Home LiteratureArticle Details
PMID: 20844752 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

The CC-NB-LRR-type Rdg2a resistance gene confers immunity to the seed-borne barley leaf stripe pathogen in the absence of hypersensitive cell death.

PloS one ·Vol. 5 ·No. 9 ·2010-09-10

Bulgarelli D, Biselli C, Collins NC, Consonni G, Stanca AM, Schulze-Lefert P, Valè G

Abstract

Leaf stripe disease on barley (Hordeum vulgare) is caused by the seed-transmitted hemi-biotrophic fungus Pyrenophora graminea. Race-specific resistance to leaf stripe is controlled by two known Rdg (Resistance to Drechslera graminea) genes: the H. spontaneum-derived Rdg1a and Rdg2a, identified in H. vulgare. The aim of the present work was to isolate the Rdg2a leaf stripe resistance gene, to characterize the Rdg2a locus organization and evolution and to elucidate the histological bases of Rdg2a-based leaf stripe resistance. We describe here the positional cloning and functional characterization of the leaf stripe resistance gene Rdg2a. At the Rdg2a locus, three sequence-related coiled-coil, nucleotide-binding site, and leucine-rich repeat (CC-NB-LRR) encoding genes were identified. Sequence comparisons suggested that paralogs of this resistance locus evolved through recent gene duplication, and were subjected to frequent sequence exchange. Transformation of the leaf stripe susceptible cv. Golden Promise with two Rdg2a-candidates under the control of their native 5' regulatory sequences identified a member of the CC-NB-LRR gene family that conferred resistance against the Dg2 leaf stripe isolate, against which the Rdg2a-gene is effective. Histological analysis demonstrated that Rdg2a-mediated leaf stripe resistance involves autofluorescing cells and prevents pathogen colonization in the embryos without any detectable hypersensitive cell death response, supporting a cell wall reinforcement-based resistance mechanism. This work reports about the cloning of a resistance gene effective against a seed borne disease. We observed that Rdg2a was subjected to diversifying selection which is consistent with a model in which the R gene co-evolves with a pathogen effector(s) gene. We propose that inducible responses giving rise to physical and chemical barriers to infection in the cell walls and intercellular spaces of the barley embryo tissues represent mechanisms by which the CC-NB-LRR-encoding Rdg2a gene mediates resistance to leaf stripe in the absence of hypersensitive cell death.

MeSH Terms
Amino Acid Sequence Ascomycota/immunology,physiology Cell Death Chromosome Mapping Cotyledon/chemistry,genetics,immunology,microbiology Hordeum/chemistry,genetics,immunology,microbiology Immunity, Innate Molecular Sequence Data Plant Diseases/immunology,microbiology Plant Leaves/chemistry,genetics,immunology,microbiology Plant Proteins/chemistry,genetics,immunology Protein Structure, Tertiary Protein Transport Sequence Alignment
Chemicals
Plant Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Bulgarelli Davide
Genomic Research Center, CRA-GPG, Fiorenzuola d'Arda, Italy.
Biselli Chiara
Collins Nicholas C
Consonni Gabriella
Stanca Antonio M
Schulze-Lefert Paul
Valè Giampiero
References (53)
53 references, click to expand
  1. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily.
    Plant J. 1999 Nov;20(3):317-32 PMID: 10571892
  2. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene.
    Trends Genet. 2004 Mar;20(3):116-22 PMID: 15049302
  3. Cleavage of Nuclear DNA into Oligonucleosomal Fragments during Cell Death Induced by Fungal Infection or by Abiotic Treatments.
    Plant Cell. 1996 Mar;8(3):393-402 PMID: 12239388
  4. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis.
    Plant Cell. 2003 Apr;15(4):809-34 PMID: 12671079
  5. Molecular diversity at the plant-pathogen interface.
    Dev Comp Immunol. 2008;32(7):736-44 PMID: 18191204
  6. Nar-1 and Nar-2, Two Loci Required for Mla12-Specified Race-Specific Resistance to Powdery Mildew in Barley.
    Plant Cell. 1994 Jul;6(7):983-994 PMID: 12244263
  7. tA single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta.
    Plant Cell. 2000 Nov;12(11):2033-46 PMID: 11090207
  8. Natural variation in the Arabidopsis response to the avirulence gene hopPsyA uncouples the hypersensitive response from disease resistance.
    Mol Plant Microbe Interact. 2005 Oct;18(10):1054-60 PMID: 16255244
  9. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells.
    Plant Cell. 2004 Mar;16(3):755-68 PMID: 14973158
  10. PromH: Promoters identification using orthologous genomic sequences.
    Nucleic Acids Res. 2003 Jul 1;31(13):3540-5 PMID: 12824362
  11. Histological and molecular analysis of Rdg2a barley resistance to leaf stripe.
    Mol Plant Pathol. 2008 Jul;9(4):463-78 PMID: 18705861
  12. High-resolution genetic mapping of the leaf stripe resistance gene Rdg2a in barley.
    Theor Appl Genet. 2004 May;108(7):1401-8 PMID: 14689188
  13. Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):15253-8 PMID: 14645721
  14. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses.
    Science. 2007 Feb 23;315(5815):1098-103 PMID: 17185563
  15. Programmed cell death during embryogenesis in maize.
    Ann Bot. 2002 Aug;90(2):287-92 PMID: 12197527
  16. Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region.
    Plant Cell. 1997 Apr;9(4):641-51 PMID: 9144966
  17. Tobacco mosaic virus regulates the expression of its own resistance gene N.
    Plant Physiol. 2004 Aug;135(4):2392-7 PMID: 15299123
  18. Nuclear trafficking during plant innate immunity.
    Mol Plant. 2008 May;1(3):411-22 PMID: 19825550
  19. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis.
    Nature. 1999 Aug 12;400(6745):667-71 PMID: 10458161
  20. Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway.
    Plant Cell. 2001 Feb;13(2):337-50 PMID: 11226189
  21. Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection.
    Mol Plant Microbe Interact. 2010 Apr;23(4):497-509 PMID: 20192836
  22. Genomic regions determining resistance to leaf stripe (Pyrenophora graminea) in barley.
    Genome. 2002 Jun;45(3):460-6 PMID: 12033613
  23. The Rx gene from potato controls separate virus resistance and cell death responses.
    Plant Cell. 1999 May;11(5):781-92 PMID: 10330465
  24. Plant NBS-LRR proteins in pathogen sensing and host defense.
    Nat Immunol. 2006 Dec;7(12):1243-9 PMID: 17110940
  25. The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana.
    Genetics. 2004 Mar;166(3):1517-27 PMID: 15082565
  26. The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat.
    Plant J. 2001 Feb;25(3):335-48 PMID: 11208025
  27. Structure, function and evolution of plant disease resistance genes.
    Curr Opin Plant Biol. 2000 Aug;3(4):278-84 PMID: 10873844
  28. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines.
    Plant Cell. 2005 Jun;17(6):1839-50 PMID: 15894715
  29. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process.
    Genome Res. 1998 Nov;8(11):1113-30 PMID: 9847076
  30. Correlation between transcript abundance of the RB gene and the level of the RB-mediated late blight resistance in potato.
    Mol Plant Microbe Interact. 2009 Apr;22(4):447-55 PMID: 19271959
  31. Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames.
    Plant Physiol. 2003 Feb;131(2):558-67 PMID: 12586880
  32. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana.
    Nature. 2003 May 1;423(6935):74-7 PMID: 12721627
  33. Independent evolution of functional Pm3 resistance genes in wild tetraploid wheat and domesticated bread wheat.
    Plant J. 2009 Mar;57(5):846-56 PMID: 18980638
  34. RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance.
    Plant Cell. 2004 Dec;16(12):3480-95 PMID: 15548741
  35. Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus.
    Proc Natl Acad Sci U S A. 2009 Jun 9;106(23):9519-24 PMID: 19470492
  36. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3135-40 PMID: 15703292
  37. Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter.
    Plant J. 2009 Feb;57(3):413-25 PMID: 18808453
  38. The expression pattern of a rice disease resistance gene xa3/xa26 is differentially regulated by the genetic backgrounds and developmental stages that influence its function.
    Genetics. 2007 Sep;177(1):523-33 PMID: 17720929
  39. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions.
    Annu Rev Phytopathol. 2007;45:399-436 PMID: 17506648
  40. RiceGAAS: an automated annotation system and database for rice genome sequence.
    Nucleic Acids Res. 2002 Jan 1;30(1):98-102 PMID: 11752265
  41. Rapid generation of new powdery mildew resistance genes after wheat domestication.
    Plant J. 2006 Jul;47(1):85-98 PMID: 16740148
  42. Balancing selection favors guarding resistance proteins.
    Trends Plant Sci. 2002 Feb;7(2):67-71 PMID: 11832277
  43. Recognitional specificity and evolution in the tomato-Cladosporium fulvum pathosystem.
    Mol Plant Microbe Interact. 2009 Oct;22(10):1191-202 PMID: 19737093
  44. Evolutionary dynamics of plant R-genes.
    Science. 2001 Jun 22;292(5525):2281-5 PMID: 11423651
  45. Structure-function analysis of the tobacco mosaic virus resistance gene N.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14789-94 PMID: 11121079
  46. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  47. Quantitative resistance to barley leaf stripe (Pyrenophora graminea) is dominated by one major locus.
    Theor Appl Genet. 1996 Jul;93(1-2):97-101 PMID: 24162205
  48. Identification and mapping of the leaf stripe resistance gene Rdg1a in Hordeum spontaneum.
    Theor Appl Genet. 2010 Apr;120(6):1207-18 PMID: 20041226
  49. Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation
    Plant Physiol. 1999 Apr;119(4):1251-60 PMID: 10198083
  50. Two modes of pathogen recognition by plants.
    Proc Natl Acad Sci U S A. 2006 Jun 6;103(23):8575-6 PMID: 16735473
  51. Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots.
    BMC Genomics. 2008 Apr 28;9:194 PMID: 18442363
  52. The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley.
    Genetics. 1999 Dec;153(4):1929-48 PMID: 10581297
  53. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid.
    Plant Mol Biol. 1996 Dec;32(6):1125-34 PMID: 9002611
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
DOI
10.1371/journal.pone.0012599
Published
2010-09-10
Epub
2010-00-10
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC2937021
Subset
IM
External Links
PubMed source DOI: 10.1371/journal.pone.0012599 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2