Abstract
Aims
Banana Fusarium wilt (Fusarium oxysporum f. sp. cubense tropical race 4) is a typical destructive soil-borne disease, which was the main limiting factor for the sustainable development of the banana industry worldwide. In banana production, soil physiochemical properties and soil microbiome were effectively affected the occurrence and spread of Fusarium wilt. However, there is still a lack of systematic research, particularly in exploring the correlation between the occurrence of banana Fusarium wilt and soil properties across various climates and soil types.
Methods
In this study we investigated the soil physicochemical properties, bacterial and fungal community composition, and pathogenic fungal abundance in 140 banana plantations which were affected by banana Fusarium wilt in Yunnan Province, China.
Results
The results showed that the abundance of soil-borne pathogenic fungi was positively correlated with total phosphorus, total nitrogen, organic matter, urease activity, annual precipitation, and the alpha diversity of bacterial and fungal communities. In contrast, it showed a significant negative correlation with the annual mean temperature. As the abundance of pathogen increased, numerous potential disease-suppressive bacterial genera (such as Rhodanobacter, Gemmatimonas, Novosphingobium) and soil-borne pathogenic fungal genera (such as Plectosphaerella, Nigrospora, Cyphellophora) also increased, and the co-occurrence network showed a higher modularization index.
Conclusions
The results enhance the understanding of the patterns of soil-borne pathogenic fungal population dynamics in banana plantations, which would provide evidence and guidance for reducing pathogenic fungal abundance and selecting beneficial microorganisms in banana production. Furthermore, this would provide a theoretical basis for sustainable prevention and control of banana wilt disease.
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References
Asaf S, Numan M, Khan AL, Al-Harrasi A (2020) Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol 40:138–152. https://doi.org/10.1080/07388551.2019.1709793
Bakker PA, Berendsen RL, Van Pelt JA, Vismans G, Yu K, Li E, Van Bentum S, Poppeliers SW, Gil JJS, Zhang H (2020) The soil-borne identity and microbiome-assisted agriculture: looking back to the future. Mol Plant 13:1394–1401. https://doi.org/10.1016/j.molp.2020.09.017
Baron NC, de Souza Pollo A, Rigobelo EC (2020) Purpureocillium lilacinum and metarhizium marquandii as plant growth-promoting fungi. PeerJ 8:e9005. https://doi.org/10.7717/peerj.9005
Buddenhagen I (2009) Understanding strain diversity in Fusarium oxysporum f. sp cubense and history of introduction of tropical race 4 to better manage banana production. Acta Hortic 828:193–204. https://doi.org/10.17660/ActaHortic.2009.828.19
Carlucci A, Raimondo M, Santos J, Phillips A (2012) Plectosphaerella species associated with root and collar rots of horticultural crops in southern Italy. Persoonia 28:34–48. https://doi.org/10.3767/003158512X638251
Chen S, Zhou Y, Chen Y, Gu J (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890
Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350:663–666. https://doi.org/10.1093/bioinformatics/bty560
De Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:3033. https://doi.org/10.1038/s41467-018-05516-7
Delgado-Baquerizo M, Guerra CA, Cano-Díaz C, Egidi E, Wang J-T, Eisenhauer N, Singh BK, Maestre FT (2020) The proportion of soil-borne pathogens increases with warming at the global scale. Nat Clim Change 10:550–554. https://doi.org/10.1038/s41558-020-0759-3
Dharmakeerthi R, Thenabadu M (1996) Urease activity in soils: a review. Natl Sci Found 24:159–195. https://doi.org/10.4038/jnsfsr.v24i3.5548
Ding L, Xu L, Chu X, Yang L, Zhu H, Huang J (2021) Dissimilarity analysis of microbial communities in the rhizosphere and tissues of diseased and healthy cherry trees (Cerasus Pseudocerasus). Can J Plant Pathol 43:612–621. https://doi.org/10.1080/07060661.2020.1861101
Dita M, Perez-Vicente L, Guzman M, Urias C, Staver, C (2017) Fusarium tropical race 4 and it threat to food security and the banana industry in Latin America and the Caribbean. Phytopathology 107:8
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
Du S, Trivedi P, Wei Z, Feng J, Hu H, Bi L, Liu Y (2022) The proportion of soil-borne fungal pathogens increases with elevated organic carbon in agricultural soils. Msystems 7(2):e01337-21. https://doi.org/10.1128/msystems.01337-21
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Evans EA, Ballen FH, Siddiq M (2020) Banana production, global trade, consumption trends, postharvest handling, and processing. Handbook of banana production, postharvest science, processing technology, and nutrition. Wiley, New Jersey, pp 1–18
Franke-Whittle IH, Manici LM, Insam H, Stres B (2015) Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards. Plant Soil 395:317–333. https://doi.org/10.1007/s11104-015-2562-x
Fu L, Penton CR, Ruan Y, Shen Z, Xue C, Li R, Shen Q (2017) Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol Biochem 104:39–48. https://doi.org/10.1016/j.soilbio.2016.10.008
Fu L, Ou Y, Shen Z, Wang B, Li R, Shen Q (2019) Stable microbial community and specific beneficial taxa associated with natural healthy banana rhizosphere. J Microbiol Biotechnol 1624–1628. https://doi.org/10.4014/jmb.1904.04061
Gao M, Xiong C, Gao C, Tsui CK, Wang M-M, Zhou X, Zhang A-M, Cai L (2021) Disease-induced changes in plant microbiome assembly and functional adaptation. Microbiome 9:1–18. https://doi.org/10.1186/s40168-021-01138-2
Garbeva Pv, Van Veen JA, Van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270. https://doi.org/10.1146/annurev.phyto.42.012604.135455
García-Bastidas F, Ordóñez N, Konkol J, Al-Qasim M, Naser Z, Abdelwali M, Salem N, Waalwijk C, Ploetz RC, Kema GHJ (2014) First report of Fusarium oxysporum f. sp cubense tropical race 4 associated with Panama disease of banana outside Southeast Asia. Plant Dis 98(5):694. https://doi.org/10.1094/PDIS-09-13-0954-PDN
Ghorbani R, Wilcockson S, Koocheki A, Leifert C (2008) Soil management for sustainable crop disease control: a review. Environ Chem Lett 6:149–162. https://doi.org/10.1007/s10311-008-0147-0
Han W, Lee J, Pham M, Yu J (2010) iGraph: a framework for comparisons of disk-based graph indexing techniques. Proc Vldb Endow 3:449–459. https://doi.org/10.14778/1920841.1920901
Hartmann M, Six J (2023) Soil structure and microbiome functions in agroecosystems. Nat Rev Earth Env 4:4–18. https://doi.org/10.1038/s43017-022-00366-w
He P, Li S, Xu S, Fan H, Wang Y, Zhou W, Fu G, Han G, Wang Y-Y, Zheng S-J (2021) Monitoring tritrophic biocontrol interactions between Bacillus spp, Fusarium oxysporum f. sp. cubense, tropical race 4, and banana plants in vivo based on fluorescent transformation system. Front Microbiol 12:754918. https://doi.org/10.3389/fmicb.2021.754918
Hong, S, Jv, H, Lu, M, Wang, B, Zhao, Y, Ruan, Y (2020) Significant decline in banana Fusarium wilt disease is associated with soil microbiome reconstruction under chilli pepper-banana rotation. Eur J Soil Biol 97:103154. https://doi.org/10.1016/j.ejsobi.2020.103154
Innerebner G, Knief C, Vorholt JA (2011) Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl Environ Microbiol 77:3202–3210. https://doi.org/10.1128/AEM.00133-11
Islam W, Noman A, Naveed H, Huang Z, Chen HY (2020) Role of environmental factors in shaping the soil microbiome. Environ Sci Pollut Res 27:41225–41247. https://doi.org/10.1007/s11356-020-10471-2
Katan J (2017) Diseases caused by soilborne pathogens: biology, management and challenges. J Plant Pathol 305–315. https://doi.org/10.4454/jpp.v99i2.3862
Kaushal M, Mahuku G, Swennen R (2020) Metagenomic insights of the root colonizing microbiome associated with symptomatic and non-symptomatic bananas in Fusarium wilt infected fields. Plants 9(2):263. https://doi.org/10.3390/plants9020263
Ke J, Wang B, Yoshikuni Y (2021) Microbiome engineering: synthetic biology of plant-associated microbiomes in sustainable agriculture. Trends Biotechnol 39:244–261. https://doi.org/10.1016/j.tibtech.2020.07.008
Klute A, Page AL (1986) Methods of soil analysis. Part 1. Physical and mineralogical methods; part 2. Chemical and microbiological properties. American Society of Agronomy, Inc., Madison
Li F, Zhang S, Wang Y, Li Y, Li P, Chen L, Jie X, Hu D, Feng B, Yue K (2020) Rare fungus, Mortierella capitata, promotes crop growth by stimulating primary metabolisms related genes and reshaping rhizosphere bacterial community. Soil Biol Biochem 151:108017. https://doi.org/10.1016/j.soilbio.2020.108017
Li J, Wang C, Liang W, Liu S (2021a) Rhizosphere microbiome: the emerging barrier in plant-pathogen interactions. Front Microbiol 12:772420. https://doi.org/10.3389/fmicb.2021.772420
Li P, Liu M, Li G, Liu K, Liu T, Wu M, Saleem M, Li ZJ (2021b) Phosphorus availability increases pathobiome abundance and invasion of rhizosphere microbial networks by Ralstonia. Environ Microbiol 23:5992–6003. https://doi.org/10.1111/1462-2920.15696
Liu S, Plaza C, Ochoa-Hueso R, Trivedi C, Wang J, Trivedi P, Zhou G, Piñeiro J, Martins C, Singh B, Delgado-Baquerizo M (2023) Litter and soil biodiversity jointly drive ecosystem functions. Glob Change Biol 29:6276–6285. https://doi.org/10.1111/gcb.16913
Löbmann MT, Vetukuri RR, De Zinger L, Alsanius BW, Grenville-Briggs LJ, Walter AJ (2016) The occurrence of pathogen suppressive soils in Sweden in relation to soil biota, soil properties, and farming practices. Appl Soil Ecol 107:57–65. https://doi.org/10.1016/j.apsoil.2016.05.011
Lundberg D, Lebeis S, Paredes S, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio T, Edgar R, Eickhorst T, Ley R, Hugenholtz P, Tringe S, Dangl J (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Maryani N, Lombard L, Poerba YS, Subandiyah S, Crous PW, Kema GHJ (2019) Phylogeny and genetic diversity of the banana Fusarium wilt pathogen fusarium oxysporum f. sp. cubense in the Indonesian centre of origin. Stud Mycol 92:155–194. https://doi.org/10.1016/j.simyco.2018.06.003
Mesny F, Miyauchi S, Thiergart T, Pickel B, Atanasova L, Karlsson M, Hüttel B, Barry KW, Haridas S, Chen C (2021) Genetic determinants of endophytism in the Arabidopsis root mycobiome. Nat Commun 12:7227. https://doi.org/10.1038/s41467-021-27479-y
Molina AB, Fabregar E, Sinohin VG, Yi G, Viljoen A (2009) Recent occurrence of Fusarium oxysporum f. sp cubense tropical race 4 in Asia. Acta Hortic 828:109–116. https://doi.org/10.17660/ActaHortic.2009.828.10
Newbery F, Qi A, Fitt BD (2016) Modelling impacts of climate change on arable crop diseases: progress, challenges and applications. Curr Opin Plant Biol 32:101–109. https://doi.org/10.1016/j.pbi.2016.07.002
Ou Y, Penton CR, Geisen S, Shen Z, Sun Y, Lv N, Wang B, Ruan Y, Xiong W, Li R (2019) Deciphering underlying drivers of disease suppressiveness against pathogenic Fusarium oxysporum. Front Microbiol 10:2535. https://doi.org/10.3389/fmicb.2019.02535
Ozimek E, Hanaka A (2020) Mortierella species as the plant growth-promoting fungi present in the agricultural soils. Agriculture 11:7. https://doi.org/10.3390/agriculture11010007
Page, A. Miller, R. Keeney, D (1982) Methods of soil analysis, part 2: chemical and microbiological properties. American Society of Agronomy, Inc. and Soil Science Society of America. Inc., Madison, p 1159
Panth M, Hassler SC, Baysal-Gurel F (2020) Methods for management of soilborne diseases in crop production. Agriculture 10:16. https://doi.org/10.3390/agriculture10010016
Pang Z, Fallah N, Weng P, Zhou Y, Tang X, Tayyab M, Liu Y, Liu Q, Xiao Y, Hu C (2022) Sugarcane–peanut intercropping system enhances bacteria abundance, diversity, and sugarcane parameters in rhizospheric and bulk soils. Front Microbiol 12:815129. https://doi.org/10.3389/fmicb.2021.815129
Pegg KG, Coates LM, O’Neill WT, Turner DW (2019) The epidemiology of Fusarium wilt of banana. Front Plant Sci 10:1395. https://doi.org/10.3389/fpls.2019.01395
Ploetz RC (2006) Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp cubense. Phytopathology 96:653–656. https://doi.org/10.1094/PHYTO-96-06
Raimondo ML, Carlucci A (2018) Characterization and pathogenicity assessment of Plectosphaerella species associated with stunting disease on tomato and pepper crops in Italy. Plant Pathol 67:626–641. https://doi.org/10.1111/ppa.12766
Rangjaroen C, Sungthong R, Rerkasem B, Teaumroong N, Noisangiam R, Lumyong S (2017) Untapped endophytic colonization and plant growth-promoting potential of the genus Novosphingobium to optimize rice cultivation. Microbes Environ 32:84–87. https://doi.org/10.1264/jsme2.ME16112
Ray P, Lakshmanan V, Labbé JL, Craven KD (2020) Microbe to microbiome: a paradigm shift in the application of microorganisms for sustainable agriculture. Front Microbiol 11:622926. https://doi.org/10.3389/fmicb.2020.622926
Revelle, W, Revelle, M (2015) Package ‘psych’. The comprehensive R archive network 337(338). https://cran.rstudio.org/web/packages/psych/psych.pdf
Segura-Mena R, Stoorvogel J, Garcia-Bastidas F, Salacinas-Niez M, Kema GH, Sandoval JA (2021) Evaluating the potential of soil management to reduce the effect of Fusarium oxysporum f. sp. cubense in banana (Musa AAA). Eur J Plant Pathol 160:441–455. https://doi.org/10.1007/s10658-021-02255-2
Segura RA, Stoorvogel JJ, Sandoval JA (2022) The effect of soil properties on the relation between soil management and Fusarium wilt expression in Gros Michel bananas. Plant Soil 1–12. https://doi.org/10.1007/s11104-021-05192-5
Shen Z, Zhong S, Wang Y, Wang B, Mei X, Li R, Ruan Y, Shen Q (2013) Induced soil microbial suppression of banana fusarium wilt disease using compost and biofertilizers to improve yield and quality. Eur J Soil Biol 57:1–8. https://doi.org/10.1016/j.ejsobi.2013.03.006
Shen Z, Wang D, Ruan Y, Xue C, Zhang J, Li R, Shen Q (2014) Deep 16S rRNA pyrosequencing reveals a bacterial community associated with banana Fusarium wilt disease suppression induced by bio-organic fertilizer application. PLoS ONE 9:e98420. https://doi.org/10.1371/journal.pone.0098420
Siamak SB, Zheng S (2018) Banana Fusarium wilt (Fusarium oxysporum f. sp. cubense) control and resistance, in the context of developing wilt-resistant bananas within sustainable production systems. Hortic. Hortic Plant J 4:208–218. https://doi.org/10.1016/j.hpj.2018.08.001
Snelders NC, Rovenich H, Petti GC, Rocafort M, van den Berg GC, Vorholt JA, Mesters JR, Seidl MF, Nijland R, Thomma BP (2020) Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins. Nat Plants 6:1365–1374. https://doi.org/10.1038/s41477-020-00799-5
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 44:846–849. https://doi.org/10.1099/00207713-44-4-846
Tao C, Li R, Xiong W, Shen Z, Liu S, Wang B, Ruan Y, Geisen S, Shen Q, Kowalchuk GA (2020) Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 8:1–14. https://doi.org/10.1186/s40168-020-00892-z
Toju H, Peay KG, Yamamichi M, Narisawa K, Hiruma K, Naito K, Fukuda S, Ushio M, Nakaoka S, Onoda Y (2018) Core microbiomes for sustainable agroecosystems. Nat Plants 4:247–257. https://doi.org/10.1038/s41477-018-0139-4
Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18:607–621. https://doi.org/10.1038/s41579-020-0412-1
Van Agtmaal M, Straathof AL, Termorshuizen A, Lievens B, Hoffland E, de Boer W (2018) Volatile-mediated suppression of plant pathogens is related to soil properties and microbial community composition. Soil Biol Biochem 117:164–174. https://doi.org/10.1016/j.soilbio.2017.11.015
Vorholt JA, Vogel C, Carlström CI, Müller DB (2017) Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22:142–155. https://doi.org/10.1016/j.chom.2017.07.004
Walters D, Bingham I (2007) Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control. Ann Appl Biol 151:307–324. https://doi.org/10.1111/j.1744-7348.2007.00176.x
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang Y, Wang L, Suo M, Qiu Z, Wu H, Zhao M, Yang H (2022) Regulating root fungal community using Mortierella alpina for Fusarium oxysporum resistance in Panax ginseng. Front Microbiol 13:850917. https://doi.org/10.3389/fmicb.2022.850917
Wei Z, Yang T, Friman V-P, Xu Y, Shen Q, Jousset A (2015) Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun 6:8413. https://doi.org/10.1038/ncomms9413
Xiong W, Guo S, Jousset A, Zhao Q, Wu H, Li R, Kowalchuk GA, Shen Q (2017) Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biol Biochem 114:238–247. https://doi.org/10.1016/j.soilbio.2017.07.016
Xu H, Yu F, Zuo Y, Dai Y, Deng H, Xie J (2022) Selected rhizosphere bacteria are associated with endangered species-Scutellaria tsinyunensis via comparative microbiome analysis. Microbiol Res 258:126917. https://doi.org/10.1016/j.micres.2021.126917
Zantua M, Dumenil L, Bremner J (1977) Relationships between soil urease activity and other soil properties. Soil Sci Soc Am J 41:350–352. https://doi.org/10.2136/sssaj1977.03615995004100020036x
Zhang N, Xin H, Zhang J, Raza W, Xing-Ming Y, Yun-Ze R, Qi-Rong S, Huang Q (2014) Suppression of Fusarium wilt of banana with application of bio-organic fertilizers. Pedosphere 24:613–624. https://doi.org/10.1016/S1002-0160(14)60047-3
Zhang Y, Ye C, Su Y, Peng W, Lu R, Liu Y, Huang H, He X, Yang M, Zhu S (2022) Soil acidification caused by excessive application of nitrogen fertilizer aggravates soil-borne diseases: evidence from literature review and field trials. Agric Ecosyst Environ 340:108176. https://doi.org/10.1016/j.agee.2022.108176
Zhu F, Fang Y, Wang Z, Wang P, Yang K, Xiao L, Wang R (2022) Salicylic acid remodeling of the rhizosphere microbiome induces watermelon root resistance against Fusarium oxysporum f. sp. niveum infection. Front Microbiol 13:1015038. https://doi.org/10.3389/fmicb.2022.1015038
Zin NA, Badaluddin NA (2020) Biological functions of Trichoderma spp. for agriculture applications. Ann Agric Sci 65:168–178. https://doi.org/10.1016/j.aoas.2020.09.003
Zuo C, Deng G, Li B, Huo H, Li C, Hu C, Kuang R, Yang Q, Dong T, Sheng O (2018) Germplasm screening of Musa spp for resistance to Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4). Eur J Plant Pathol 151:723–734. https://doi.org/10.1007/s10658-017-1406-3
Acknowledgements
We thank all staff members in the Yunnan Key Laboratory of Green Prevention and Control of Agricultural Transboundary Pests for their considerable help with samples collection. The research leading to these results received funding from Yunnan Provincial Agricultural Joint Special Project (202101BD070001-001), Yunnan Provincial Xingdian Talent Program “Young talent” Project (YNWR-QNBJ-2019-246; YNWR-QNBJ-2020-298), Natural Science Foundation of China (31600349), Yunnan Science and Technology Mission (202204BI090019) and the earmarked fund for CARS (CARS-31-22). Special thank you is also given to the reviewers.
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Wenlong Zhang: Methodology, Software, Visualization, Writing - review & editing. Tingting Bai: Conceptualization, Supervision, Funding acquisition. Arslan Jamil: Writing - review & editing. Huacai Fan: Resources, Investigation. Xundong Li: Supervision, Funding acquisition. Si-Jun Zheng: Conceptualization, Supervision, Funding acquisition. Shengtao Xu: Conceptualization, Supervision, Funding acquisition, Writing - review & editing.
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Zhang, W., Bai, T., Jamil, A. et al. The interaction between Fusarium oxysporum f. sp. cubense tropical race 4 and soil properties in banana plantations in Southwest China. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06709-4
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DOI: https://doi.org/10.1007/s11104-024-06709-4