Skip to main content
SpringerLink
Log in

Genome Wide Identification of the MLO Gene Family Associated with Powdery Mildew Resistance in Rubber Trees (Hevea brasiliensis)

  • Published:
Tropical Plant Biology Aims and scope Submit manuscript

Abstract

Powdery mildew (PM) is one of the most destructive diseases affecting rubber trees (Hevea brasiliensis), leading to severe yield losses. Sulfur dusting is used to control the propagation of the disease, and no specific fungicides have been developed yet. Therefore, identification of genetic level disease resistance in the rubber trees is very crucial. In this study, we describe the whole-genome sequencing of a PM resistant rubber clone, RRIC 52, as well as a PM susceptible clone, PB 235, using massively parallel paired-end sequencing. The MLO (mildew resistance locus O) genes were identified and analyzed for their structural features, and the variations were compared in the MLO gene family between the two clones. Sequencing results showed that RRIC 52 contained 4,280,477 SNPs and 400,667 InDels, while PB 235 contained 3,651,524 SNPs and 318,899 InDels. We identified 34 MLO genes (HbMLO 1 to 34) in the rubber genome. Multiple sequence alignment identified the conserved MLO domain and its TM domain in all HbMLO proteins. Sequence analysis identified non-synonymous variations (NSVs) in 12 HbMLO proteins. Phylogenetic analysis of the HBMLO genes revealed seven different clades. Six HbMLO genes in Clade V were orthologous to Arabidopsis genes where PM interaction was previously identified. The outcomes of this study widen the understanding of the MLO gene family, which can be used in breeding disease resistant rubber varieties in the future.

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

References

  • Acevedo-Garcia J, Kusch S, Panstruga R (2014) Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytol 204(2):273–281

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  CAS  Google Scholar 

  • Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley MLO gene: a novel control element of plant pathogen resistance. Cell 88:695–705

    Article  Google Scholar 

  • Chen Y, Wang Y, Zhang H (2014) Genome-wide analysis of the mildew resistance locus o (‘MLO’) gene family in tomato (‘Solanum lycopersicum’L.). Plant Omics 7(2):87

  • Consonni C, Bednarek P, Humphry M, Francocci F, Ferrari S, Harzen A, Panstruga R (2010) Tryptophan-derived metabolites are required for antifungal defense in the Arabidopsis mlo2 mutant. Plant Physiol 152(3):1544–1561

    Article  CAS  Google Scholar 

  • Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Panstruga R (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38(6):716–720. https://doi.org/10.1038/ng1806

    Article  CAS  PubMed  Google Scholar 

  • Devoto A, Hartmann HA, Piffanelli P, Elliott C, Simmons C, Taramino G, Goh CS, Cohen FE, Emerson BC, Schulze-Lefert P, Panstruga R (2003) Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. J Mol Evol 56:77–88

    Article  CAS  Google Scholar 

  • Devoto A, Piffanelli P, Nilsson IM, Wallin E, Panstruga R, von Heijne G, Schulze-Lefert P (1999) Topology, subcellular localization, and sequence diversity of the MLO family in plants. J Biol Chem 274:34993–35004

    Article  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Feechan A, Jermakow AM, Torregrosa L, Panstruga R, Dry IB (2008) Identification of grapevine MLO gene candidates involved in susceptibility to powdery mildew. Funct Plant Biol 35:1255–1266

    Article  CAS  Google Scholar 

  • Fernando TM (1971) Oidium leaf disease-the effect of environment and control measures on incidence of disease and atmospheric spore concentration. Quart J Rubb Res Inst Ceylon 48:100–111

    Google Scholar 

  • Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Bateman A (2016) The Pfam protein families’ database: towards a more sustainable future. Nucleic Acids Res 44(1):279–285. https://doi.org/10.1093/nar/gkv1344

    Article  CAS  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

  • Jayasinghe CK (2001) Common disease. In: Tillekaratne LMK, Nugawela A (eds) Hand book of rubber agronomy, vol 1. Rubber Research Institute of Sri Lanka, Sri Lanka, pp 97–105

    Google Scholar 

  • Jorgensen JH (1992) Discovery, characterization and exploitation of MLO powdery mildew resistance in barley. Euphytica 63:141–152

    Article  Google Scholar 

  • Kim MC, Lee SH, Kim JK, Chun HJ, Choi MS, Chung WS, Moon BC, Kang CH, Park CY, Yoo JH, Kang YH, Koo SC, Koo YD, Jung JC, Kim ST, Schulze-Lefert P, Lee SY, Cho MJ (2002) MLO, a modulator of plant defense and cell death, is a novel calmodulin-binding protein. J Biol Chem 277:19304–19314

    Article  CAS  Google Scholar 

  • Konishi S, Sasakuma T, Sasanuma T (2010) Identifcation of novel Mlo family members in wheat and their genetic characterization. Genes Genet Sys 85:167–175

    Article  CAS  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25(14):1754–1760

    Article  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079

    Article  Google Scholar 

  • Liyanage AS, Kuruvilla JC (1992) Diseases of economic importance in rubber. In: Sethuraj MR, Mathew NM (eds) Natural rubber: biology, cultivation and technology, developments in crop science, vol 23. Elsevier, The Netherland, pp 324–359

    Google Scholar 

  • Liyanage KK, Khan S, Mortimer PE, Hyde KD, Xu J, Brooks S, Ming Z (2016) Powdery mildew disease of rubber tree. Forest Pathol 46(2):90–103

    Article  Google Scholar 

  • Liyanage KK, Khan S, Brooks S, Mortimer PE, Karunarathna SC, Xu J, Hyde KD (2018) Morpho-molecular characterization of two Ampelomyces spp. (Pleosporales) strains. Mycoparasites of powdery mildew of Hevea brasiliensis. Front Microbiol 9:12. https://doi.org/10.3389/fmicb.2018.00012

    Article  PubMed  PubMed Central  Google Scholar 

  • Liyanage KK, Khan S, Brooks S, Mortimer PE, Karunarathna SC, Xu J, Hyde KD (2017) Taxonomic revision and phylogenetic analyses of rubber powdery mildew fungi. Microb Pathog 105:185–195

    Article  CAS  Google Scholar 

  • Min T, Haibin C, Aihua S, Huisun H (2012) In vitro culture method of powdery mildew (O. heveae Stanmann) of Hevea brasiliensis. Afr J Biotechnol 11(65):13167–13172

    Google Scholar 

  • Mistry J, Finn RD, Eddy SR, Bateman A, Punta M (2013) Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res 41(12):e121. https://doi.org/10.1093/nar/gkt263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore AD, Heldy A, Terrapon N, Weiner J, Bornberg-Bauer E. (2014) DoMosaics: software for domain arrangement visualization and domain-centric analysis of proteins. Bioinformatics, 30(2): 282–283. https://doi.org/10.1093/bioinformatics/ btt640

  • Narayanan C, Mydin KK (2012) Breeding for disease resistance in Hevea spp.-status, potential threats, and possible strategies. In: Sniezko RA, Yanchuk AD, Kliejunas JT, Palmieri KM, Alexander JM, Frankel SJ, tech. coords (eds) Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: Disease and insect resistance in forest trees. Gen. Tech. Rep. PSW-GTR-240, 240. Pacific Southwest Research Station, Forest Service, US Department of Agriculture, Albany, CA, pp 240-251

  • Okonechnikov K, Golosova O, Fursov M, Varlamov A, Vaskin Y, Efremov I, Tleukenov T (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28(8):1166–1167. https://doi.org/10.1093/bioinformatics/bts091

    Article  CAS  PubMed  Google Scholar 

  • Omasits U, Ahrens CH, Müller S, Wollscheid B (2014) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30(6):884–886. https://doi.org/10.1093/bioinformatics/btt607

    Article  CAS  PubMed  Google Scholar 

  • Panstruga R (2005) Discovery of novel conserved peptide domains by ortholog comparison within plant multi-protein families. Plant Mol Biol 59(3):485–500

    Article  CAS  Google Scholar 

  • Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129(3):1076–1085

    Article  CAS  Google Scholar 

  • Qin B, Zheng F, Zhang Y (2015) Molecular cloning and characterization of a Mlo gene in rubber tree (Hevea brasiliensis). J Plant Physiol 175:78–85

    Article  CAS  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal omega. Mol Syst Biol 7(539):539. https://doi.org/10.1038/msb.2011.75

    Article  PubMed  PubMed Central  Google Scholar 

  • Silvestro D, Michalak I (2012) RaxmlGUI: a graphical front-end for RAxML. Org Diver Evol 12(4):335–337. https://doi.org/10.1007/s13127-011-0056-0

    Article  Google Scholar 

  • Tang C, Yang M, Fang Y, Luo Y et al (2016) The rubber tree genome reveals new insight into rubber production and species adaptation. Nat Plants 2:16073. https://doi.org/10.1038/NPLANTS.2016.73

  • Wastie RL (1975) Disease of rubber and their control. Tropical Pest Manag 21(3):268–288

    Google Scholar 

  • Wolter M, Hollricher K, Salamini F, Schulze-Lefert P (1993) The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol Genet Genomics 239:122–128

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Key Research Program of Frontier Sciences, CAS, grant No. QYZDY-SSW-SMC014. We would like to thank the National Science Foundation of China (NSFC) for funding this work under the project codes Y4ZK111B01, 41761144055, 41771063, 31650410651, 41761144055 and 31550110215. Key Research Program of the Ministry of Sciences and Technology (Grant No. 2017YFC0505101) of China partially supported this work.

Author information

Authors and Affiliations

  1. Center of Excellence in Fungal Research, and School of Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Kapila K. Liyanage, Siraprapa Brooks & Kevin D. Hyde

  2. World Agroforestry Centre, East and Central Asia, Kunming, 132 Lanhei Rd, Heilongtan, Kunming, Yunnan, China

    Kapila K. Liyanage, Sehroon Khan, Peter E. Mortimer & Jianchu Xu

  3. Center for Mountain Ecosystem Studies, Kunming Institute of Botany, Chinese Academy of Science, Kunming, 650201, Yunnan, China

    Kapila K. Liyanage, Sehroon Khan, Peter E. Mortimer, Sadia Nadir, Kevin D. Hyde & Jianchu Xu

  4. Department of Chemistry, University of Science and Technology, Bannu, KPK, 28100, Pakistan

    Sadia Nadir

  5. Department of Agricultural Biology, Faculty of Agriculture, University of Peradeniya, Peradeniya, Sri Lanka

    Venura Herath

  6. Rubber Research Institute of Sri Lanka, Dartonfield, Agalawatta, Sri Lanka

    Kapila K. Liyanage

Authors
  1. Kapila K. Liyanage
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sehroon Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Venura Herath
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Siraprapa Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter E. Mortimer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sadia Nadir
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kevin D. Hyde
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jianchu Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Sehroon Khan or Jianchu Xu.

Additional information

Communicated by: Jorge M. Santamaria

Publisher’s Note

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

Electronic supplementary material

ESM 1

(DOCX 12 kb)

ESM 2

(DOCX 12 kb)

ESM 3

(DOCX 13 kb)

ESM 4

(JPG 261 kb)

ESM 5

(JPG 291 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liyanage, K.K., Khan, S., Herath, V. et al. Genome Wide Identification of the MLO Gene Family Associated with Powdery Mildew Resistance in Rubber Trees (Hevea brasiliensis). Tropical Plant Biol. 13, 331–342 (2020). https://doi.org/10.1007/s12042-020-09262-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12042-020-09262-3

Keywords

Search

Navigation