Skip to main content
Springer Nature Link
Log in

Transcriptional effects of carbon and nitrogen starvation on Ganoderma boninense, an oil palm phytopathogen

  • Original Article
  • Published:
Save article
View saved research
Molecular Biology Reports Aims and scope Submit manuscript

A Correspondence to this article was published on 30 July 2024

Abstract

Background

Ganoderma boninense is a phytopathogen of oil palm, causing basal and upper stem rot diseases.

Methods

The genome sequence was used as a reference to study gene expression during growth in a starved carbon (C) and nitrogen (N) environment with minimal sugar and sawdust as initial energy sources. This study was conducted to mimic possible limitations of the C–N nutrient sources during the growth of G. boninense in oil palm plantations.

Results

Genome sequencing of an isolate collected from a palm tree in West Malaysia generated an assembly of 67.12 Mb encoding 19,851 predicted genes. Transcriptomic analysis from a time course experiment during growth in this starvation media identified differentially expressed genes (DEGs) that were found to be associated with 29 metabolic pathways. During the active growth phase, 26 DEGs were related to four pathways, including secondary metabolite biosynthesis, carbohydrate metabolism, glycan metabolism and mycotoxin biosynthesis. G. boninense genes involved in the carbohydrate metabolism pathway that contribute to the degradation of plant cell walls were up-regulated. Interestingly, several genes associated with the mycotoxin biosynthesis pathway were identified as playing a possible role in pathogen-host interaction. In addition, metabolomics analysis revealed six metabolites, maltose, xylobiose, glucooligosaccharide, glycylproline, dimethylfumaric acid and arabitol that were up-regulated on Day2 of the time course experiment.

Conclusions

This study provides information on genes expressed by G. boninense in metabolic pathways that may play a role in the initial infection of the host.

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+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

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

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Data availability

Genome sequences are available in GenBank under the BioProject PRJNA912356 (Link to data: https://dataview.ncbi.nlm.nih.gov/object/PRJNA912356?reviewer=m1q88r1gkqlllct4ilhatr9fo3). PER71 RNAseq data used as evidence in the pipelines were: (i) 27 libraries from the C–N starvation study; (ii) Iso-seq 1-3 kb; (iii) PER71 grown on PDA; (iv) PER71 grown on rubber woodblock for 47 days (PER71-47).

References

  1. Parveez GKA, Tarmizi AHA, Sundram S et al (2021) Oil palm economic performance in Malaysia and R&D progress in 2020. J Oil Palm Res 33(2):181–214

    CAS  Google Scholar 

  2. Olaniyi ON, Szulczyk KR (2020) Estimating the economic damage and treatment cost of basal stem rot striking the Malaysian oil palms. For Policy Econ 116(2020):102163

    Google Scholar 

  3. Kamu A, Phin CK, Seman IA et al (2021) Estimating the yield loss of oil palm due to Ganoderma basal stem rot disease by using bayesian model averaging. J Oil Palm Res 33(1):46–55

    Google Scholar 

  4. Wahab MAA (2016) Ganoderma stem rot of oil palm: Epidemiology, diversity and pathogenicity. Dissertation, University of Bath, UK

  5. Villavicencio EV, Mali T, Mattila HK et al (2020) Enzyme activity profiles produced on wood and straw by four fungi of different decay strategies. Microorganisms 8:73–90

    CAS  Google Scholar 

  6. Corley RHV, Tinker PBH (2015) The oil palm, 5th edn. Wiley, NJ

    Google Scholar 

  7. Ramzi AB, Che Me ML, Ruslan US et al (2019) Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis. PeerJ 7:e8065

    PubMed  PubMed Central  Google Scholar 

  8. Nicolas C, Martin-Bertelsen T, Floudas D et al (2019) The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen. The ISME J 13:977–988

    CAS  PubMed  Google Scholar 

  9. Di Lonardo DP, van der Wal A, Harkes P et al (2020) Effect of nitrogen on fungal growth efficiency. Plant Biosystems–An International Journal Dealing with all Aspects of Plant Biology 154(4):433–437

    Google Scholar 

  10. Nagappan J, Chin CF, Angel LPL et al (2018) Improved nucleic acid extraction protocols for Ganoderma boninense, G. miniatocinctum and G. tornatum. Biotechnol Lett 40:1541–1550

    CAS  PubMed  Google Scholar 

  11. Chin C-S, Peluso P, Sedlazeck FJ et al (2016) Phased diploid genomes assembly with single molecule real-time sequencing. Nat Methods 13(12):1050–1054

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Korlach J, Gedman G, Kingan SB et al (2017) De novo PacBio long-read and phased avian genome assemblies correct and add to reference genes generated with intermediate and short reads. GigaScience 6:1–16

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Manni M, Berkeley MR, Seppey M et al (2021) BUSCO: assessing genomic data quality and beyond. Curr Protoc 1:e323

    PubMed  Google Scholar 

  14. Kim D, Paggi JM, Park C et al (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37(1):1–12

    Google Scholar 

  15. Holt C, Yandell M (2011) MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinform 12(1):491–504

    Google Scholar 

  16. Solovyev V, Kosarev P, Seledsov I et al (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7(Suppl 1):S101–S112

    Google Scholar 

  17. Chan K-L, Rosli R, Tatarinova TV et al (2017) Seqping: gene prediction pipeline for plant genomes using self-training gene models and transcriptomic data. BMC Bioinform 18(Suppl 1):29–35

    Google Scholar 

  18. Bray NL, Pimentel H, Melsted P et al (2016) Near-optimal probabilistic RNAseq quantification. Nat Biotechnol 34(5):525–527

    CAS  PubMed  Google Scholar 

  19. Ellstrom M, Shah F, Johannsson T et al (2015) The carbon starvation response of the ectomycorrhizal fungus Paxillus involutus. FEMS Microbiol Ecol 91(4):fiv027

    PubMed  PubMed Central  Google Scholar 

  20. Dobin A, Davis CA, Schlesinger F et al (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29(1):15–21

    CAS  PubMed  Google Scholar 

  21. Anders S, Pyl PT, Huber W (2015) HTSeq - a python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169

    CAS  PubMed  Google Scholar 

  22. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550–570

    PubMed  PubMed Central  Google Scholar 

  23. Nurazah Z, Othman A, Ramli US (2020) Principal component analysis (PCA) evaluation of liquid chromatography-mass spectrometry (LC-MS) datasets of Ganoderma boninense intracellular metabolites. J Oil Palm Res 33(3):555–564

    Google Scholar 

  24. Bahari MNA, Sakeh NM, Abdullah SNA et al (2018) Transcriptome profiling at early infection of Elaeis guineensis by Ganoderma boninense provides novel insights on fungal transition from biotrophic to necrotrophic phase. BMC Plant Biol 18:377–401

    PubMed  PubMed Central  Google Scholar 

  25. Dzulkafli SB, Othamn A, Lau BYC et al (2023) Understanding the effects of carbon and nitrogen starvation on the comparative secretomes of G. boninense and G. tornatum. Physiol Mol Plant Pathol. https://doi.org/10.1016/j.pmpp.2023.102084

    Article  Google Scholar 

  26. Utomo C, Tanjung ZA, Aditama R et al (2018) Draft genome sequence of the phytopathogenic fungus Ganoderma boninense, the causal agent of basal stem rot Disease in oil palm. Genome Announc 6(17):10–1128

    Google Scholar 

  27. Utomo C, Tanjung ZA, Aditama R et al (2019) High quality genome sequence reveals the 12 pseudo-chromosomes of Ganoderma boninense. bioRxiv. https://doi.org/10.1101/817510

    Article  Google Scholar 

  28. Chen S, Xu J, Liu C et al (2012) Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 3:913–921

    PubMed  Google Scholar 

  29. Castanera R, Borgognone A, Pisabarro AG et al (2017) Biology, dynamics, and applications of transposable elements in basidiomycete fungi. Appl Microbiol Biotechnol 101:1337–1350

    CAS  PubMed  Google Scholar 

  30. Govender N, Wong MY (2017) Detection of oil palm root penetration by Agrobacterium-mediated transformed Ganoderma boninense, expressing green fluorescent protein. Phytopathology 107:483–490

    CAS  PubMed  Google Scholar 

  31. Hilditch S, Berghall S, Kalkkinen N et al (2007) The missing link in the fungal D-galacturonate pathways: identification of the L-threo-3-deoxy-hexulosonate aldolase. J Biol Chem 282(36):26195–26201

    CAS  PubMed  Google Scholar 

  32. Hong Y, Dashtban M, Kepka G et al (2014) Overexpression of D-xylose reductase (xyl1) gene and antisense inhibition of D-xylulokinase (xyiH) gene increase xylitol production in Trichoderma reesei. BioMed Res Int. https://doi.org/10.1155/2014/169705

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kameshwar AKS, Qin W (2018) Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi. Mycology 2:93–105

    Google Scholar 

  34. Zhang J, Silverstein KAT, Castano JD et al (2019) Gene regulation shifts shed light on fungal adaption in plant biomass decomposers. mBio 10(6):10–1128

    Google Scholar 

  35. Qhanya LB, Matowane G, Chen W et al (2015) Genome-wide annotation and comparative analysis of cytochrome P450 monooxygenases (P450s) in basidiomycete biotrophic plant pathogens. PLoS ONE 10(11):e0142100

    PubMed  PubMed Central  Google Scholar 

  36. Kohut G, Adam AL, Fazekas B et al (2009) N-starvation stress induced FUM gene expression and fumonisin production is mediated via the HOG-type MAPK pathway in Fusarium proliferatum. Int J Food Microbiol 130:65–69

    CAS  PubMed  Google Scholar 

  37. Wu Y, Li T, Gong L et al (2019) Effects of different carbon sources on fumonisin production and FUM gene expression by Fusarium proliferatum. Toxins 11:289–303

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Fountain JC, Bajaj P, Pandey M et al (2016) Oxidative stress and carbon metabolism influence Aspergillus flavus transcriptome composition and secondary metabolite production. Sci Rep 6(38747):1–12

    Google Scholar 

  39. Kameshwar AKS, Qin W (2020) Systematic metadata analysis of brown rot fungi gene expression data reveals the gene involved in Fenton’s reaction and wood decay process. Mycology 11(1):22–37

    CAS  Google Scholar 

  40. Kumar M, Verma S, Gazara RK et al (2018) Genomic and proteomic analysis of lignin degrading and polyhydroxyalkanoate accumulating β–proteobacterium Pandoraea sp. ISTKB. Biotechnol Biofuels 11:154–176

    PubMed  PubMed Central  Google Scholar 

  41. Yuenyong W, Sirikantaramas S, Qu L-J et al (2019) Isocitrate lyase plays important roles in plant salt tolerance. BMC Plant Biol 19:472–485

    PubMed  PubMed Central  Google Scholar 

  42. Dunn MF, Ramirez-Trujillo JA, Hernandez-Lucas I (2009) Major roles of isocitrate lyase and malate synthase in bacterial and fungal pathogenesis. Microbiology 155:3166–3175

    CAS  PubMed  Google Scholar 

  43. Martins MP, Gomes EV, Sanches PR et al (2018) mus-52 disruption and metabolic regulation in Neurospora crassa: transcriptional responses to extracellular phosphate availability. PLoS ONE 13(4):e0195871

    PubMed  PubMed Central  Google Scholar 

  44. Mendez-Liter JA, de Eugenio LI, Prieto A et al (2018) The β–glucosidase secreted by Talaromyces amestolkiae under carbon starvation: a versatile catalyst for biofuel production from plant and algal biomass. Biotechnol Biofuels 11:123–136

    PubMed  PubMed Central  Google Scholar 

  45. Han G, Zhao K, Yan X et al (2019) Differential regulation of mycelia growth and aflatoxin biosynthesis by Aspergillus flavus under different temperatures as revealed by strand-specific. RNA-Seq MicrobiologyOpen 8:e897

    CAS  PubMed  Google Scholar 

  46. Rokas A, Mead ME, Steenwyk JL et al (2021) Biosynthetic gene clusters and the evolution of fungal chemodiversity. Nat Prod Rep 37(7):868–878

    Google Scholar 

  47. Haridas S, Gonzalez JN, Riley R et al (2023) T-Toxin virulence genes: unconnected dots in a sea of repeats. mBio. https://doi.org/10.1128/mbio.00261-23

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ho C-L (2023) Comparative genomics analysis of Ganoderma orthologs involved in plant-pathogenesis. Forests 14:653–672

    Google Scholar 

  49. Zong Y, Li B, Tian S (2015) Effects of carbon, nitrogen and ambient pH on patulin production and related gene expression in Penicillium expansum. Int J Food Microbiol 206:102–108

    CAS  PubMed  Google Scholar 

  50. Li T, Gong L, Jiang G et al (2017) Carbon sources influence fumonisin production in Fusarium proliferatum. Proteomics 17:1700070

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Director General of the Malaysian Palm Oil Board (MPOB) for permission to publish this article. Our appreciation is extended to Christina Cuomo at the Broad Institute of MIT and Harvard, USA for her role in providing advice and assistance with early data analysis. We acknowledge the invaluable contributions of Mariah Zainal Abidin (Energy and Environment Unit, E&P Research Division, MPOB). Special thanks to the late Dr. Richard Cooper for his advice in the initial experimental design of this study. We also express our gratitude to the members of the Breeding and Tissue Culture Unit, ABBC, MPOB, for the usage of their laboratory and technical support. Special thanks to Nik Shazana Nik Mohd Sanusi for her technical support in software configuration. We are grateful to Meilina Ong-Abdullah and Rajinder Singh for their role in providing advice on funding acquisition. This research was funded by the Malaysian Palm Oil Board.

Funding

This work was supported by The Malaysian Palm Oil Board.

Author information

Authors and Affiliations

  1. Malaysian Palm Oil Board, 6, Persiaran Institusi, Bandar Baru Bangi, 43000, Kajang, Selangor, Malaysia

    Jayanthi Nagappan, Siew-Eng Ooi, Kuang-Lim Chan, Faizun Kadri, Zain Nurazah, Mohd Amin Ab Halim, Lee Pei Lee Angel, Shamala Sundram & Eng Ti Leslie Low

  2. School of Biosciences, University of Nottingham Malaysia, Jalan Broga, 43500, Semenyih, Selangor, Malaysia

    Jayanthi Nagappan & Chiew-Foan Chin

  3. School of Biosciences, University of Nottingham, Sutton Bonington Campus, Nr Loughborough, LE12 5RD, UK

    Sean T. May

Authors
  1. Jayanthi Nagappan
    View author publications

    Search author on:PubMed Google Scholar

  2. Siew-Eng Ooi
    View author publications

    Search author on:PubMed Google Scholar

  3. Kuang-Lim Chan
    View author publications

    Search author on:PubMed Google Scholar

  4. Faizun Kadri
    View author publications

    Search author on:PubMed Google Scholar

  5. Zain Nurazah
    View author publications

    Search author on:PubMed Google Scholar

  6. Mohd Amin Ab Halim
    View author publications

    Search author on:PubMed Google Scholar

  7. Lee Pei Lee Angel
    View author publications

    Search author on:PubMed Google Scholar

  8. Shamala Sundram
    View author publications

    Search author on:PubMed Google Scholar

  9. Chiew-Foan Chin
    View author publications

    Search author on:PubMed Google Scholar

  10. Sean T. May
    View author publications

    Search author on:PubMed Google Scholar

  11. Eng Ti Leslie Low
    View author publications

    Search author on:PubMed Google Scholar

Contributions

JN: Conception and design of study, investigation, analysis and interpretation of data, drafting the manuscript, revising the manuscript critically, approval of the version of the manuscript to be published. SEO: Revising the manuscript critically, approval of the version of the manuscript to be published. KLC: Data curation, software. FK: Investigation. ZN: Analysis and interpretation of data, drafting the manuscript. MAAH: Visualization. LPLA: Drafting the manuscript. SS: Resource of study material. CFC: Conception and design of study. STM: Conception and design of study. ETLL: Conception and design of study, supervision, revising the manuscript critically, approval of the version of the manuscript to be published.

Corresponding author

Correspondence to Eng Ti Leslie Low.

Ethics declarations

Competing interests

The authors declare that they have no conflict of interest.

Ethical approval

Our research does not involve human participants and/or animals.

Consent to publish

Informed consent for publication were obtained from all participants included in this study.

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

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nagappan, J., Ooi, SE., Chan, KL. et al. Transcriptional effects of carbon and nitrogen starvation on Ganoderma boninense, an oil palm phytopathogen. Mol Biol Rep 51, 212 (2024). https://doi.org/10.1007/s11033-023-09054-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Version of record:

  • DOI: https://doi.org/10.1007/s11033-023-09054-4

Keywords

Profiles

  1. Sean T. May View author profile
  2. Eng Ti Leslie Low View author profile