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PMID: 24023067 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Arabidopsis semidwarfs evolved from independent mutations in GA20ox1, ortholog to green revolution dwarf alleles in rice and barley.

Barboza L, Effgen S, Alonso-Blanco C, Kooke R, Keurentjes JJ, Koornneef M, Alcázar R

Abstract

Understanding the genetic bases of natural variation for developmental and stress-related traits is a major goal of current plant biology. Variation in plant hormone levels and signaling might underlie such phenotypic variation occurring even within the same species. Here we report the genetic and molecular basis of semidwarf individuals found in natural Arabidopsis thaliana populations. Allelism tests demonstrate that independent loss-of-function mutations at GA locus 5 (GA5), which encodes gibberellin 20-oxidase 1 (GA20ox1) involved in the last steps of gibberellin biosynthesis, are found in different populations from southern, western, and northern Europe; central Asia; and Japan. Sequencing of GA5 identified 21 different loss-of-function alleles causing semidwarfness without any obvious general tradeoff affecting plant performance traits. GA5 shows signatures of purifying selection, whereas GA5 loss-of-function alleles can also exhibit patterns of positive selection in specific populations as shown by Fay and Wu's H statistics. These results suggest that antagonistic pleiotropy might underlie the occurrence of GA5 loss-of-function mutations in nature. Furthermore, because GA5 is the ortholog of rice SD1 and barley Sdw1/Denso green revolution genes, this study illustrates the occurrence of conserved adaptive evolution between wild A.thaliana and domesticated plants.

Keywords
Arabidopsis natural variation dwarf accessions gibberellin mutants
MeSH Terms
Alleles Arabidopsis/anatomy & histology,genetics Arabidopsis Proteins/genetics,metabolism Biological Evolution Genetic Loci/genetics Genome-Wide Association Study Genotype Geography Hordeum/genetics Mixed Function Oxygenases/genetics,metabolism Molecular Sequence Data Mutation/genetics Oryza/genetics Phylogeny Population Dynamics Sequence Homology, Amino Acid
Chemicals
Arabidopsis Proteins Mixed Function Oxygenases gibberellin 3beta-hydroxylase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Barboza Luis
Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.
Effgen Sigi
Alonso-Blanco Carlos
Kooke Rik
Keurentjes Joost J B
Koornneef Maarten
Alcázar Rubén
References (36)
36 references, click to expand
  1. Natural variation in GA1 associates with floral morphology in Arabidopsis thaliana.
    New Phytol. 2012 Jul;195(1):58-70 PMID: 22510148
  2. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.
    Mol Ecol. 2005 Jul;14(8):2611-20 PMID: 15969739
  3. The genes of the Green Revolution.
    Trends Genet. 2003 Jan;19(1):5-9 PMID: 12493241
  4. The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle.
    Plant J. 2008 Feb;53(3):488-504 PMID: 18069939
  5. GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley.
    Funct Integr Genomics. 2009 May;9(2):255-62 PMID: 19280236
  6. Variance component model to account for sample structure in genome-wide association studies.
    Nat Genet. 2010 Apr;42(4):348-54 PMID: 20208533
  7. Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh.
    Theor Appl Genet. 1980 Nov;58(6):257-63 PMID: 24301503
  8. Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions.
    Nat Genet. 2010 Dec;42(12):1135-9 PMID: 21037570
  9. The scale of population structure in Arabidopsis thaliana.
    PLoS Genet. 2010 Feb 12;6(2):e1000843 PMID: 20169178
  10. Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis.
    Plant Physiol. 2005 Nov;139(3):1304-12 PMID: 16244146
  11. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  12. Adaptation and extinction in experimentally fragmented landscapes.
    Proc Natl Acad Sci U S A. 2010 Nov 2;107(44):19120-5 PMID: 20956303
  13. Whole-genome sequencing of multiple Arabidopsis thaliana populations.
    Nat Genet. 2011 Aug 28;43(10):956-63 PMID: 21874002
  14. A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism.
    Genetics. 2005 Mar;169(3):1601-15 PMID: 15654111
  15. Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian peninsula.
    Genetics. 2008 Oct;180(2):1009-21 PMID: 18716334
  16. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.
    Bioinformatics. 2009 Jun 1;25(11):1451-2 PMID: 19346325
  17. Green revolution: a mutant gibberellin-synthesis gene in rice.
    Nature. 2002 Apr 18;416(6882):701-2 PMID: 11961544
  18. The GA5 locus of Arabidopsis thaliana encodes a multifunctional gibberellin 20-oxidase: molecular cloning and functional expression.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6640-4 PMID: 7604047
  19. Analysis of the developmental roles of the Arabidopsis gibberellin 20-oxidases demonstrates that GA20ox1, -2, and -3 are the dominant paralogs.
    Plant Cell. 2012 Mar;24(3):941-60 PMID: 22427334
  20. Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21199-204 PMID: 21078970
  21. Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis.
    Plant Physiol. 2011 Dec;157(4):1942-55 PMID: 21988878
  22. A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase.
    Plant Mol Biol. 2004 Mar;54(4):533-47 PMID: 15316288
  23. Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development.
    Plant J. 2006 Mar;45(5):804-18 PMID: 16460513
  24. Evolutionary rate patterns of the Gibberellin pathway genes.
    BMC Evol Biol. 2009 Aug 18;9:206 PMID: 19689796
  25. The Loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation.
    Evolution. 2013 May;67(5):1235-50 PMID: 23617905
  26. Genetic trade-offs and conditional neutrality contribute to local adaptation.
    Mol Ecol. 2013 Feb;22(3):699-708 PMID: 22420446
  27. Plant Biology. Hormones and the green revolution.
    Science. 2003 Oct 3;302(5642):71-2 PMID: 14526071
  28. Expression level of a gibberellin 20-oxidase gene is associated with multiple agronomic and quality traits in barley.
    Theor Appl Genet. 2011 May;122(8):1451-60 PMID: 21318371
  29. Semidwarf (sd-1), "green revolution" rice, contains a defective gibberellin 20-oxidase gene.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):9043-8 PMID: 12077303
  30. New Arabidopsis recombinant inbred line populations genotyped using SNPWave and their use for mapping flowering-time quantitative trait loci.
    Genetics. 2006 Mar;172(3):1867-76 PMID: 16361234
  31. Gibberellin biosynthesis and its regulation.
    Biochem J. 2012 May 15;444(1):11-25 PMID: 22533671
  32. Extremely low genetic variability and highly structured local populations of Arabidopsis thaliana at higher latitudes.
    Mol Ecol. 2010 Nov;19(21):4753-64 PMID: 20887360
  33. Inference of population structure using multilocus genotype data.
    Genetics. 2000 Jun;155(2):945-59 PMID: 10835412
  34. Gibberellin metabolism and its regulation.
    Annu Rev Plant Biol. 2008;59:225-51 PMID: 18173378
  35. Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana.
    Structure. 2002 Jan;10(1):93-103 PMID: 11796114
  36. TCS: a computer program to estimate gene genealogies.
    Mol Ecol. 2000 Oct;9(10):1657-9 PMID: 11050560
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2013-09-24
Epub
2013-00-10
Pages
15818-23
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3785751
Subset
IM
Databases
GENBANK
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