Home LiteratureArticle Details
PMID: 12172030 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley.

The Plant cell ·Vol. 14 ·No. 8 ·2002-08-00 ·Pages 1903-17

Wei F, Wing RA, Wise RP

Abstract

Genes that confer defense against pathogens often are clustered in the genome and evolve via diverse mechanisms. To evaluate the organization and content of a major defense gene complex in cereals, we determined the complete sequence of a 261-kb BAC contig from barley cv Morex that spans the Mla (powdery mildew) resistance locus. Among the 32 predicted genes on this contig, 15 are associated with plant defense responses; 6 of these are associated with defense responses to powdery mildew disease but function in different signaling pathways. The Mla region is organized as three gene-rich islands separated by two nested complexes of transposable elements and a 45-kb gene-poor region. A heterochromatic-like region is positioned directly proximal to Mla and is composed of a gene-poor core with 17 families of diverse tandem repeats that overlap a hypermethylated, but transcriptionally active, gene-dense island. Paleontology analysis of long terminal repeat retrotransposons indicates that the present Mla region evolved over a period of >7 million years through a variety of duplication, inversion, and transposon-insertion events. Sequence-based recombination estimates indicate that R genes positioned adjacent to nested long terminal repeat retrotransposons, such as Mla, do not favor recombination as a means of diversification. We present a model for the evolution of the Mla region that encompasses several emerging features of large cereal genomes.

MeSH Terms
DNA Methylation DNA Transposable Elements/genetics Evolution, Molecular Fungi/growth & development Gene Expression Genome, Plant Hordeum/genetics,microbiology Immunity, Innate/genetics Minisatellite Repeats/genetics Molecular Sequence Data Multigene Family/genetics Mutagenesis, Insertional Plant Diseases/genetics,microbiology Plant Proteins/genetics Retroelements/genetics Signal Transduction/genetics Tandem Repeat Sequences/genetics Transcriptional Activation/genetics
Chemicals
DNA Transposable Elements MLA1 protein, Hordeum vulgare Plant Proteins Retroelements
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wei Fusheng
Interdepartmental Genetics Program and Department of Plant Pathology, Iowa State University, Ames, IA 50011-1020, USA.
Wing Rod A
Wise Roger P
References (63)
63 references, click to expand
  1. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis.
    Plant Cell. 1999 Nov;11(11):2099-112 PMID: 10559437
  2. Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution.
    Plant J. 2001 May;26(3):307-16 PMID: 11439119
  3. Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8807-14 PMID: 10922039
  4. Ethylene-regulated expression of a tomato fruit ripening gene encoding a proteinase inhibitor I with a glutamic residue at the reactive site.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8012-6 PMID: 2903499
  5. Molecular characterization of a tandem repeat, Afa family, and its distribution among Triticeae.
    Genome. 1995 Jun;38(3):479-86 PMID: 7557360
  6. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11655-60 PMID: 11027363
  7. Consed: a graphical tool for sequence finishing.
    Genome Res. 1998 Mar;8(3):195-202 PMID: 9521923
  8. Alleles of Pto and Fen occur in bacterial speck-susceptible and fenthion-insensitive tomato cultivars and encode active protein kinases.
    Plant Cell. 1997 Jan;9(1):61-73 PMID: 9014365
  9. BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.).
    Plant Mol Biol. 1993 Aug;22(5):829-46 PMID: 7689350
  10. 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
  11. Putting knowledge of plant disease resistance genes to work.
    Curr Opin Plant Biol. 2001 Aug;4(4):281-7 PMID: 11418336
  12. Tissue-specific patterns of a maize Myb transcription factor are epigenetically regulated.
    Plant J. 2001 Sep;27(5):467-78 PMID: 11576430
  13. 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
  14. The generation of plant disease resistance gene specificities.
    Trends Plant Sci. 2000 Sep;5(9):373-9 PMID: 10973092
  15. How can we deliver the large plant genomes? Strategies and perspectives.
    Curr Opin Plant Biol. 2002 Apr;5(2):173-7 PMID: 11856615
  16. The paleontology of intergene retrotransposons of maize.
    Nat Genet. 1998 Sep;20(1):43-5 PMID: 9731528
  17. The distribution of genes in the genomes of Gramineae.
    Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6857-61 PMID: 9192656
  18. Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans.
    Genetics. 2000 Dec;156(4):1661-9 PMID: 11102365
  19. A contiguous 60 kb genomic stretch from barley reveals molecular evidence for gene islands in a monocot genome.
    Nucleic Acids Res. 1998 Feb 15;26(4):1056-62 PMID: 9461468
  20. Molecular characterization and phylogenetic studies of a wound-inducible proteinase inhibitor I gene in Lycopersicon species.
    Proc Natl Acad Sci U S A. 1986 Oct;83(19):7277-81 PMID: 3463966
  21. Base-calling of automated sequencer traces using phred. II. Error probabilities.
    Genome Res. 1998 Mar;8(3):186-94 PMID: 9521922
  22. The human major histocompatability complex: lessons from the DNA sequence.
    Annu Rev Genomics Hum Genet. 2000;1:117-37 PMID: 11701627
  23. Post-transcriptional regulation through the HO 3'-UTR by Mpt5, a yeast homolog of Pumilio and FBF.
    EMBO J. 2001 Feb 1;20(3):552-61 PMID: 11157761
  24. 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
  25. 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
  26. Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution.
    Mol Biol Evol. 2002 Jan;19(1):76-84 PMID: 11752192
  27. Signaling in plant-microbe interactions.
    Science. 1997 May 2;276(5313):726-33 PMID: 9115193
  28. A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion.
    Genome Res. 2000 Jul;10(7):908-15 PMID: 10899140
  29. Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli.
    Nature. 1991 Aug 8;352(6335):544-7 PMID: 1865910
  30. Differential methylation of genes and retrotransposons facilitates shotgun sequencing of the maize genome.
    Nat Genet. 1999 Nov;23(3):305-8 PMID: 10545948
  31. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome.
    Genome Res. 2001 Oct;11(10):1660-76 PMID: 11591643
  32. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana.
    Nature. 1999 Dec 16;402(6763):761-8 PMID: 10617197
  33. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.
    Cell. 1997 Jan 10;88(1):57-63 PMID: 9019406
  34. Identification of individual barley chromosomes based on repetitive sequences: conservative distribution of Afa-family repetitive sequences on the chromosomes of barley and wheat.
    Genes Genet Syst. 1997 Oct;72(5):303-9 PMID: 9511227
  35. Expression analysis of genes induced in barley after chemical activation reveals distinct disease resistance pathways.
    Mol Plant Pathol. 2000 Sep 1;1(5):277-86 PMID: 20572974
  36. Prediction of complete gene structures in human genomic DNA.
    J Mol Biol. 1997 Apr 25;268(1):78-94 PMID: 9149143
  37. A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome.
    Theor Appl Genet. 1993 Jul;86(6):705-12 PMID: 24193780
  38. Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans.
    Genetics. 1995 Sep;141(1):159-79 PMID: 8536965
  39. Resistance gene complexes: evolution and utilization.
    Annu Rev Phytopathol. 2001;39:285-312 PMID: 11701867
  40. Gene silencing and DNA methylation processes.
    Curr Opin Plant Biol. 2001 Apr;4(2):123-9 PMID: 11228434
  41. Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants.
    Plant Cell. 1994 Jun;6(6):907-16 PMID: 8061524
  42. Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):1082-7 PMID: 11792865
  43. Expression of a maize proteinase inhibitor gene is induced in response to wounding and fungal infection: systemic wound-response of a monocot gene.
    Plant J. 1994 Aug;6(2):141-50 PMID: 7920708
  44. GeneMark.hmm: new solutions for gene finding.
    Nucleic Acids Res. 1998 Feb 15;26(4):1107-15 PMID: 9461475
  45. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex.
    Mol Cell. 1999 Jul;4(1):21-33 PMID: 10445024
  46. A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans.
    Cell. 1999 Nov 12;99(4):355-66 PMID: 10571178
  47. 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
  48. Limits to the role of palindromy in deletion formation.
    J Bacteriol. 1991 Jan;173(1):315-8 PMID: 1846137
  49. CEREAL CHROMOSOME STRUCTURE, EVOLUTION, AND PAIRING.
    Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:195-222 PMID: 15012191
  50. Nested retrotransposons in the intergenic regions of the maize genome.
    Science. 1996 Nov 1;274(5288):765-8 PMID: 8864112
  51. Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes.
    Nat Genet. 2002 Feb;30(2):194-200 PMID: 11799393
  52. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance.
    Science. 2002 Mar 15;295(5562):2073-6 PMID: 11847307
  53. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL.
    Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10274-9 PMID: 8816790
  54. Mutator transposase is widespread in the grasses.
    Plant Physiol. 2001 Mar;125(3):1293-303 PMID: 11244110
  55. Microsatellite variation and evolution in the Mimulus guttatus species complex with contrasting mating systems.
    Mol Biol Evol. 1997 Oct;14(10):1023-34 PMID: 9335142
  56. High gene density is conserved at syntenic loci of small and large grass genomes.
    Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):8265-70 PMID: 10393983
  57. Advances in the molecular genetic analysis of the flax-flax rust interaction.
    Annu Rev Phytopathol. 1997;35:271-91 PMID: 15012524
  58. Miropeats: graphical DNA sequence comparisons.
    Comput Appl Biosci. 1995 Dec;11(6):615-9 PMID: 8808577
  59. Base-calling of automated sequencer traces using phred. I. Accuracy assessment.
    Genome Res. 1998 Mar;8(3):175-85 PMID: 9521921
  60. Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome.
    Genome Res. 2002 Mar;12(3):400-7 PMID: 11875027
  61. Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests.
    J Insect Physiol. 1997 Sep;43(9):833-842 PMID: 12770495
  62. Plant disease-resistance proteins and the gene-for-gene concept.
    Trends Biochem Sci. 1998 Dec;23(12):454-6 PMID: 9868361
  63. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2002-08-00
Pages
1903-17
Language
English
Region
England
NLM ID
9208688
PMCID
PMC151473
Subset
IM
Databases
GENBANK
AF427791
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]