All Issue

2023 Vol.41, Issue 5 Preview Page

Research Article

Tug of War-Who is the Winner? Canker Disease Restructures the Endophytic Bacterial Community of Citrus
Jian-Yu Zhou12†
,
Yi Zhang2†
,
Wen-Ping Xu3
,
Misbah Naz2
,
Xiao-Meng Li3
,
Xu Li2
,
Bi-Ying Zhao4
,
Shan-Shan Qi5
,
Zhi-Cong Dai126*
,
Dao-Lin Du2
1School of Emergency Management, Jiangsu University, 301 Xuefu Road, Zhenjiang 212013, China
2Institute of Environment and Ecology, School of The Environment and Safety Engineering, Jiangsu University, Zhenjiang 212013, China
3Shanghai Key Laboratory of Chemical Biology, School of Pharmacy, East China University of Science and Technology, Shanghai 200237, China
4International Genome Center, Jiangsu University, Zhenjiang 212013, China
5Key Laboratory of Modern Agricultural Equipment and Technology, Ministry of Education, School of Agricultural Engineering Jiangsu University, Zhenjiang 212013, China
6Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment, Suzhou University of Science and Technology, Suzhou 215009, China
*Corresponding Author
†These authors contributed equally to this work.
31 October 2023. pp. 605-616
PDF XML Citation
Abstract

High-throughput sequencing and a 16S rRNA gene clone library amplicon analysis were used to study the endophytic microbial diversity in citrus leaves in response to a Xanthomonas citri pv. Citri (Xcc) infection in an effort to develop a biocontrol scheme for citrus canker disease. There are more species of moderate citrus canker disease (MCD) than severe citrus canker disease (SCD) in terms of both Shannon and Simpson index measurements. Taxonomy has shown that the MCD Firmicutes group (25.2%) outnumber the SCD group (0.55%). Some Firmicutes can suppress Xcc, but in SCD leaves, they are in a competitive position and do not have a dominating niche; therefore, their population is greatly decreased. Sphingomonas and Methylobacterium, two genera of the phylum Proteobacteria, are growth-promoting and stress-resistant in most plants and comprise approximately 60% of the SCD group, whereas the MCD group was less abundant. In conclusion, citrus canker disease restructures bacterial communities in infected leaves, causing the endophytic community to evolve toward “weakening its spear and strengthening its shield.” This research provides support for the idea that introducing helpful bacterial strains in advance may alter the relative abundance of bacteria in a given area and hence decrease the likelihood of infection by harmful bacteria. The future of sequencing technology lies in research on microbial community functions, the elucidation of plant processes and pathogen occurrence, and support for the development of plant biological control technologies.

Keywords
biocontrol potential
biodiversity
citrus canker disease
endophytic bacteria
16S metagenomics
References
1
Asaf S, Khan AL, Khan MA, Al-Harrasi A, Lee IJ (2018) Complete genome sequencing and analysis of endophytic Sphingomonas sp. LK11 and its potential in plant growth. 3 Biotech 8:389. doi:10.1007/s13205-018-1403-z 10.1007/s13205-018-1403-z30175026PMC6111035
2
Asaf S, Khan AL, Khan MA, Imran QM, Yun B-W, Lee IJ (2017) Osmoprotective functions conferred to soybean plants via inoculation with Sphingomonas sp. LK11 and exogenous trehalose. Microbiol Res 205:135-1445. doi:10.1016/j.micres.2017.08.009 10.1016/j.micres.2017.08.00928942839
3
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. doi:10.1080/07388551.2019.1709793 10.1080/07388551.2019.170979331906737
4
Azarbad H, van Straalen NM, Laskowski R, Nikiel K, Röling WFM, Niklińska M (2016) Susceptibility to additional stressors in metal-tolerant soil microbial communities from two pollution gradients. Appl Soil Ecol 98:233-242. doi:10.1016/j.apsoil.2015.10.020 10.1016/j.apsoil.2015.10.020
5
Bakker P, Pieterse CMJ, de Jonge R, Berendsen RL (2018) The Soil-Borne Legacy. Cell 172:1178-1180. doi:10.1016/j.cell.2018.02.024 10.1016/j.cell.2018.02.02429522740
6
Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R, Burgman WP, Burmolle M, Herschend J, Bakker P, et al. (2018) Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:1496-1507. doi:10.1038/s41396-018-0093-1 10.1038/s41396-018-0093-129520025PMC5956071
7
Bishop YM, Barton LL, Johnson GV (2011) Influence of Methylobacterium on iron translocation in plants. Biometals 24:575-580. doi:10.1007/s10534-011-9408-7 10.1007/s10534-011-9408-721240540
8
Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2012) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57-59. doi:10.1038/nmeth.2276 10.1038/nmeth.227623202435PMC3531572
9
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. doi:10.1093/bioinformatics/btu170 10.1093/bioinformatics/btu17024695404PMC4103590
10
Bulgari D, Casati P, Crepaldi P, Daffonchio D, Quaglino F, Brusetti L, Bianco PA (2011) Restructuring of endophytic bacterial communities in grapevine yellows-diseased and recovered Vitis vinifera L. plants. Appl Environ Microbiol 77:5018-5022. doi:10.1128/AEM.00051-11 10.1128/AEM.00051-1121622794PMC3147392
11
Carper DL, Carrell AA, Kueppers LM, Frank AC (2018) Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors. Plant and Soil 428:335-352. doi:10.1007/s11104-018-3682-x 10.1007/s11104-018-3682-x
12
Carrion VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, de Hollander M, Ruiz-Buck D, Mendes LW, van Ijcken WFJ, Gomez-Exposito R, et al. (2019) Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366:606-612. doi:10.1126/science.aaw9285 10.1126/science.aaw928531672892
13
Chen T, Nomura K, Wang X, Sohrabi R, Xu J, Yao L, Paasch BC, Ma L, Kremer J, et al. (2020) A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580:653-657. doi:10.1038/s41586-020-2185-0 10.1038/s41586-020-2185-032350464PMC7197412
14
de Souza RSC, Armanhi JSL, Arruda P (2020) From Microbiome to Traits: Designing Synthetic Microbial Communities for Improved Crop Resiliency. Front Plant Sci 11:1179. doi:10.3389/fpls.2020.01179 10.3389/fpls.2020.0117932983187PMC7484511
15
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996-998. doi:10.1038/nmeth.2604 10.1038/nmeth.260423955772
16
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194-2200. doi:10.1093/bioinformatics/btr381 10.1093/bioinformatics/btr38121700674PMC3150044
17
Fatin Nabilah I, Ainihayati Abdul R, Lee Jia M, Nur Amimi Muliana A, Nurul Najah F (2021) Preliminary analysis of Endophytic Plant Growth Promoting (PGP) Methylobacterium sp. Isolated from Palm Oil (Elaeis guineensis) Leaves. IOP Conf Ser. Earth Environ Sci 765. doi:10.1088/1755-1315/765/1/012071 10.1088/1755-1315/765/1/012071
18
Fernandez-Conradi P, Fort T, Castagneyrol B, Jactel H, Robin C (2019) Fungal endophyte communities differ between chestnut galls and surrounding foliar tissues. Fungal Ecol 42. doi:10.1016/j.funeco.2019.100876 10.1016/j.funeco.2019.100876
19
Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17:377-386. doi:10.1101/gr.5969107 10.1101/gr.596910717255551PMC1800929
20
Islam MN, Ali MS, Choi SJ, Hyun JW, Baek KH (2019) Biocontrol of citrus canker disease caused by Xanthomonas citri subsp. citriusing an endophytic Bacillus thuringiensis. Plant Pathol J 35:486-497. doi:10.5423/PPJ.OA.03.2019.0060 10.5423/PPJ.OA.03.2019.006031632223PMC6788417
21
Janowsky J, Kimbrough E, Kandalepas D, Shaffer G, Formel SK, Van Bael SA (2019) Bacterial and fungal endophyte communities differ in trees of natural versus wastewater-treatment wetlands. Wetl Ecol Manag 27:711-723. doi:10.1007/s11273-019-09688-x 10.1007/s11273-019-09688-x
22
Jelušić A, Popović T, Dimkić I, Mitrović P, Peeters K, Miklavčič Višnjevec A, Tavzes Č, Stanković S, Berić T (2021) Changes in the winter oilseed rape microbiome affected by Xanthomonas campestris pv. campestris and biocontrol potential of the indigenous Bacillus and Pseudomonas isolates. Biol Control 160. doi:10.1016/j.biocontrol.2021.104695 10.1016/j.biocontrol.2021.104695
23
Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, et al. (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689-695. doi:10.1007/s12275-014-4002-7 10.1007/s12275-014-4002-724994010
24
Köberl M, Dita M, Martinuz A, Staver C, Berg G (2017) Members of Gammaproteobacteria as indicator species of healthy banana plants on Fusarium wilt-infested fields in Central America. Sci Rep 7. doi:10.1038/srep45318 10.1038/srep4531828345666PMC5366900
25
Kreitzman M, Toensmeier E, Chan KMA, Smukler S, Ramankutty N (2020) Perennial Staple Crops: Yields, Distribution, and Nutrition in the Global Food System. Front Sustainable Food Syst 4. doi:10.3389/fsufs.2020.588988 10.3389/fsufs.2020.588988
26
Lamit LJ, Lau MK, Sthultz CM, Wooley SC, Whitham TG, Gehring CA (2014) Tree genotype and genetically based growth traits structure twig endophyte communities. Am J Bot 101:467-478. doi:10.3732/ajb.1400034 10.3732/ajb.140003424634436
27
Leach JE, Triplett LR, Argueso CT, Trivedi P (2017) Communication in the Phytobiome. Cell 169:587-596. doi:10.1016/j.cell.2017.04.025 10.1016/j.cell.2017.04.02528475891
28
Liao Y, Huang Y (2021) Eradicate history and resistance of main citrus cultivars to citrus bacterial canker disease in Guangxi. Guangxi Plant Protection 34:28-33
29
Liu H, Brettell LE (2019) Plant defense by VOC-induced microbial priming. Trends Plant Sci 24:187-189. doi:10.1016/j.tplants.2019.01.008 10.1016/j.tplants.2019.01.00830738790
30
Liu H, Brettell LE, Qiu Z, Singh BK (2020) Microbiome-mediated stress resistance in plants. Trends Plant Sci 25:733-743. doi:10.1016/j.tplants.2020.03.014 10.1016/j.tplants.2020.03.01432345569
31
Liu L, Ma L, Feng J, Lu X (2022) Dynamic fluctuation and niche differentiation of fungal pathogens infecting Bell Pepper plants. Appl Environ Microbiol 88. doi:10.1128/aem.01003-22 10.1128/aem.01003-2236036572PMC9499033
32
Luo Q, Zhu Y, Zhang Z, Cao Y, Zhang W (2020) Variations in fungal community and diversity in Doushen with different flavors. Front Microbiol 11:447. doi:10.3389/fmicb.2020.00447 10.3389/fmicb.2020.0044732265878PMC7099864
33
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957-2963. doi:10.1093/bioinformatics/btr507 10.1093/bioinformatics/btr50721903629PMC3198573
34
Manching HC, Balint-Kurti PJ, Stapleton AE (2014) Southern leaf blight disease severity is correlated with decreased maize leaf epiphytic bacterial species richness and the phyllosphere bacterial diversity decline is enhanced by nitrogen fertilization. Front Plant Sci 5:403. doi:10.3389/fpls.2014.00403 10.3389/fpls.2014.0040325177328PMC4133650
35
Michavila G, Adler C, De Gregorio PR, Lami MJ, Caram Di Santo MC, Zenoff AM, de Cristobal RE, Vincent PA (2017) Pseudomonas protegens CS1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent. Plant Biol 19:608-617. doi:10.1111/plb.12556 10.1111/plb.1255628194866
36
Murate LS, Oliveira A, Higashi AY, Barazetti AR, Andrade GJAS (2015) Activity of secondary bacterial metabolites in the control of citrus canker. Agricultural Sciences 6:295-303. doi:10.4236/as.2015.63030 10.4236/as.2015.63030
37
Qi SS, Manoharan B, Dhandapani V, Jegadeesan S, Rutherford S, Wan JSH, Huang P, Dai ZC, Du DL (2022) Pathogen resistance in Sphagneticola trilobata (Singapore daisy): molecular associations and differentially expressed genes in response to disease from a widespread fungus. Genetica 150:13-26. doi:10.1007/s10709-021-00147-1 10.1007/s10709-021-00147-135031940
38
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 28. doi:10.1093/nar/gks1219 10.1093/nar/gks121923193283PMC3531112
39
Rabbee MF, Ali MS, Baek KH (2019) Endophyte Bacillus velezensisisolated from Citrus spp. Controls Streptomycin-Resistant Xanthomonas citri subsp. citri That Causes Citrus Bacterial Canker. Agronomy 9:470. doi:10.3390/agronomy9080470 10.3390/agronomy9080470
40
Rabbee MF, Islam N, Baek KH (2022) Biocontrol of citrus bacterial canker caused by Xanthomonas citri subsp. citri by Bacillus velezensis. Saudi J Biol Sci 29:2363-2371. doi:10.1016/j.sjbs.2021.12.005 10.1016/j.sjbs.2021.12.00535531204PMC9072923
41
Rizaludin MS, Stopnisek N, Raaijmakers JM, Garbeva P (2021) The chemistry of stress: understanding the 'Cry for Help' of plant roots. Metabolites 11:357. doi:10.3390/metabo11060357 10.3390/metabo1106035734199628PMC8228326
42
Santos-Medellín C, Edwards J, Liechty Z, Nguyen B, Sundaresan V (2017) Drought stress results in a compartment-Specific restructuring of the rice root-associated microbiomes. mBio 8. doi:10.1128/mbio.00764-17 10.1128/mBio.00764-1728720730PMC5516253
43
Schulz-Bohm K, Gerards S, Hundscheid M, Melenhorst J, de Boer W, Garbeva P (2018) Calling from distance: attraction of soil bacteria by plant root volatiles. ISME J 12:1252-1262. doi:10.1038/s41396-017-0035-3 10.1038/s41396-017-0035-329358736PMC5931972
44
Sokol H, Seksik P (2010) The intestinal microbiota in inflammatory bowel diseases: time to connect with the host. Curr Opin Gastroenterol 26:327-331. doi:10.1097/MOG.0b013e328339536b 10.1097/MOG.0b013e328339536b20445446
45
Suhaimi NSM, Goh SY, Ajam N, Othman RY, Chan KG, Thong KL (2017) Diversity of microbiota associated with symptomatic and non-symptomatic bacterial wilt-diseased banana plants determined using 16S rRNA metagenome sequencing. World J Microbiol Biotechnol 33:168. doi:10.1007/s11274-017-2336-0 10.1007/s11274-017-2336-028828756
46
Trivedi P, Duan Y, Wang N (2010) Huanglongbing, a systemic disease, restructures the bacterial community associated with citrus roots. Appl Environ Microbiol 76:3427-3436. doi:10.1128/AEM.02901-09 10.1128/AEM.02901-0920382817PMC2876436
47
Turpin W, Goethel A, Bedrani L, Croitoru Mdcm K (2018) Determinants of IBD Heritability: Genes, Bugs, and More. Inflamm Bowel Dis 24:1133-1148. doi:10.1093/ibd/izy085 10.1093/ibd/izy08529701818PMC6093195
48
Voges MJEEE, Bai Y, Schulze-Lefert P, Sattely ES (2019) Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. Proc Natl Acad Sci U.S.A. 116:12558-12565. doi:10.1073/pnas.1820691116 10.1073/pnas.182069111631152139PMC6589675
49
Wang X, Liang L, Shao H, Ye X, Yang X, Chen X, Shi Y, Zhang L, Xu L, et al. (2022) Isolation of the novel strain Bacillus amyloliquefaciens F9 and identification of Lipopeptide extract components responsible for activity against Xanthomonas citri subsp. citri. Plants (Basel) 11:457. doi:10.3390/plants11030457 10.3390/plants1103045735161438PMC8840523
50
Wang Z, Song Y (2022) Toward understanding the genetic bases underlying plant-mediated "cry for help" to the microbiota. iMeta 1:e8. doi:10.1002/imt2.8 10.1002/imt2.8
51
Weber T, Charusanti P, Musiol-Kroll EM, Jiang X, Tong Y, Kim HU, Lee SY (2015) Metabolic engineering of antibiotic factories: new tools for antibiotic production in actinomycetes. Trends Biotechnol 33:15-26. doi:10.1016/j.tibtech.2014.10.009 10.1016/j.tibtech.2014.10.00925497361
52
Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309-348. doi:10.1146/annurev.phyto.40.030402.110010 10.1146/annurev.phyto.40.030402.11001012147763
53
Wemheuer B, Thomas T, Wemheuer F (2019) Fungal endophyte communities of three agricultural important grass species differ in their response towards management regimes. Microorganisms 7:37. doi:10.3390/microorganisms7020037 10.3390/microorganisms702003730691243PMC6407066
54
Xu DB, Ye WW, Han Y, Deng ZX, Hong K (2014) Natural products from mangrove actinomycetes. Mar Drugs 12:2590-2613. doi:10.3390/md12052590 10.3390/md1205259024798926PMC4052306
55
Yan H, Zhou B, Jiang B, Lv Y, Moniruzzaman MD, Zhong G, Zhong Y (2021) Comparative analysis of bacterial and fungal endophytes responses to Candidatus Liberibacter asiaticus infection in leaf midribs of Citrus reticulata cv. Shatangju. Physiol Mol Plant Pathol 113. doi:10.1016/j.pmpp.2020.101590 10.1016/j.pmpp.2020.101590
56
Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G (2020) How plant hormones mediate salt stress responses. Trends Plant Sci 25:1117-1130. doi:10.1016/j.tplants.2020.06.008 10.1016/j.tplants.2020.06.00832675014
57
Zhang C, Wang MY, Khan N, Tan LL, Yang S (2021) Potentials, utilization, and bioengineering of plant growth-promoting Methylobacterium for sustainable agriculture. Sustainability 13:3941. doi:10.3390/su13073941 10.3390/su13073941
58
Zhang W, Gong W, Zhang Z, Luo Q, Li Y (2022) Bacterial communities in home-made Doushen with and without chili pepper. Food Res Int 156:111321. doi:10.1016/j.foodres.2022.111321 10.1016/j.foodres.2022.11132135651075
59
Zhao M, Liu D, Zhou J, Wei Z, Wang Y, Zhang X (2022) Ammonium stress promotes the conversion to organic nitrogen and reduces nitrogen loss based on restructuring of bacterial communities during sludge composting. Bioresour Technol 360. doi:10.1016/j.biortech.2022.127547 10.1016/j.biortech.2022.12754735777648
60
Zin NM, Baba MS, Zainal-Abidin AH, Latip J, Mazlan NW, Edrada-Ebel R (2017) Gancidin W, a potential low-toxicity antimalarial agent isolated from an endophytic Streptomyces SUK10. Drug Des Devel Ther 11:351-363. doi:10.2147/DDDT.S121283 10.2147/DDDT.S12128328223778PMC5308589
Information
  • Publisher :KOREAN SOCIETY FOR HORTICULTURAL SCIENCE
  • Publisher(Ko) :원예과학기술지
  • Journal Title :Horticultural Science and Technology
  • Journal Title(Ko) :원예과학기술지
  • Volume : 41
  • No :5
  • Pages :605-616
  • Received Date : 2023-03-15
  • Revised Date : 2023-06-26
  • Accepted Date : 2023-07-12
  • DOI :https://doi.org/10.7235/HORT.20230052
Journal Informaiton Horticultural Science and Technology Horticultural Science and Technology
Online Submission
  • scopus
  • NRF
  • KOFST
  • crossref crossmark
  • crossref cited-by
  • crosscheck
  • orcid
  • open access
  • ccl
Journal Informaiton Journal Informaiton - close