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PMID: 30520727 Published · epublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Drought adaptation in Arabidopsis thaliana by extensive genetic loss-of-function.

eLife ·Vol. 7 ·2018-00-06

Monroe JG, Powell T, Price N, Mullen JL, Howard A, Evans K, Lovell JT, McKay JK

Abstract

Interdisciplinary syntheses are needed to scale up discovery of the environmental drivers and molecular basis of adaptation in nature. Here we integrated novel approaches using whole genome sequences, satellite remote sensing, and transgenic experiments to study natural loss-of-function alleles associated with drought histories in wild Arabidopsis thaliana. The genes we identified exhibit population genetic signatures of parallel molecular evolution, selection for loss-of-function, and shared associations with flowering time phenotypes in directions consistent with longstanding adaptive hypotheses seven times more often than expected by chance. We then confirmed predicted phenotypes experimentally in transgenic knockout lines. These findings reveal the importance of drought timing to explain the evolution of alternative drought tolerance strategies and further challenge popular assumptions about the adaptive value of genetic loss-of-function in nature. These results also motivate improved species-wide sequencing efforts to better identify loss-of-function variants and inspire new opportunities for engineering climate resilience in crops.

Keywords
A. thaliana climate adaptation drought tolerance evolutionary biology functional genomics gene editing genetics genomics molecular evolution remote sensing
MeSH Terms
Adaptation, Physiological/genetics Arabidopsis/genetics Droughts Flowers/genetics Gene Expression Profiling Loss of Function Mutation Phenotype Plants, Genetically Modified Stress, Physiological Time Factors
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Monroe J Grey ORCID
Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States. | Graduate Degree Program in Ecology, Colorado State University, Fort Collins, United States.
Powell Tyler
Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States. | Department of Biology, Colorado State University, Fort Collins, United States.
Price Nicholas ORCID
Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States.
Mullen Jack L
Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States.
Howard Anne
Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States.
Evans Kyle ORCID
Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States.
Lovell John T ORCID
HudsonAlpha Institute for Biotechnology, Huntsville, United States.
McKay John K
Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, United States. | Graduate Degree Program in Ecology, Colorado State University, Fort Collins, United States.
Conflict of Interest

JM, TP, NP, JM, AH, KE, JL, JM No competing interests declared

References (75)
75 references, click to expand
  1. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis.
    Nature. 1999 Aug 12;400(6745):667-71 PMID: 10458161
  2. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time.
    Science. 2000 Oct 13;290(5490):344-7 PMID: 11030654
  3. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis.
    Plant Cell. 2001 Mar;13(3):681-93 PMID: 11251105
  4. Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1.
    Mol Biol Evol. 2001 Sep;18(9):1754-63 PMID: 11504855
  5. 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
  6. DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time.
    Mol Biol Evol. 2002 Aug;19(8):1261-71 PMID: 12140238
  7. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana.
    Genetics. 2003 Feb;163(2):735-46 PMID: 12618410
  8. Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits.
    Mol Ecol. 2003 May;12(5):1137-51 PMID: 12694278
  9. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana.
    Nature. 2003 May 1;423(6935):74-7 PMID: 12721627
  10. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  11. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14587-92 PMID: 14506289
  12. Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root.
    Genes Dev. 2004 Mar 15;18(6):700-14 PMID: 15031265
  13. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA.
    Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4712-7 PMID: 15070783
  14. Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation.
    Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2460-5 PMID: 15695584
  15. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis.
    Plant Physiol. 2005 Jun;138(2):1163-73 PMID: 15908596
  16. 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
  17. A single amino acid mutation contributes to adaptive beach mouse color pattern.
    Science. 2006 Jul 7;313(5783):101-4 PMID: 16825572
  18. Principal components analysis corrects for stratification in genome-wide association studies.
    Nat Genet. 2006 Aug;38(8):904-9 PMID: 16862161
  19. Soft sweeps III: the signature of positive selection from recurrent mutation.
    PLoS Genet. 2006 Dec 15;2(12):e186 PMID: 17173482
  20. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation.
    Proc Natl Acad Sci U S A. 2007 Jan 23;104(4):1278-82 PMID: 17220273
  21. Roles of Arabidopsis cyclin-dependent kinase C complexes in cauliflower mosaic virus infection, plant growth, and development.
    Plant Cell. 2007 Apr;19(4):1388-402 PMID: 17468259
  22. The locus of evolution: evo devo and the genetics of adaptation.
    Evolution. 2007 May;61(5):995-1016 PMID: 17492956
  23. Mechanistic approaches to the study of evolution: the functional synthesis.
    Nat Rev Genet. 2007 Sep;8(9):675-88 PMID: 17703238
  24. Intraspecific competition reveals conditional fitness effects of single gene polymorphism at the Arabidopsis root growth regulator BRX.
    New Phytol. 2008;180(1):71-80 PMID: 18627499
  25. Relaxed selection on the CBF/DREB1 regulatory genes and reduced freezing tolerance in the southern range of Arabidopsis thaliana.
    Mol Biol Evol. 2008 Dec;25(12):2547-55 PMID: 18775899
  26. 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
  27. Population genomics of the Arabidopsis thaliana flowering time gene network.
    Mol Biol Evol. 2009 Nov;26(11):2475-86 PMID: 19625391
  28. Linking genotype to phenotype using the Arabidopsis unimutant collection.
    Plant J. 2010 Mar;61(6):928-40 PMID: 20409268
  29. Parallel adaptation: one or many waves of advance of an advantageous allele?
    Genetics. 2010 Oct;186(2):647-68 PMID: 20660645
  30. Multiple reference genomes and transcriptomes for Arabidopsis thaliana.
    Nature. 2011 Aug 28;477(7365):419-23 PMID: 21874022
  31. Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario.
    J Exp Bot. 2012 Jan;63(1):25-31 PMID: 21963615
  32. 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
  33. Phytozome: a comparative platform for green plant genomics.
    Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86 PMID: 22110026
  34. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools.
    Nucleic Acids Res. 2012 Jan;40(Database issue):D1202-10 PMID: 22140109
  35. A systematic survey of loss-of-function variants in human protein-coding genes.
    Science. 2012 Feb 17;335(6070):823-8 PMID: 22344438
  36. Natural variation in GL1 and its effects on trichome density in Arabidopsis thaliana.
    Mol Ecol. 2012 Jul;21(14):3501-15 PMID: 22625421
  37. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3.
    Fly (Austin). 2012 Apr-Jun;6(2):80-92 PMID: 22728672
  38. Natural Arabidopsis brx loss-of-function alleles confer root adaptation to acidic soil.
    Curr Biol. 2012 Oct 23;22(20):1962-8 PMID: 23041192
  39. GWASTools: an R/Bioconductor package for quality control and analysis of genome-wide association studies.
    Bioinformatics. 2012 Dec 15;28(24):3329-31 PMID: 23052040
  40. Parallel Loss-of-Function at the RPM1 Bacterial Resistance Locus in Arabidopsis thaliana.
    Front Plant Sci. 2012 Dec 26;3:287 PMID: 23272006
  41. MAFFT multiple sequence alignment software version 7: improvements in performance and usability.
    Mol Biol Evol. 2013 Apr;30(4):772-80 PMID: 23329690
  42. A bountiful harvest: genomic insights into crop domestication phenotypes.
    Annu Rev Plant Biol. 2013;64:47-70 PMID: 23451788
  43. Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation.
    Proc Biol Sci. 2013 May 22;280(1763):20131043 PMID: 23698015
  44. Natural variation of C-repeat-binding factor (CBFs) genes is a major cause of divergence in freezing tolerance among a group of Arabidopsis thaliana populations along the Yangtze River in China.
    New Phytol. 2013 Sep;199(4):1069-80 PMID: 23721132
  45. Arabidopsis semidwarfs evolved from independent mutations in GA20ox1, ortholog to green revolution dwarf alleles in rice and barley.
    Proc Natl Acad Sci U S A. 2013 Sep 24;110(39):15818-23 PMID: 24023067
  46. Genetic architecture of naturally occurring quantitative traits in plants: an updated synthesis.
    Curr Opin Plant Biol. 2014 Apr;18:37-43 PMID: 24565952
  47. Reduced Dormancy5 encodes a protein phosphatase 2C that is required for seed dormancy in Arabidopsis.
    Plant Cell. 2014 Nov;26(11):4362-75 PMID: 25415980
  48. The IBO germination quantitative trait locus encodes a phosphatase 2C-related variant with a nonsynonymous amino acid change that interferes with abscisic acid signaling.
    New Phytol. 2015 Feb;205(3):1076-82 PMID: 25490966
  49. Direct and indirect selection on flowering time, water-use efficiency (WUE, δ (13)C), and WUE plasticity to drought in Arabidopsis thaliana.
    Ecol Evol. 2014 Dec;4(23):4505-21 PMID: 25512847
  50. Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes.
    Am Nat. 2015 Feb;185(2):212-27 PMID: 25616140
  51. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability.
    Nat Rev Genet. 2015 Apr;16(4):237-51 PMID: 25752530
  52. The evolution of drought escape and avoidance in natural herbaceous populations.
    Plant Sci. 2015 May;234:155-62 PMID: 25804818
  53. Natural Variation Identifies ICARUS1, a Universal Gene Required for Cell Proliferation and Growth at High Temperatures in Arabidopsis thaliana.
    PLoS Genet. 2015 May 07;11(5):e1005085 PMID: 25951176
  54. Alleles versus mutations: Understanding the evolution of genetic architecture requires a molecular perspective on allelic origins.
    Evolution. 2015 Dec;69(12):3025-38 PMID: 26374707
  55. When natural selection gives gene function the cold shoulder.
    Bioessays. 2015 Nov;37(11):1169-73 PMID: 26411745
  56. Population Genomics for Understanding Adaptation in Wild Plant Species.
    Annu Rev Genet. 2015;49:315-38 PMID: 26436459
  57. Convergent Evolution During Local Adaptation to Patchy Landscapes.
    PLoS Genet. 2015 Nov 16;11(11):e1005630 PMID: 26571125
  58. The effect of timing of growing season drought on flowering of a dominant C4 grass.
    Oecologia. 2016 Jun;181(2):391-9 PMID: 26886131
  59. Evolution by gene loss.
    Nat Rev Genet. 2016 Jul;17(7):379-91 PMID: 27087500
  60. Molecular mechanisms of adaptation and speciation: why do we need an integrative approach?
    Mol Ecol. 2017 Jan;26(1):277-290 PMID: 27230590
  61. Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana.
    Mol Ecol. 2016 Aug;25(15):3632-44 PMID: 27247130
  62. Sequence Polymorphisms at the REDUCED DORMANCY5 Pseudophosphatase Underlie Natural Variation in Arabidopsis Dormancy.
    Plant Physiol. 2016 Aug;171(4):2659-70 PMID: 27288362
  63. 1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana.
    Cell. 2016 Jul 14;166(2):481-491 PMID: 27293186
  64. Genetics of water use physiology in locally adapted Arabidopsis thaliana.
    Plant Sci. 2016 Oct;251:12-22 PMID: 27593459
  65. Multiple alleles at a single locus control seed dormancy in Swedish Arabidopsis.
    Elife. 2016 Dec 14;5: PMID: 27966430
  66. The genomic basis of adaptation in plants.
    Curr Opin Plant Biol. 2017 Apr;36:88-94 PMID: 28242535
  67. Fitness effects of mutation: testing genetic redundancy in Arabidopsis thaliana.
    J Evol Biol. 2017 Jun;30(6):1124-1135 PMID: 28387971
  68. Genome-Wide Identification and Expression Analysis of NRAMP Family Genes in Soybean (Glycine Max L.).
    Front Plant Sci. 2017 Aug 18;8:1436 PMID: 28868061
  69. Recent natural selection causes adaptive evolution of an avian polygenic trait.
    Science. 2017 Oct 20;358(6361):365-368 PMID: 29051380
  70. Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana.
    Mol Ecol. 2018 Oct;27(20):4052-4065 PMID: 30118161
  71. Identification of candidate domestication-related genes with a systematic survey of loss-of-function mutations.
    Plant J. 2018 Dec;96(6):1218-1227 PMID: 30246271
  72. Natural selection and the concept of a protein space.
    Nature. 1970 Feb 7;225(5232):563-4 PMID: 5411867
  73. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing.
    Plant Cell. 1997 Aug;9(8):1317-26 PMID: 9286109
  74. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15843-8 PMID: 9861058
  75. When less is more: gene loss as an engine of evolutionary change.
    Am J Hum Genet. 1999 Jan;64(1):18-23 PMID: 9915938
Article Info
Journal
eLife
Abbr.
Elife
ISSN
2050-084X
Published
2018-00-06
Epub
2018-00-06
Language
English
Region
England
NLM ID
101579614
PMCID
PMC6326724
Subset
IM
Analysis Services
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