Skip to main content
SpringerLink
Log in

Evolutionary relationship of the NBS-LRR gene family in Melaleuca and Eucalyptus (Myrtaceae)

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Myrtaceous plants such as Eucalyptus and Melaleuca are economically and ecologically important. Many species, including M. alternifolia and M. quinquenervia, are known to be susceptible to the exotic rust fungus Austropuccinia psidii. Identifying the molecular basis of resistance against A. psidii would assist in incorporating resistance to this pathogen for industries producing essential oils and for re-afforestation. Nucleotide-binding sites and leucine-rich repeat (NBS-LRR) genes have been identified as important candidates in several studies. It is unknown whether resistance against A. psidii is conserved among, as well as within species of Myrtaceae. Therefore, this study aimed to identify whether candidate NBS-LRR genes that may have contributed to defence in M. alternifolia and M. quinquenervia are closely related to candidate NBS-LRR genes within the A. psidii resistance loci of E. grandis and E. globulus. NBS-LRR sequences of M. alternifolia, M. quinquenervia and E. grandis were subjected to phylogenetic analysis. Although no candidate NBS-LRR genes for A. psidii defence from M. alternifolia or M. quinquenervia were found to be orthologous to NBS-LRR genes within the E. grandis Ppr1 locus, one candidate NBS-LRR gene for defence against A. psidii in M. quinquenervia was orthologous to a candidate NBS-LRR within Ppr2 from E. globulus. Phylogenetic analysis of multiple species of Myrtaceae also revealed that NBS-LRR genes within Ppr1 may not be the result of recent gene duplications and were highly diverse.

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

Similar content being viewed by others

Data Availability

All data are available as described in the Data archiving statement.

References

  • Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signalling pathways in Arabidopsis. Proc Natl Acad Sci USA 95:10306–10311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alves AA, Rosado CCG, Faria DA, da Silva Guimaraes LM, Lau D, Brommonschenkel SH, Grattapaglia D, Alfenas AC (2012) Genetic mapping provides evidence for the role of additive and non-additive QTLs in the response of inter-specific hybrids of Eucalyptus to Puccinia psidii rust infection. Euphytica 183:27–38

    Article  CAS  Google Scholar 

  • Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Pages 28–36 in: Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology. American Association for Artificial Intelligence Press, Menlo Park, CA, USA

  • Beenken L (2017) Austropuccinia: a new genus name for the myrtle rust Puccinia psidii placed within the redefined family Sphaerophragmiaceae (Pucciniales). Phytotaxa 297:53–61

    Article  Google Scholar 

  • Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS–LRR proteins and their partners. Curr Opin Plant Biol 7:391–399

    Article  CAS  PubMed  Google Scholar 

  • Berthon KA, Fernandez-Winzer L, Sandhu K, Cuddy W, Manea A, Carnegie AJ, Leishman MR (2019) Endangered species face an extra threat: susceptibility to the invasive pathogen Austropuccinia psidii (myrtle rust) in Australia. Aust Plant Pathol 48:385–393

    Article  Google Scholar 

  • Burdon RD, KlápšTě J (2019) Alternative selection methods and explicit or implied economic-worth functions for different traits in tree breeding. Tree Genet Genomes 15:79

    Article  Google Scholar 

  • Butler JB, Freeman JS, Vaillancourt RE, Potts BM, Glen M, Lee DJ, Pegg GS (2016) Evidence for different QTL underlying the immune and hypersensitive responses of Eucalyptus globulus to the rust pathogen Puccinia psidii. Tree Genet Genomes 12:1–13

    Article  Google Scholar 

  • Carnegie AJ, Kathuria A, Pegg GS, Entwistle P, Nagel M, Giblin FR (2016) Impact of the invasive rust Puccinia psidii (myrtle rust) on native Myrtaceae in natural ecosystems in Australia. Biol Invasions 18:127–144

    Article  Google Scholar 

  • Carocha V, Soler M, Hefer C, Cassan-Wang H, Fevereiro P, Myburg AA, Paiva JA, Grima-Pettenati J (2015) Genome-wide analysis of the lignin toolbox of Eucalyptus grandis. New Phytol 206:1297–1313

    Article  CAS  PubMed  Google Scholar 

  • Christie N, Tobias PA, Naidoo S, Külheim C (2016) The Eucalyptus grandis NBS-LRR gene family: physical clustering and expression hotspots. Front Plant Sci 6:1238

    Article  PubMed  PubMed Central  Google Scholar 

  • Collier SM, Hamel LP, Moffett P (2011) Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol Plant Microbe Interact 24:918–931

    Article  CAS  PubMed  Google Scholar 

  • DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nature Rev Genet 11:539–548

    Article  CAS  PubMed  Google Scholar 

  • Esch L, Schaffrath U (2017) An update on jacalin-like lectins and their role in plant defense. Int J Mol Sci 18:1592

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Winzer L, Berthon KA, Entwistle P, Manea A, Winzer N, Pegg G, Carnegie AJ, Leishman MR (2020) Direct and indirect community effects of the invasive plant pathogen Austropuccinia psidii (myrtle rust) in eastern Australian rainforests. Biol Invasions 22:2357–2369

    Article  Google Scholar 

  • Gassmann W, Hinsch ME, Staskawicz BJ (1999) The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20:265–277

    Article  CAS  PubMed  Google Scholar 

  • Haas BJ, Papanicolaou A et al (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protocols 8:1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Holliday JA, Aitken SN et al (2017) Advances in ecological genomics in forest trees and applications to genetic resources conservation and breeding. Mol Ecol 26:706–717. https://doi.org/10.1111/mec.13963

    Article  PubMed  Google Scholar 

  • Hsieh J-F, Chuah A, Patel HR, Sandhu KS, Foley WJ, Külheim C (2018) Transcriptome profiling of Melaleuca quinquenervia challenged by myrtle rust reveals differences in defense responses among resistant individuals. Phytopath 108:495–509

    Article  Google Scholar 

  • Huang X, Yan HD et al (2016) De novo transcriptome analysis and molecular marker development of two Hemarthria species. Front Plant Sci 7:496

    Article  PubMed  PubMed Central  Google Scholar 

  • Isabel N, Holliday JA, Aitken SN (2020) Forest genomics: advancing climate adaptation, forest health, productivity, and conservation. Evol Appl 13:3–10. https://doi.org/10.1111/eva.12902

    Article  PubMed  Google Scholar 

  • Junghans DT, Alfenas AC, Brommonschenkel SH, Oda S, Mello EJ, Grattapaglia D (2003) Resistance to rust (Puccinia psidii Winter) in Eucalyptus: mode of inheritance and mapping of a major gene with RAPD markers. Theor Appl Genet 108:175–180

    Article  CAS  PubMed  Google Scholar 

  • Kainer D, Stone EA, Padovan A, Foley WJ, Külheim C (2018) Accuracy of genomic prediction for foliar terpene traits in Eucalyptus polybractea. G3: Genes. Genomes, Genetics 8:2573–2583

    CAS  Google Scholar 

  • Kearse M, Moir R et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Külheim C, Padovan A, Hefer C, Krause ST, Köllner TG, Myburg AA, Degenhardt J, Foley WJ (2015) The Eucalyptus terpene synthase gene family. BMC Genomics 16:450

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20:116–122

    Article  CAS  PubMed  Google Scholar 

  • Lenz PRN, Nadeau S et al (2020) Multi-trait genomic selection for weevil resistance, growth, and wood quality in Norway Spruce. Evol Appl 13:76–94. https://doi.org/10.1111/eva.12823

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Klápště J et al (2019) Genomic selection for non-key traits in radiata pine when the documented pedigree is corrected using DNA marker information. BMC Genomics 20:1026. https://doi.org/10.1186/s12864-019-6420-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Low YW, Rajaraman S et al (2022) Genomic insights into rapid speciation within the world’s largest tree genus Syzygium. Nat Commun 13:5031. https://doi.org/10.1038/s41467-022-32637-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lozano R, Hamblin MT, Prochnik S, Jannink JL (2015) Identification and distribution of the NBS-LRR gene family in the Cassava genome. BMC Genomics 16:360

    Article  PubMed  PubMed Central  Google Scholar 

  • Mamani EM, Bueno NW, Faria DA, Guimarães LM, Lau D, Alfenas AC, Grattapaglia D (2010) Positioning of the major locus for Puccinia psidii rust resistance (Ppr1) on the Eucalyptus reference map and its validation across unrelated pedigrees. Tree Genet Genome 6:953–962

    Article  Google Scholar 

  • Marone D, Russo MA, Laidò G, De Leonardis AM, Mastrangelo AM (2013) Plant nucleotide binding site–leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. Int J Mol Sci 14:7302–7326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: Adaptable guards. Genome Biol 7:212

    Article  PubMed  PubMed Central  Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    Article  CAS  PubMed  Google Scholar 

  • Naidoo S, Külheim C, Zwart L, Mangwanda R, Oates CN, Visser EA, Wilken FE, Mamni TB, Myburg AA (2014) Uncovering the defence responses of Eucalyptus to pests and pathogens in the genomics age. Tree Physiol 34:931–943

    Article  CAS  PubMed  Google Scholar 

  • Pal A, Chakrabarti A, Basak J (2007) New motifs within the NB-ARC domain of R proteins: probable mechanisms of integration of geminiviral signatures within the host species of Fabaceae family and implications in conferring disease resistance. J Theor Biol 246:564–573

    Article  CAS  PubMed  Google Scholar 

  • Rairdan GJ, Collier SM, Sacco MA, Baldwin TT, Boettrich T, Moffett P (2008) The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signalling. Plant Cell 20:739–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rüdiger H, Gabius HJ (2001) Plant lectins: occurrence, biochemistry, functions and applications. Glycoconj J 18:589–613

    Article  PubMed  Google Scholar 

  • Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV (2016) Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Serrano M, Coluccia F, Torres M, L’Haridon F, Métraux JP (2014) The cuticle and plant defense to pathogens. Front Plant Sci 5:274

    Article  PubMed  PubMed Central  Google Scholar 

  • Shao ZQ, Zhang YM et al (2014) Long-term evolution of nucleotide-binding site-leucine-rich repeat genes: understanding gained from and beyond the legume family. Plant Physiol 166:217–234

    Article  PubMed  PubMed Central  Google Scholar 

  • Silva AC, Souza PE, Resende MLV, Silva MB, Ribeiro PM, Zeviani WM (2014) Local and systemic control of powdery mildew in Eucalyptus using essential oils and decoctions from traditional Brazilian medicinal plants. Forest Pathol 44:145–153

    Article  Google Scholar 

  • Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100

    Article  CAS  PubMed  Google Scholar 

  • Takken FL, Goverse A (2012) How to build a pathogen detector: structural basis of NB-LRR function. Curr Opin Plant Biol 15:375–384

    Article  CAS  PubMed  Google Scholar 

  • Tameling WI, Vossen JH, Albrecht M, Lengauer T, Berden JA, Haring MA, Cornelissen BJ, Takken FL (2006) Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol 140:1233–1245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thornhill AH, Ho SY, Külheim C, Crisp MD (2015) Interpreting the modern distribution of Myrtaceae using a dated molecular phylogeny. Mol Phylogenet Evol 93:29–43

    Article  PubMed  Google Scholar 

  • Thumma B, Pegg G, Warburton P, Brawner J, Macdonell P, Southerton S (2013) Molecular tagging of rust resistance genes in Eucalypts. Report PHA_6.2. Plant Health Australia Limited, pp 1–15

  • Tobias PA, Guest DI (2014) Tree immunity: growing old without antibodies. Trends Plant Sci 19:367–370

    Article  CAS  PubMed  Google Scholar 

  • Tobias PA, Guest DI, Külheim C, Hsieh J-F, Park RF (2016) A curious case of resistance to a new encounter pathogen: Myrtle rust in Australia. Mol Plant Pathol 17:783–788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tobias PA, Christie N, Naidoo S, Guest DI, Külheim C (2017a) Identification of the Eucalyptus grandis chitinase gene family and expression characterization under different biotic stress challenges. Tree Physiol 37:565–582

    Article  CAS  PubMed  Google Scholar 

  • Tobias PA, Guest D, Külheim C, Park RF (2017b) De novo transcriptome study identifies candidate genes involved in resistance to Austropuccinia psidii (myrtle rust) in Syzygium luehmannnii (Riberry). Phytopath 108:627–640. https://doi.org/10.1094/PHYTO-09-17-0298-R

    Article  Google Scholar 

  • Trigg J, Gutwin K, Keating AE, Berger B (2011) Multicoil2: predicting coiled coils and their oligomerization states from sequence in the twilight zone. PLoS ONE 6:e23519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuda K, Katagiri F (2010) Comparing signalling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465

    Article  CAS  PubMed  Google Scholar 

  • Underwood W (2012) The plant cell wall: a dynamic barrier against pathogen invasion. Front Plant Sci 3:85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urbach JM, Ausubel FM (2017) The NBS-LRR architectures of plant R-proteins and metazoan NLRs evolved in independent events. Proc Natl Acad Sci USA 114:1063–1068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Der Biezen EA, Jones JD (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456

    Article  PubMed  Google Scholar 

  • Vijay N, Poelstra JW, Künstner A, Wolf JB (2013) Challenges and strategies in transcriptome assembly and differential gene expression quantification. A comprehensive in silico assessment of RNA-seq experiments. Mol Ecol 22:620–634

    Article  CAS  PubMed  Google Scholar 

  • Wan H, Yuan W et al (2012) Analysis of TIR-and non-TIR-NBS-LRR disease resistance gene analogous in pepper: characterization, genetic variation, functional divergence and expression patterns. BMC Genomics 13:502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 29:118–120

    Article  Google Scholar 

  • Zhang Y, Xia R, Kuang H, Meyers BC (2016) The diversification of plant NBS-LRR defense genes directs the evolution of microRNAs that target them. Mol Biol Evol 33:2692–2705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng F, Wu H, Zhang R, Li S, He W, Wong FL, Li G, Zhao S, Lam HM (2016) Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family. BMC Genomics 17:402

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng X, Chen S, et al (2022) The chromosome-level Melaleuca alternifolia genome provides insights into the molecular mechanisms underlying terpenoids biosynthesis. Ind Crops and Products https://doi.org/10.1016/j.indcrop.2022.115819

  • Zhong Y, Yin H, Sargent DJ, Malnoy M, Cheng ZMM (2015) Species-specific duplications driving the recent expansion of NBS-LRR genes in five Rosaceae species. BMC Genomics 16:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Zipfel C, Felix G (2005) Plants and animals: a different taste for microbes? Curr Opin Plant Biol 8:353–360

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Peri Tobias (University of Sydney), for kindly providing aligned sequences of the 480 NBS-LRR genes of E. grandis. We are grateful to Dr. Karanjeet Sandhu (University of Sydney) for his assistance with myrtle rust inoculation experiments and Dr. Hardip Patel and Mr. Aaron Chuah (Australian National University) for their help with transcriptome assemblies and analysis.

Funding

Funding was provided by Plant Health Australia (PHA-P214) to C. K. and W. J. F. and by Rural Industries Research Development Corporation (PRJ-007524) to C. K. and W. J. F.

Author information

Author notes

  1. Swapan Chakrabarty and Ji-Fan Hsieh have contributed equally to this study.

Authors and Affiliations

  1. College of Forest Resource and Environmental Science, Michigan Technological University, Houghton, MI, 49931, USA

    Swapan Chakrabarty & Carsten Külheim

  2. Research School of Biology, The Australian National University, 46 Sullivans Creek Rd, Acton, ACT, 2601, Australia

    Ji-Fan Hsieh & William J. Foley

  3. Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA, 50011, USA

    Panchali Chakraborty

Authors
  1. Swapan Chakrabarty
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ji-Fan Hsieh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Panchali Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. William J. Foley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carsten Külheim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carsten Külheim.

Ethics declarations

Competing interests

The authors declare no competing interests.

Data archiving statement

Raw Illumina read data for the study by Hsieh et al. (2018) is available at the Sequence Read Archive database under SRA identifier SRP095052 as well as BioProject accession number PRJNA357284. Raw Illumina read data for the study by Hsieh, Foley, Külheim (unpublished), has been submitted to the Sequence Read Archive database under SRA submission SUB12328219 as well as BioProject accession number PRJNA905442. The assembled and annotated transcriptomes are available through each BioProject (SUB12850958, SUB12845553).

Additional information

Communicated by L. Bianco.

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 886 KB)

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

Chakrabarty, S., Hsieh, JF., Chakraborty, P. et al. Evolutionary relationship of the NBS-LRR gene family in Melaleuca and Eucalyptus (Myrtaceae). Tree Genetics & Genomes 19, 25 (2023). https://doi.org/10.1007/s11295-023-01602-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-023-01602-0

Keywords

Search

Navigation