[go: up one dir, main page]
Skip to main content

Advertisement

SpringerLink
Log in

Prediction of Effector Proteins from Trichoderma longibrachiatum Through Transcriptome Sequencing

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Trichoderma longibrachiatum SMF2 is an important biocontrol strain isolated by our group that can promote plant growth and induce plant disease resistance. To further study its biocontrol mechanism, the effector proteins secreted by T. longibrachiatum SMF2 were analyzed through bioinformatics and transcriptome sequencing. Overall, 478 secretory proteins produced by T. longibrachiatum were identified, of which 272 were upregulated after treatment with plants. Functional annotation showed that 36 secretory proteins were homologous with different groups of effectors from pathogenic microorganisms. Moreover, the quantitative PCR results of six putative effector proteins were consistent with those of transcriptome sequencing. Taken together, these findings indicate that the secretory proteins secreted by T. longibrachiatum SMF2 may act as effectors to facilitate its own growth and colonization or to induce plant immunity response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The geneom of T. longibrachiatum SMF2 were stored in NCBI (KB290581.1); The predicted secreted proteins are stored in the attachment table S1; The transcriptome datasets generated by Shanhai Origingene Bio-phaem Technology Co.Ltd. during the current study were stored in NCBI(https://www.ncbi.nlm.nih.gov/sra/PRJNA883996).

References

  1. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84(1):11–18. https://doi.org/10.1007/s00253-009-2092-7

    Article  CAS  PubMed  Google Scholar 

  2. Benitez T, Rincón AM, Limón MC, Codón AC (2004) Biocontrol Mechanisms of Trichoderma Strains. Int Microbiol 7(4):249–260

    CAS  PubMed  Google Scholar 

  3. Li HY, Luo Y, Zhang XS, Shi WL, Gong ZT, Shi M, Chen LL, Chen XL, Zhang YZ, Song XY (2014) Trichokonins from Trichoderma pseudokoningii SMF2 induce resistance against Gram-negative Pectobacterium carotovorum subsp. carotovorum in Chinese cabbage. FEMS Microbiol Lett 354(5):75–82. https://doi.org/10.1111/1574-6968.12427

    Article  CAS  PubMed  Google Scholar 

  4. Zhao PB, Ren AZ, Dong P, Sheng YS, Chang X, Zhang XS (2018) The antimicrobial peptaibol trichokonin IV promotes plant growth and induces systemic resistance against Botrytis cinerea infection in moth orchid. J Phytopathol 166(5):346–354. https://doi.org/10.1111/jph.12692

    Article  CAS  Google Scholar 

  5. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56. https://doi.org/10.1038/nrmicro797

    Article  CAS  PubMed  Google Scholar 

  6. Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8(6):737–746. https://doi.org/10.1111/j.1364-3703.2007.00430.x

    Article  CAS  PubMed  Google Scholar 

  7. Paulina GG, Mario IAD, Luis D, Alfredo HE, Vianey OM (2017) Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism. BMC Genet 18(1):16–36. https://doi.org/10.1186/s12863-017-0481-y

    Article  CAS  Google Scholar 

  8. Strakowska J, Błaszczyk L, Chełkowski J (2014) The significance of cellulolytic enzymes produced by Trichoderma in opportunistic lifestyle of this fungus. J Basic Microbiol 54(S1):2–13. https://doi.org/10.1002/jobm.201300821

    Article  CAS  Google Scholar 

  9. Claudia ARV, Sergio CF, Vianey OM (2019) Trichoderma as a model to study effector-like molecules. Front Microbiol 10(1030):1–14. https://doi.org/10.3389/fmicb.2019.01030

    Article  Google Scholar 

  10. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158(1):17–25. https://doi.org/10.1099/mic.0.052274-0

    Article  CAS  PubMed  Google Scholar 

  11. Slavica DJ, Walter AV, Michael VK, Michelle H, Aric W, Charles MK (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145(11):875–889. https://doi.org/10.1104/pp.107.103689

    Article  CAS  Google Scholar 

  12. Koanna G, Claudine B, Dominique R, Sylvain R (2014) Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics 15(1):336. https://doi.org/10.1186/1471-2164-15-336

    Article  CAS  Google Scholar 

  13. Cock PJ, Fields CJ, Goto N, Heuer ML, Rice PM (2010) The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. Nucleic Acids Res 38(6):1767–1771. https://doi.org/10.1093/nar/gkp1137

    Article  CAS  PubMed  Google Scholar 

  14. Erlich Y, Mitra PP, dela Bastide M, McCombie WR, Hannon GJ (2008) Alta-Cyclic: a self-optimizing base caller for next-generation sequencing. Nat Methods 5(8):679–682. https://doi.org/10.1038/nmeth.1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Thomas LM (2009) BLAST+: architecture and applications. BMC Bioinform 10:421. https://doi.org/10.1186/1471-2105-10-421

    Article  CAS  Google Scholar 

  17. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. https://doi.org/10.1093/bioinformatics/bti610

    Article  CAS  PubMed  Google Scholar 

  18. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren YX, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515. https://doi.org/10.1038/nbt.1621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31(1):46–53. https://doi.org/10.1038/nbt.2450

    Article  CAS  PubMed  Google Scholar 

  20. Reiner A, Yekutieli D, Benjamini Y (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19(3):368–375. https://doi.org/10.1093/bioinformatics/btf877

    Article  CAS  PubMed  Google Scholar 

  21. Barbara R, Robert LM (2014) Genes from Trichoderma as a source for improving plant resistance to fungal pathogen. Biotechnol Biol Trichoderma 37:505–513. https://doi.org/10.1016/B978-0-444-59576-8.00037-0

    Article  Google Scholar 

  22. Hogenhout SA, Hoorn RALV, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22(2):115–122. https://doi.org/10.1094/MPMI-22-2-0115

    Article  CAS  PubMed  Google Scholar 

  23. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124(4):803–814. https://doi.org/10.1016/j.cell.2006.02.008

    Article  CAS  PubMed  Google Scholar 

  24. Kamoun S (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10(4):358–365. https://doi.org/10.1016/j.pbi.2007.04.017

    Article  CAS  PubMed  Google Scholar 

  25. Jones JD, Dang JL (2006) The plant immune system. Nature 444(7117):323–329. https://doi.org/10.1038/nature05286

    Article  CAS  PubMed  Google Scholar 

  26. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87(1):4–10. https://doi.org/10.1094/PDIS.2003.87.1.4

    Article  CAS  PubMed  Google Scholar 

  27. Martinez C, Blanc F, Le Claire E, Besnard O, Nicole M, Baccou JC (2001) Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat denatured cellulase from Trichoderma longibrachiatum. Plant Physiol 127(1):334–344. https://doi.org/10.1104/pp.127.1.334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yordan JRC, Claudia ARV, Paulina GG, Juan IMS, Julio CVC, Vianey OM (2019) Tal6 from Trichoderma atroviride is a LysM effector involved in mycoparasitism and plant association. Front Microbiol 10(9):1–15. https://doi.org/10.3389/fmicb.2019.02231

    Article  Google Scholar 

  29. Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263. https://doi.org/10.1146/annurev.phyto.112408.132637

    Article  CAS  PubMed  Google Scholar 

  30. Qi MS, Link TI, Müller M, Hirschburger D, Pudake RN, Pedley KF, Braun E, Voegele RT, Baum TJ, Whitham SA (2016) A small cysteine-rich protein from the Asian soybean rust fungus, Phakopsora pachyrhizi, suppresses plant immunity. PLoS Pathog 12(9):27–36. https://doi.org/10.1371/journal.ppat.1005827

    Article  CAS  Google Scholar 

  31. Quarantin A, Glasenapp A, Schäfer W, Favaron F, Sella L (2016) Involvement of the Fusarium graminearum cerato-platanin proteins in fungal growth and plant infection. Plant Physiol Biochem 109:220–229. https://doi.org/10.1016/j.plaphy.2016.10.001

    Article  CAS  PubMed  Google Scholar 

  32. Miguel ASM, María IIJ, María AIO, Pablo DS, Juan FJB, Margarita RK, María TRS, Alfredo HE, Sergio CF (2015) The Epl1 and Sm1 proteins from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum. Front Plant Sci 6:77–85. https://doi.org/10.3389/fpls.2015.00077

    Article  Google Scholar 

  33. De Jonge R, Thomma BPHJ (2009) Fungal LysM effectors-extinguishers of host immunity? Trends Microbiol 17(4):151–157. https://doi.org/10.1016/j.tim.2009.01.002

    Article  CAS  PubMed  Google Scholar 

  34. Bolton MD, van Esse HP, Vossen JH, Jonge R et al (2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 69(1):119–136. https://doi.org/10.1111/j.1365-2958.2008.06270.x

    Article  CAS  PubMed  Google Scholar 

  35. van Esse HP, Bolton MD, Stergiopoulos I, de Wit PJGM, Thomma BPHJ (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20(9):1092–1101. https://doi.org/10.1094/MPMI-20-9-1092

    Article  CAS  PubMed  Google Scholar 

  36. Irieda H, Inoue Y, Mori M, Yamada K, Oshikawa Y et al (2019) Conserved fungal effector suppresses PAMP-triggered immunity by targeting plant immune kinases. Proc Natl Acad Sci 116(2):496–505. https://doi.org/10.1073/pnas.1807297116

    Article  CAS  PubMed  Google Scholar 

  37. Yoshino K, Irieda H, Sugimoto F, Yoshioka H, Okuno T, Takano Y (2012) Cell death of Nicotiana benthamiana is induced by secreted protein NIS1 of Colletotrichum orbiculare and is suppressed by a homologue of CgDN3. Mol Plant-Microbe Interact 25(5):625–636. https://doi.org/10.1094/MPMI-12-11-0316

    Article  CAS  PubMed  Google Scholar 

  38. Nie JJ, Zhou WJ, Lin YH, Liu ZY, Yin ZY, Huang LL (2022) Two NIS1-like proteins from apple canker pathogen (Valsa mali) play distinct roles in plant recognition and pathogen virulence. Stress Biology 2(7):23–32. https://doi.org/10.1007/s44154-021-00031-0

    Article  CAS  Google Scholar 

  39. Kulkarni R, Kelkar H, Dean R (2003) An eight- cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem Sci 28(3):118–121. https://doi.org/10.1016/S0968-0004(03)00025-2

    Article  CAS  PubMed  Google Scholar 

  40. Kou Y, Tan YH, Ramanujam R, Naqvi NI (2017) Structure–function analyses of the Pth11 receptor reveal an important role for CFEM motif and redox regulation in rice blast. New Phytol 214(1):330–342. https://doi.org/10.1111/nph.14347

    Article  CAS  PubMed  Google Scholar 

  41. Seifbarghi S, Borhan MH, Wei YD, Coutu C, Robinson SJ, Hegedus DD (2017) Changes in the Sclerotinia sclerotiorum transcriptome during infection of Brassica napus. BMC Genomics 18(1):266–275. https://doi.org/10.1186/s12864-017-3642-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Aboubakr M, Mohamed ES, Jordi G, Tina A, Paul D, Krzysztof W, Markus K, Felix M (2021) Expression of a fungal lectin in arabidopsis enhances plant growth and resistance toward microbial pathogens and a plant-parasitic nematode. Front Plant Sci 12(4):1–13. https://doi.org/10.3389/fpls.2021.657451

    Article  Google Scholar 

  43. Liu JJ, Rona S, Abul KME (2010) The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Rep 29(5):419–436. https://doi.org/10.1007/s00299-010-0826-8

    Article  CAS  PubMed  Google Scholar 

  44. Jean G, Claude P, Alain A (2000) Some fungi express β-1,3-glucanases similar to thaumatin-like proteins. Mycologia 92(5):841–848. https://doi.org/10.2307/3761579

    Article  Google Scholar 

  45. Adams J, Kelso R, Cooley L (2010) The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol 10(1):17–24. https://doi.org/10.1016/s0962-8924(99)01673-6

    Article  Google Scholar 

  46. Natalie Z, Raz Z (2012) Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Structure 20(3):397–405. https://doi.org/10.1016/j.str.2012.01.006

    Article  CAS  Google Scholar 

  47. Bröms JE, Edqvist PJ, Forsberg A, Francis MS (2006) Tetratricopeptide repeats are essential for PcrH chaperone function in Pseudomonas aeruginosa type III secretion. FEMS Microbiol Lett 256(1):57–66. https://doi.org/10.1111/j.1574-6968.2005.00099.x

    Article  CAS  PubMed  Google Scholar 

  48. Harvey S, Kumari P, Lapin D, Griebel T, Hickman R, Guo WB, Zhang RX, Parker JE, Beynon J, Denby K, Steinbrenner J (2020) Downy Mildew effector HaRxL21 interacts with the transcriptional repressor TOPLESS to promote pathogen susceptibility. PLoS Pathog 16(8):1–26. https://doi.org/10.1371/journal.ppat.1008835

    Article  CAS  Google Scholar 

  49. Karimi JM, Mehrabi R, Collemare J, Mesarich CH, de Wit PJGM (2015) The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant–pathogen interactions. Front Plant Sci 6:584. https://doi.org/10.3389/fpls.2015.00584

    Article  Google Scholar 

  50. Tian M, Chaudhry F, Ruzicka DR, Meagher RB, Staiger CJ, Day B (2009) Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol 150:815–824. https://doi.org/10.1104/pp.109.137604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Tian M, Benedetti B, Kamoun S (2005) A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69b of tomato. Plant Physiol 138:1785–1793. https://doi.org/10.1104/pp.105.061226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Tian M, Huitema E, da Cunha L, Torto-Alalibo T, Kamoun S (2004) A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69b. J Biol Chem 279:26370–26377. https://doi.org/10.1074/jbc.m400941200

    Article  CAS  PubMed  Google Scholar 

  53. Rivas S, Genin S (2011) A plethora of virulence strategies hidden behind nuclear targeting of microbial effectors. Front Plant Sci 2:104. https://doi.org/10.3389/fpls.2011.00104

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, Hahn M, Voegele RT (2005) Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant-Microbe Interact 18(11):1130–1139. https://doi.org/10.1094/MPMI-18-1130

    Article  CAS  PubMed  Google Scholar 

  55. Petre B, Saunders DG, Sklenar J, Lorrain C, Win J, Duplessis S, Kamoun S (2015) Candidate effector proteins of the rust pathogen Melampsora larici-populina target diverse plant cell compartments. Mol Plant-Microbe Interact 28(6):689–700. https://doi.org/10.1094/MPMI-01-15-0003-R

    Article  CAS  PubMed  Google Scholar 

  56. Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209. https://doi.org/10.1016/j.cub.2011.06.044

    Article  CAS  PubMed  Google Scholar 

  57. Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A, Tyler BM, Pardo AG, Martin F (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 21:1197–1203. https://doi.org/10.1016/j.cub.2011.05.033

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Prof. Zhang Yuzhong in Shandong University for providing the strains and the genome sequence of T. longibrachiatum SMF2.The library preparations were sequenced on an Illumina Novaseq 6000 platform and paired-end reads were generated and bioinformatics analysis (Shanhai Origingene Bio-phaem Technology Co.Ltd., China) We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Funding

This work was supported by Nature Science Fund of Shandong Province (ZR2020MC125, ZR2013CM006); Key R & D plan of Shandong Province (2019GNC106018); and Shandong Provincial Key Laboratory of Agricultural Microbiology Open Fund (SDKL2017015).

Author information

Author notes

  1. Jialin Zhang and Lijun Wang are co-first author.

Authors and Affiliations

  1. Liaocheng University, Liaocheng, 252000, China

    Jialin Zhang, Lijun Wang, Aizhi Ren, Yinsheng Sheng, Xue Chang, Xiaolong Li, Mengjiao Guan, Na Shang, Peibao Zhao & Shulei Sun

  2. Liaocheng Land and Resources Bureau, Liaocheng, 252000, China

    Xue Chang

  3. Liaocheng Academy of Agricultural Sciences, Liaocheng, 252000, China

    Na Shang

  4. University of California San Diego, San Diego, CA, 92121, USA

    Shulei Sun

Authors
  1. Jialin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lijun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aizhi Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yinsheng Sheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xue Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaolong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mengjiao Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Na Shang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Peibao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shulei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived of or designed study: PBZ, AZR; Performed research: LJW, YSS, XC, NS; Analyzed data: JLZ, XLL, MJG; Contributed new methods or models: SLS; Writing: PBZ, AZR; Review and editing: PBZ, SLS; Funding acquisition: PBZ, AZR. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Peibao Zhao or Shulei Sun.

Ethics declarations

Conflict of interest

This experiment was independently completed by our team in Liaocheng University with the support of local government funding (ZR2020MC125, ZR2013CM006, 2019GNC106018 and SDKL2017015), Dr. Shulei Sun from University of California San Diego participated in the work of bioinformatics analysis and paper revision. All authors have read the enclosed version of the manuscript, and all of us make sure the author group, the corresponding author and the order of authors are all correct at submission. All the authors listed have approved the manuscript and have no potential conflicts of interest, also we make sure that there is no conflict of interest with others.

Ethical Approval

We have read and have abided by the statement of ethical standards for manuscripts submitted to Current Microbiology, We ensure that the data is authentic and reliable, without fabrication, falsification or inappropriate data manipulation and, also we certify that the work described has not been submitted elsewhere for publication, in whole or in part.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Wang, L., Ren, A. et al. Prediction of Effector Proteins from Trichoderma longibrachiatum Through Transcriptome Sequencing. Curr Microbiol 80, 259 (2023). https://doi.org/10.1007/s00284-023-03296-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03296-y

Search

Navigation