Home LiteratureArticle Details
PMID: 15171794 Published · epublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana.

BMC plant biology ·Vol. 4 ·2004-06-01 ·Pages 10

Cannon SB, Mitra A, Baumgarten A, Young ND, May G

Abstract

Most genes in Arabidopsis thaliana are members of gene families. How do the members of gene families arise, and how are gene family copy numbers maintained? Some gene families may evolve primarily through tandem duplication and high rates of birth and death in clusters, and others through infrequent polyploidy or large-scale segmental duplications and subsequent losses. Our approach to understanding the mechanisms of gene family evolution was to construct phylogenies for 50 large gene families in Arabidopsis thaliana, identify large internal segmental duplications in Arabidopsis, map gene duplications onto the segmental duplications, and use this information to identify which nodes in each phylogeny arose due to segmental or tandem duplication. Examples of six gene families exemplifying characteristic modes are described. Distributions of gene family sizes and patterns of duplication by genomic distance are also described in order to characterize patterns of local duplication and copy number for large gene families. Both gene family size and duplication by distance closely follow power-law distributions. Combining information about genomic segmental duplications, gene family phylogenies, and gene positions provides a method to evaluate contributions of tandem duplication and segmental genome duplication in the generation and maintenance of gene families. These differences appear to correspond meaningfully to differences in functional roles of the members of the gene families.

MeSH Terms
Arabidopsis/genetics Arabidopsis Proteins/genetics Cysteine Endopeptidases/genetics Databases, Protein Evolution, Molecular Gene Duplication Genome, Plant Immunity, Innate/genetics Light-Harvesting Protein Complexes/genetics Multienzyme Complexes/genetics Multigene Family/genetics Phylogeny Proteasome Endopeptidase Complex Sequence Alignment/methods Tandem Repeat Sequences/genetics
Chemicals
Arabidopsis Proteins Light-Harvesting Protein Complexes Multienzyme Complexes Cysteine Endopeptidases Proteasome Endopeptidase Complex
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Cannon Steven B
Plant Biology Department, University of Minnesota, St, Paul, MN 55108, USA. [email protected]
Mitra Arvind
Baumgarten Andrew
Young Nevin D
May Georgiana
References (72)
72 references, click to expand
  1. OrthoParaMap: distinguishing orthologs from paralogs by integrating comparative genome data and gene phylogenies.
    BMC Bioinformatics. 2003 Sep 2;4:35 PMID: 12952558
  2. 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
  3. Transient expression of members of the germin-like gene family in epidermal cells of wheat confers disease resistance.
    Plant J. 1999 Dec;20(5):541-52 PMID: 10652126
  4. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses.
    Planta. 2001 Sep;213(5):794-801 PMID: 11678285
  5. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins.
    Trends Plant Sci. 2003 Mar;8(3):135-42 PMID: 12663224
  6. The frequency distribution of gene family sizes in complete genomes.
    Mol Biol Evol. 1998 May;15(5):583-9 PMID: 9580988
  7. 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
  8. Putting knowledge of plant disease resistance genes to work.
    Curr Opin Plant Biol. 2001 Aug;4(4):281-7 PMID: 11418336
  9. Cytochrome P450s as genes for crop improvement.
    Curr Opin Plant Biol. 2001 Apr;4(2):162-7 PMID: 11228441
  10. Making inroads into plant receptor kinase signalling pathways.
    Trends Plant Sci. 2003 May;8(5):231-7 PMID: 12758041
  11. The hidden duplication past of Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13627-32 PMID: 12374856
  12. The crystal structure of the antifungal protein zeamatin, a member of the thaumatin-like, PR-5 protein family.
    Nat Struct Biol. 1996 Jan;3(1):19-23 PMID: 8548448
  13. Analysis of intrachromosomal duplications in yeast Saccharomyces cerevisiae: a possible model for their origin.
    Mol Biol Evol. 2000 Aug;17(8):1268-75 PMID: 10908647
  14. DiagHunter and GenoPix2D: programs for genomic comparisons, large-scale homology discovery and visualization.
    Genome Biol. 2003;4(10):R68 PMID: 14519203
  15. COFFEE: an objective function for multiple sequence alignments.
    Bioinformatics. 1998 Jun;14(5):407-22 PMID: 9682054
  16. The automatic detection of homologous regions (ADHoRe) and its application to microcolinearity between Arabidopsis and rice.
    Genome Res. 2002 Nov;12(11):1792-801 PMID: 12421767
  17. Non-random association of transposable elements with duplicated genomic blocks in Arabidopsis thaliana.
    Mol Phylogenet Evol. 2003 Dec;29(3):410-6 PMID: 14615183
  18. Genome-level evolution of resistance genes in Arabidopsis thaliana.
    Genetics. 2003 Sep;165(1):309-19 PMID: 14504238
  19. Structural divergence of chromosomal segments that arose from successive duplication events in the Arabidopsis genome.
    Nucleic Acids Res. 2003 Feb 15;31(4):1339-50 PMID: 12582254
  20. A hitchhiker's guide to the proteasome.
    Sci STKE. 2001 Aug 28;2001(97):pe2 PMID: 11698580
  21. Origin and early evolution of photosynthesis.
    Photosynth Res. 1992;33:91-111 PMID: 11538390
  22. Orthologs, paralogs and genome comparisons.
    Curr Opin Genet Dev. 1999 Dec;9(6):630-6 PMID: 10607614
  23. Tandem mass spectrometric identification of spinach Photosystem II light-harvesting components.
    Photosynth Res. 2002;72(2):159-73 PMID: 16228515
  24. A draft sequence of the rice genome (Oryza sativa L. ssp. indica).
    Science. 2002 Apr 5;296(5565):79-92 PMID: 11935017
  25. Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness.
    Plant J. 2003 Aug;35(3):350-61 PMID: 12887586
  26. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome.
    Genome Res. 2003 Feb;13(2):137-44 PMID: 12566392
  27. Interaction between Arabidopsis heat shock transcription factor 1 and 70 kDa heat shock proteins.
    J Exp Bot. 2002 Feb;53(367):371-5 PMID: 11807141
  28. Ocatin. A novel tuber storage protein from the andean tuber crop oca with antibacterial and antifungal activities.
    Plant Physiol. 2002 Apr;128(4):1291-302 PMID: 11950978
  29. The mitochondrial carrier family of transport proteins: structural, functional, and evolutionary relationships.
    Crit Rev Biochem Mol Biol. 1993;28(3):209-33 PMID: 8325039
  30. Sequence analysis of two new members of the major latex protein gene family supports the triploid-hybrid origin of the opium poppy.
    Gene. 1994 Feb 25;139(2):207-9 PMID: 8112605
  31. The evolutionary demography of duplicate genes.
    J Struct Funct Genomics. 2003;3(1-4):35-44 PMID: 12836683
  32. Organization of the major latex protein gene family in opium poppy.
    Plant Mol Biol. 1992 Nov;20(4):749-52 PMID: 1450390
  33. The Saccharomyces cerevisiae ubiquitin-proteasome system.
    Philos Trans R Soc Lond B Biol Sci. 1999 Sep 29;354(1389):1513-22 PMID: 10582237
  34. Molecular organization of the 20S proteasome gene family from Arabidopsis thaliana.
    Genetics. 1998 Jun;149(2):677-92 PMID: 9611183
  35. The 20S proteasome gene family in Arabidopsis thaliana.
    FEBS Lett. 1997 Oct 27;416(3):281-5 PMID: 9373170
  36. A novel gene family in moss (Physcomitrella patens) shows sequence homology and a phylogenetic relationship with the TIR-NBS class of plant disease resistance genes.
    J Mol Evol. 2002 Nov;55(5):595-605 PMID: 12399933
  37. MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource based on the first complete plant genome.
    Nucleic Acids Res. 2002 Jan 1;30(1):91-3 PMID: 11752263
  38. The origins of genomic duplications in Arabidopsis.
    Science. 2000 Dec 15;290(5499):2114-7 PMID: 11118139
  39. The protein information resource (PIR).
    Nucleic Acids Res. 2000 Jan 1;28(1):41-4 PMID: 10592177
  40. Mitochondrial uncoupling proteins in mammals and plants.
    Biosci Rep. 2001 Apr;21(2):201-12 PMID: 11725869
  41. The promoter of a basic PR1-like gene, AtPRB1, from Arabidopsis establishes an organ-specific expression pattern and responsiveness to ethylene and methyl jasmonate.
    Plant Mol Biol. 2001 Nov;47(5):641-52 PMID: 11725949
  42. A novel promoter from soybean that is active in a complex developmental pattern with and without its proximal 650 base pairs.
    Plant Mol Biol. 1999 Sep;41(2):217-31 PMID: 10579489
  43. Solute carriers involved in energy transfer of mitochondria form a homologous protein family.
    FEBS Lett. 1987 Feb 9;212(1):1-9 PMID: 3026849
  44. The Bioperl toolkit: Perl modules for the life sciences.
    Genome Res. 2002 Oct;12(10):1611-8 PMID: 12368254
  45. The early stages of duplicate gene evolution.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15682-7 PMID: 14671323
  46. Arabidopsis thaliana germin-like proteins: common and specific features point to a variety of functions.
    Planta. 2000 Aug;211(3):345-54 PMID: 10987552
  47. Multigene families and the evolution of complexity.
    J Mol Evol. 1991 Jul;33(1):34-41 PMID: 1909373
  48. Sequential and structural homology between intracellular pathogenesis-related proteins and a group of latex proteins.
    Plant Mol Biol. 1998 Dec;38(6):1243-6 PMID: 9869429
  49. Germins and germin like proteins: an overview.
    Indian J Exp Biol. 2001 Mar;39(3):191-200 PMID: 11495276
  50. The evolutionary fate and consequences of duplicate genes.
    Science. 2000 Nov 10;290(5494):1151-5 PMID: 11073452
  51. ATV: display and manipulation of annotated phylogenetic trees.
    Bioinformatics. 2001 Apr;17(4):383-4 PMID: 11301314
  52. Function of the ubiquitin-proteasome pathway in auxin response.
    Trends Biochem Sci. 2000 Mar;25(3):133-8 PMID: 10694884
  53. Plants lacking the main light-harvesting complex retain photosystem II macro-organization.
    Nature. 2003 Feb 6;421(6923):648-52 PMID: 12571599
  54. Primary structures of two ribonucleases from ginseng calluses. New members of the PR-10 family of intracellular pathogenesis-related plant proteins.
    FEBS Lett. 1997 Apr 28;407(2):207-10 PMID: 9166900
  55. Patterns of nucleotide substitution among simultaneously duplicated gene pairs in Arabidopsis thaliana.
    Mol Biol Evol. 2002 Sep;19(9):1464-73 PMID: 12200474
  56. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  57. Structural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26S proteasome.
    Plant J. 1999 Jun;18(5):529-39 PMID: 10417703
  58. The major birch pollen allergen, Bet v 1, shows ribonuclease activity.
    Planta. 1996;199(3):413-5 PMID: 8771801
  59. Extensive duplication and reshuffling in the Arabidopsis genome.
    Plant Cell. 2000 Jul;12(7):1093-101 PMID: 10899976
  60. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis.
    Plant Cell. 2003 Apr;15(4):809-34 PMID: 12671079
  61. Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies.
    J Mol Evol. 2002 Apr;54(4):548-62 PMID: 11956693
  62. The Pfam protein families database.
    Nucleic Acids Res. 2002 Jan 1;30(1):276-80 PMID: 11752314
  63. The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes.
    Biochemistry. 2003 Jan 28;42(3):608-13 PMID: 12534272
  64. Gene families: the taxonomy of protein paralogs and chimeras.
    Science. 1997 Oct 24;278(5338):609-14 PMID: 9381171
  65. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing.
    Bioinformatics. 2002 Mar;18(3):502-4 PMID: 11934758
  66. Protein Information Resource: a community resource for expert annotation of protein data.
    Nucleic Acids Res. 2001 Jan 1;29(1):29-32 PMID: 11125041
  67. The age of the Arabidopsis thaliana genome duplication.
    Plant Mol Biol. 2003 Apr;51(6):859-66 PMID: 12777046
  68. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10763-8 PMID: 11526204
  69. Arabidopsis thaliana contains a large family of germin-like proteins: characterization of cDNA and genomic sequences encoding 12 unique family members.
    Plant Mol Biol. 1998 Dec;38(6):929-43 PMID: 9869400
  70. Model of amino acid substitution in proteins encoded by mitochondrial DNA.
    J Mol Evol. 1996 Apr;42(4):459-68 PMID: 8642615
  71. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events.
    Nature. 2003 Mar 27;422(6930):433-8 PMID: 12660784
  72. 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
BMC plant biology
Abbr.
BMC Plant Biol
ISSN
1471-2229
Published
2004-06-01
Epub
2004-00-01
Pages
10
Language
English
Region
England
NLM ID
100967807
PMCID
PMC446195
Subset
IM
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]