Skip to main content
SpringerLink
Log in

Comparative transcriptome profiling of Polianthes tuberosa during a compatible interaction with root-knot nematode Meloidogyne incognita

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

The root-knot nematode (RKN; Meloidogyne spp.) is the most destructive plant parasitic nematode known to date. RKN infections, especially those caused by Meloidogyne incognita, are one of the most serious diseases of tuberose.

Methods and Results

To investigate the molecular mechanism in the host-pathogen interactions, the Illumina sequencing platform was employed to generate comparative transcriptome profiles of uninfected and Meloidogyne incognita-infected tuberose plants, during early, mid, and late infection stage. A total of 7.5 GB (49 million reads) and 9.3 GB (61 million reads) of high-quality data was generated for the control and infected samples, respectively. These reads were combined and assembled using the Trinity assembly program which clustered them into 1,25,060 unigenes. A total of 85,360 validated CDS were obtained from the combined transcriptome whereas 6,795 CDS and 7,778 CDS were found in the data for the control and infected samples, respectively. Gene ontology terms were assigned to 958 and 1,310 CDSs from the control and infected data, respectively. The KAAS pathway analysis revealed that 1,248 CDS in the control sample and 1,482 CDS in the infected sample were enriched with KEGG pathways. The major proportions of CDS were annotated for carbohydrate metabolism, signal transduction and translation related pathways in control and infected samples. Of the 8,289 CDS commonly expressed between the control and infected plants, 256 were significantly upregulated and 129 were significantly downregulated in the infected plants.

Conclusions

Collectively, our results provide a comprehensive gene expression changes in tuberose during its association with RKNs and point to candidate genes that are involved in nematode stress signaling for further investigation. This is the first report addressing genes associated with M. incognita-tuberose interaction and the results have important implications for further characterization of RKN resistance genes in tuberose.

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

Access this article

Log in via an institution

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

Availability of data and material

The raw transcriptome data are submitted to Sequence Read Archive (SRA) (http://www.ncbi.nlm.nih.gov/sra/) under accession number PRJNA670213.

References

  1. Hemalatha D, Prabhu S, Rani WB, Anandham R (2018) Isolation and characterization of toxins from Xenorhabdus nematophilus against Ferrisia virgata (Ckll.) on tuberose, Polianthes tuberosa. Toxicon 146:42–49. https://doi.org/10.1016/j.toxicon.2018.03.012

    Article  CAS  PubMed  Google Scholar 

  2. Kadam V, Chettri D, Mukhopadhyay AK (2019) Study on the symptomatology of floral malady of tuberose associated with foliar nematode infestation on the plants. pharma Innov 8:29–32

    Google Scholar 

  3. Bala SC, Ravindranath N (2018) Field Evaluation of Tuberose Cultivars and Symptom Manifestation Caused by Foliar Nematode, Aphelenchoides besseyi in Tuberose. Int J Curr Microbiol Appl Sci 7:1364–1370. https://doi.org/10.20546/ijcmas.2018.703.163

    Article  Google Scholar 

  4. Barghout N, Chebata N, Moumene S, Khennouf S, Gharbi A, Gharbi A, El Hadi D (2020) Antioxidant and antimicrobial effect of alkaloid bulbs extract of Polianthes tuberosa L. (Amaryllidaceae) cultivated in Algeria. J Drug Delivery Ther 10:44–48

    Article  Google Scholar 

  5. Pocha PNR, Mallikarjun M, Devi GN, Kumar MR (2019) Assessment of Improved Variety of Tuberose (Polianthes tuberosa) Prajwal for Yield and Economics in Western Parts of Chittoor District of Andhra Pradesh. J Krishi Vigyan 8:13–18

    Article  Google Scholar 

  6. Khan MR (2020) Nematode Pest Problems of Tuberose. In: Advances in Pest Management in Commercial Flowers (Eds Pal S & Chakravarthy AK). Apple Academic Press, pp 119–136.

  7. Singh S, Singh B, Singh AP (2015) Nematodes: A Threat to Sustainability of Agriculture. Procedia Environ Sci 29:215–216. https://doi.org/10.1016/j.proenv.2015.07.270

    Article  Google Scholar 

  8. Jones JT et al (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961. https://doi.org/10.1111/mpp.12057

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bernard GC, Egnin M, Bonsi C (2017) The impact of plant-parasitic nematodes on agriculture and methods of control. In: Nematology - Concepts, Diagnosis and Control (Eds Shah MM & Mahamood M) Ch. 4. https://doi.org/10.5772/intechopen.68958

  10. Mishra S, Mahalik JK, Archarya A (2017) Efficacy of oil cakes, nematicides and biocontrol agents for management of Meloidogyne incognita in tuberose. Annals of Plant Protection Sciences. 25:344–388. https://doi.org/10.5958/0974-0163.2017.00033.7

  11. Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends in Genetics 22:396–403. https://doi.org/10.1016/j.tig.2006.05.003

    Article  CAS  PubMed  Google Scholar 

  12. Ranchana P, Anita B (2015) Screening of selected tuberose genotypes for resistance to Meloidogyne incognita in Tamil Nadu. Trends in Biosciences 8(6):1431–1434.

    Google Scholar 

  13. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659. https://doi.org/10.1093/bioinformatics/btl158

    Article  CAS  PubMed  Google Scholar 

  16. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323. https://doi.org/10.1186/1471-2105-12-323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59. https://doi.org/10.1038/nmeth.3176

    Article  CAS  PubMed  Google Scholar 

  18. Götz S et al (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic acids research 36:3420–3435. https://doi.org/10.1093/nar/gkn176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic acids research 35:W182–W185. https://doi.org/10.1093/nar/gkm321

    Article  PubMed  PubMed Central  Google Scholar 

  20. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome biology 11:R106. https://doi.org/10.1186/gb-2010-11-10-r106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Howe EA, Sinha R, Schlauch D, Quackenbush J (2011) RNA-Seq analysis in MeV. Bioinformatics 27:3209–3210. https://doi.org/10.1093/bioinformatics/btr490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jayanthi M, Gantasala NP, Papolu PK, Banakar P, Kumari C, Rao U (2015) Identification and evaluation of internal control genes for gene expression studies by real-time quantitative PCR normalization in different tissues of Tuberose (Polianthes tuberosa). Sci Hort 194:63–70.

    Article  CAS  Google Scholar 

  23. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3:1101.

    Article  CAS  Google Scholar 

  24. Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248. https://doi.org/10.3389/fmicb.2013.00248

    Article  PubMed  PubMed Central  Google Scholar 

  25. Li X, Wu J, Yin L, Zhang Y, Qu J, Lu J (2015) Comparative transcriptome analysis reveals defense-related genes and pathways against downy mildew in Vitis amurensis, grapevine. Plant Physiol Biochem 95:1–4. https://doi.org/10.1016/j.plaphy.2015.06.016

    Article  CAS  PubMed  Google Scholar 

  26. Dai X, Wang Y, Zhang WH (2016) OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Experimental Bot 67:947–960. https://doi.org/10.1093/jxb/erv515

    Article  CAS  Google Scholar 

  27. Mammadov J et al (2018) Wild relatives of maize, rice, cotton, and soybean: treasure troves for tolerance to biotic and abiotic stresses. Front Plant Sci 9:886. https://doi.org/10.3389/fpls.2018.00886

    Article  PubMed  PubMed Central  Google Scholar 

  28. Li J, Zhu L, Hull JJ, Liang S, Daniell H, Jin S, Zhang X (2016) Transcriptome analysis reveals a comprehensive insect resistance response mechanism in cotton to infestation by the phloem feeding insect Bemisia tabaci (whitefly). Plant Biotechnol J 14:1956–1975. https://doi.org/10.1111/pbi.12554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Madhavan J, Jayaswal P, Singh KB, Rao U (2018) Identification of putative flowering genes and transcription factors from flower de novo transcriptome dataset of tuberose (Polianthes tuberosa L.). Data in brief. 20:2027-35. https://doi.org/10.1016/j.dib.2018.09.051

  30. Madhavan J, Jayaswal P, Singh KB, Thakur PK, Rao U (2019) Identification of SSR and miRNA from transcriptome of tuberose. Indian J Hortic 76:141–147. https://doi.org/10.5958/0974-0112.2019.00020.3

    Article  Google Scholar 

  31. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Science 17:9–15. https://doi.org/10.1016/j.tplants.2011.10.001

    Article  CAS  Google Scholar 

  32. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin plant biology 8:397–403. https://doi.org/10.1016/j.pbi.2005.05.014

    Article  CAS  Google Scholar 

  33. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9:244–252. https://doi.org/10.1016/j.tplants.2004.03.006

    Article  CAS  PubMed  Google Scholar 

  34. Palomares-Rius JE, Escobar C, Cabrera J, Vovlas A, Castillo P (2017) Anatomical alterations in plant tissues induced by plant-parasitic nematodes. Frontiers in plant science. 8:1987

  35. Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front plant Sci 7:760. https://doi.org/10.3389/fpls.2016.00760

    Article  PubMed  PubMed Central  Google Scholar 

  36. Li X et al (2018) Genome-wide identification and functional prediction of tobacco lncRNAs responsive to root-knot nematode stress. PloS one 13:e0204506. https://doi.org/10.1371/journal.pone.0204506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Grunewald W et al (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148:358–368. https://doi.org/10.1104/pp.108.119131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front plant Sci 6:902. https://doi.org/10.3389/fpls.2015.00902

    Article  PubMed  PubMed Central  Google Scholar 

  39. Houben M, Van de Poel B (2019) 1-Aminocyclopropane-1-carboxylic acid oxidase (ACO): the enzyme that makes the plant hormone ethylene. Front plant Sci 10:695. https://doi.org/10.3389/fpls.2019.00695

    Article  PubMed  PubMed Central  Google Scholar 

  40. Bahieldin A et al (2016) Ethylene responsive transcription factor ERF109 retards PCD and improves salt tolerance in plant. BMC plant biology 16:216. https://doi.org/10.1186/s12870-016-0908-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Shi H, Liu W, Yao Y, Wei Y, Chan Z (2017) Alcohol dehydrogenase 1 (ADH1) confers both abiotic and biotic stress resistance in Arabidopsis. Plant Sci 262:24–31. https://doi.org/10.1016/j.plantsci.2017.05.013

    Article  CAS  PubMed  Google Scholar 

  42. Lehmann T, Pollmann S (2009) Gene expression and characterization of a stress-induced tyrosine decarboxylase from Arabidopsis thaliana. FEBS Lett 583:1895–1900. https://doi.org/10.1016/j.febslet.2009.05.017

    Article  CAS  PubMed  Google Scholar 

  43. Wang J, Feng J, Jia W, Chang S, Li S, Li Y (2015) Lignin engineering through laccase modification: a promising field for energy plant improvement. Biotechnol Biofuels 8:145. https://doi.org/10.1186/s13068-015-0331-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sasidharan R, Voesenek LA, Pierik R (2011) Cell wall modifying proteins mediate plant acclimatization to biotic and abiotic Stresses. CRC Crit Rev Plant Sci 30:548–562. https://doi.org/10.1080/07352689.2011.615706

    Article  CAS  Google Scholar 

  45. Ebert B et al (2018) The Three Members of the Arabidopsis Glycosyltransferase Family 92 are Functional β-1, 4-Galactan Synthases. Plant and Cell Physiology 59:2624–2636. https://doi.org/10.1093/pcp/pcy180

    Article  CAS  PubMed  Google Scholar 

  46. Hamamouch N et al (2012) The interaction of the novel 30C02 cyst nematode effector protein with a plant β-1, 3-endoglucanase may suppress host defence to promote parasitism. J Experimental Bot 63:3683–3695. https://doi.org/10.1093/jxb/ers058

    Article  CAS  Google Scholar 

  47. Meier S, Ruzvidzo O, Morse M, Donaldson L, Kwezi L, Gehring C (2010) The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes. PloS one 5:5e8904. https://doi.org/10.1371/journal.pone.0008904

    Article  CAS  Google Scholar 

  48. Molinari S, Fanelli E, Leonetti P (2014) Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. Mol Plant Pathol 15:255–264. https://doi.org/10.1111/mpp.12085

    Article  CAS  PubMed  Google Scholar 

  49. Andreasson E et al (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24:2579–2589. https://doi.org/10.1038/sj.emboj.7600737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Bao Y et al (2016) Overexpression of the NDR1/HIN1-like gene NHL6 modifies seed germination in response to abscisic acid and abiotic stresses in Arabidopsis. PloS one 11:e0148572. https://doi.org/10.1371/journal.pone.0148572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Chong J et al (2002) Downregulation of a pathogen-responsive tobacco UDP-Glc: phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. The Plant Cell 14:1093–1107. https://doi.org/10.1105/tpc.010436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Dao TT, Linthorst HJ, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10:397. https://doi.org/10.1007/s11101-011-9211-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was funded by the Department of Science and Technology (DST-SERB). The authors are grateful to the Director, ICAR- IARI and ICAR-NIPB for providing the facilities to carry out the research work. Authors are also thankful to Dr. Raghunath Sadukan, Bidhan Chandra Krishi Vishwavidyalaya (West Bengal) for providing tuberose bulbs for the study.

Author information

Authors and Affiliations

  1. Division of Nematology, ICAR- Indian Agricultural Research Institute, 110012, New Delhi, India

    Kanchan B M Singh & Jayanthi M.

  2. Amity Institute of Biotechnology, Amity University, 201313, Noida, Uttar Pradesh, India

    Kanchan B M Singh & Shivani Chandra

  3. National Institute for Plant Biotechnology, 110012, Pusa, New Delhi, India

    Pawan Jayaswal & Pranab Kumar Mandal

Authors
  1. Kanchan B M Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pawan Jayaswal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shivani Chandra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jayanthi M.
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pranab Kumar Mandal
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MJ conceived, designed, supervised the research and acquired the project funds. KBMS performed the experiments. KBMS and PJ performed the data analysis. The first draft of the manuscript was written by KBMS. MJ, PKM and SC guided and edited the manuscript. All authors read and approved the final manuscript.

Ethics declarations.

Corresponding authors

Correspondence to Jayanthi M. or Pranab Kumar Mandal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, K.B.M., Jayaswal, P., Chandra, S. et al. Comparative transcriptome profiling of Polianthes tuberosa during a compatible interaction with root-knot nematode Meloidogyne incognita. Mol Biol Rep 49, 4503–4516 (2022). https://doi.org/10.1007/s11033-022-07294-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-022-07294-4

Keywords

Search

Navigation