Home LiteratureArticle Details
PMID: 12468738 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Structural analysis of the maize rp1 complex reveals numerous sites and unexpected mechanisms of local rearrangement.

The Plant cell ·Vol. 14 ·No. 12 ·2002-12-00 ·Pages 3213-23

Ramakrishna W, Emberton J, Ogden M, SanMiguel P, Bennetzen JL

Abstract

Rp1 is a complex disease resistance locus in maize that is exceptional in both allelic variability and meiotic instability. Genomic sequence analysis of three maize BACs from the Rp1 region of the B73 inbred line revealed 4 Rp1 homologs and 18 other gene-homologous sequences, of which at least 16 are truncated. Thirteen of the truncated genes are found in three clusters, suggesting that they arose from multiple illegitimate break repairs at the same sites or from complex repairs of each of these sites with multiple unlinked DNA templates. A 43-kb region that contains an Rp1 homolog, six truncated genes, and three Opie retrotransposons was found to be duplicated in this region. This duplication is relatively recent, occurring after the insertion of the three Opie elements. The breakpoints of the duplication are outside of any genes or identified repeat sequence, suggesting a duplication mechanism that did not involve unequal recombination. A physical map and partial sequencing of the Rp1 complex indicate the presence of 15 Rp1 homologs in regions of approximately 250 and 300 kb in the B73 inbred line. Comparison of fully sequenced Rp1-homologous sequences in the region demonstrates a history of unequal recombination and diversifying selection within the Leu-rich repeat 2 region, resulting in chimeric gene structures.

MeSH Terms
Chromosome Mapping Chromosomes, Artificial, Bacterial/genetics DNA, Plant/chemistry,genetics Gene Duplication Genes, Plant/genetics Immunity, Innate/genetics Leucine-Rich Repeat Proteins Molecular Sequence Data Mutagenesis, Insertional Plant Proteins/genetics,metabolism Proteins/genetics Recombination, Genetic Retroelements/genetics Sequence Analysis, DNA Zea mays/genetics,physiology
Chemicals
DNA, Plant Leucine-Rich Repeat Proteins Plant Proteins Proteins Retroelements ZmCip1 protein, Zea mays
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Ramakrishna Wusirika
Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907, USA.
Emberton John
Ogden Matthew
SanMiguel Phillip
Bennetzen Jeffrey L
References (60)
60 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. Comparative sequence analysis of plant nuclear genomes:m microcolinearity and its many exceptions.
    Plant Cell. 2000 Jul;12(7):1021-9 PMID: 10899971
  3. Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat.
    Genetics. 1996 Dec;144(4):1883-91 PMID: 8978071
  4. Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize.
    Genetics. 1993 Jan;133(1):119-25 PMID: 8417982
  5. Origination of Ds elements from Ac elements in maize: evidence for rare repair synthesis at the site of Ac excision.
    Genetics. 1999 Aug;152(4):1733-40 PMID: 10430597
  6. 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
  7. A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death.
    Plant Cell. 1994 Nov;6(11):1543-52 PMID: 7827490
  8. Complex duplications in maize lines.
    Mol Gen Genet. 1993 May;239(1-2):115-21 PMID: 8099709
  9. The generation of plant disease resistance gene specificities.
    Trends Plant Sci. 2000 Sep;5(9):373-9 PMID: 10973092
  10. Contrasting modes of evolution acting on the complex N locus for rust resistance in flax.
    Plant J. 2001 Sep;27(5):439-53 PMID: 11576428
  11. The paleontology of intergene retrotransposons of maize.
    Nat Genet. 1998 Sep;20(1):43-5 PMID: 9731528
  12. Retrotransposon reverse-transcriptase-mediated repair of chromosomal breaks.
    Nature. 1996 Oct 17;383(6601):641-4 PMID: 8857543
  13. Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses.
    Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1411-5 PMID: 8108422
  14. The arms race is ancient history in Arabidopsis, the wildflower.
    Nat Rev Genet. 2001 Jul;2(7):516-27 PMID: 11433358
  15. New rust resistance specificities associated with recombination in the Rp1 complex in maize.
    Genetics. 1995 Sep;141(1):373-81 PMID: 8536984
  16. The evolution of disease resistance genes.
    Plant Mol Biol. 2000 Jan;42(1):195-204 PMID: 10688137
  17. Recombination between paralogues at the Rp1 rust resistance locus in maize.
    Genetics. 2001 May;158(1):423-38 PMID: 11333250
  18. The major resistance gene cluster in lettuce is highly duplicated and spans several megabases.
    Plant Cell. 1998 Nov;10(11):1817-32 PMID: 9811791
  19. Transposon-mediated chromosomal rearrangements and gene duplications in the formation of the maize R-r complex.
    EMBO J. 1995 May 15;14(10):2350-63 PMID: 7774593
  20. Segmental duplications: an 'expanding' role in genomic instability and disease.
    Nat Rev Genet. 2001 Oct;2(10):791-800 PMID: 11584295
  21. On the structure of a gene for disease resistance in maize.
    Proc Natl Acad Sci U S A. 1968 Dec;61(4):1300-5 PMID: 16591724
  22. Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection.
    Plant Cell. 1998 Nov;10(11):1833-46 PMID: 9811792
  23. Saturation mapping of a gene-rich recombination hot spot region in wheat.
    Genetics. 2000 Feb;154(2):823-35 PMID: 10655233
  24. Common and contrasting themes of plant and animal diseases.
    Science. 2001 Jun 22;292(5525):2285-9 PMID: 11423652
  25. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
  26. SWAN: sliding window analysis of nucleotide sequence variability.
    Bioinformatics. 1998 Jun;14(5):467-8 PMID: 9682061
  27. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato.
    Cell. 1997 Dec 12;91(6):821-32 PMID: 9413991
  28. Signaling in plant-microbe interactions.
    Science. 1997 May 2;276(5313):726-33 PMID: 9115193
  29. Genetics of plant-pathogen interactions specifying plant disease resistance.
    Plant Physiol. 2001 Jan;125(1):73-6 PMID: 11154300
  30. The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8903-8 PMID: 11438686
  31. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  32. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome.
    Genome Res. 2001 Oct;11(10):1660-76 PMID: 11591643
  33. Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa).
    Genetics. 2001 Feb;157(2):831-49 PMID: 11157000
  34. Structure, function and evolution of plant disease resistance genes.
    Curr Opin Plant Biol. 2000 Aug;3(4):278-84 PMID: 10873844
  35. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes.
    Curr Opin Genet Dev. 1995 Dec;5(6):814-21 PMID: 8745082
  36. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes.
    Mol Biol Evol. 1997 Dec;14(12):1335-8 PMID: 9402743
  37. A structural basis of the interactions between leucine-rich repeats and protein ligands.
    Nature. 1995 Mar 9;374(6518):183-6 PMID: 7877692
  38. Recombination at the Rp1 locus of maize.
    Mol Gen Genet. 1991 May;226(3):377-82 PMID: 1674815
  39. Species-specific double-strand break repair and genome evolution in plants.
    EMBO J. 2000 Oct 16;19(20):5562-6 PMID: 11032823
  40. Sequence of three bronze alleles of maize and correlation with the genetic fine structure.
    Genetics. 1988 May;119(1):185-97 PMID: 3396861
  41. Capture of retrotransposon DNA at the sites of chromosomal double-strand breaks.
    Nature. 1996 Oct 17;383(6601):644-6 PMID: 8857544
  42. Plant-pathogen microevolution: molecular basis for the origin of a fungal disease in maize.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1686-91 PMID: 9465077
  43. Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes.
    Plant Physiol. 2001 Mar;125(3):1342-53 PMID: 11244114
  44. Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells.
    EMBO J. 1998 Oct 15;17(20):6086-95 PMID: 9774352
  45. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.
    J Mol Evol. 1980 Dec;16(2):111-20 PMID: 7463489
  46. Insertion preference of maize and rice miniature inverted repeat transposable elements as revealed by the analysis of nested elements.
    Plant Cell. 2001 Nov;13(11):2553-64 PMID: 11701888
  47. Evolution of the rice Xa21 disease resistance gene family.
    Plant Cell. 1997 Aug;9(8):1279-87 PMID: 9286106
  48. Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy.
    Plant Cell. 1998 Jun;10(6):1055-68 PMID: 9634592
  49. MEGA2: molecular evolutionary genetics analysis software.
    Bioinformatics. 2001 Dec;17(12):1244-5 PMID: 11751241
  50. Nested retrotransposons in the intergenic regions of the maize genome.
    Science. 1996 Nov 1;274(5288):765-8 PMID: 8864112
  51. Filler DNA is associated with spontaneous deletions in maize.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8731-5 PMID: 2247441
  52. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants.
    Plant Cell. 1999 Jul;11(7):1365-76 PMID: 10402435
  53. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
    Mol Biol Evol. 1986 Sep;3(5):418-26 PMID: 3444411
  54. Interphase fluorescence in situ hybridization mapping: a physical mapping strategy for plant species with large complex genomes.
    Mol Gen Genet. 1996 Oct 16;252(5):497-502 PMID: 8914510
  55. Advances in the molecular genetic analysis of the flax-flax rust interaction.
    Annu Rev Phytopathol. 1997;35:271-91 PMID: 15012524
  56. Colinearity and its exceptions in orthologous adh regions of maize and sorghum.
    Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7409-14 PMID: 10377428
  57. Organization, instability and evolution of plant disease resistance genes.
    Plant Mol Biol. 1992 Nov;20(4):575-8 PMID: 1450374
  58. 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
  59. Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family.
    Proc Natl Acad Sci U S A. 1999 May 11;96(10):5850-5 PMID: 10318973
  60. 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
DOI
10.1105/tpc.006338
Published
2002-12-00
Pages
3213-23
Language
English
Region
England
NLM ID
9208688
PMCID
PMC151213
Subset
IM
Databases
GENBANK
AF466931, AF466932
External Links
PubMed source DOI: 10.1105/tpc.006338 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: product@genelibs.com

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