomy 13:224. doi: 10.3390/agronomy13010224