Deeply diverged alleles in the arabidopsis AREB1 transcription factor drive genome-wide differences in transcriptional response to the environment

Molecular Biology and Evolution

Volumn 32, Issue 4, 2015, Pages 956-969

  Des Marais, David L ^a   Skillern, Wesley D ^a   Juenger, Thomas E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

abscisic acid; balancing selection; gene expression; gene by environment interaction; signaling network

Indexed keywords

ABSCISIC ACID; AREB1 TRANSCRIPTION FACTOR; MESSENGER RNA; SOIL WATER; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; AREB1 PROTEIN, ARABIDOPSIS; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ALLELE; ARABIDOPSIS THALIANA; ARTICLE; BALANCING SELECTION; CONTROLLED STUDY; DIVERSIFYING SELECTION; EXON; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE LINKAGE DISEQUILIBRIUM; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HAPLOTYPE; INDEL MUTATION; INTRON; NONHUMAN; OSMOTIC STRESS; PLANT GENE; PLANT STRESS; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SOIL WATER CONTENT; TRANSGENIC PLANT; ARABIDOPSIS; DROUGHT; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENE-ENVIRONMENT INTERACTION; HAPLOTYPES; POLYMORPHISM, GENETIC; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84926635585     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu401     Document Type: Article

References (76)

1. Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R.(2007).ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis.Plant Cell 19:1665-1681
2. Aguade M.(2001).Nucleotide sequence variation at two genes of the phenylpropanoid pathway, the FAH1 and F3H Genes, in Arabidopsis thaliana.Mol Biol Evol.18:1-9
3. Ayroles JF, Carbone MA, Stone EA, Jordan KW, Lyman RF, Magwire MM, Rollmann SM, Duncan LH, Lawrence F, Anholt RR, et al.(2009).Systems genetics of complex traits in Drosophila melanogaster.Nat Genet.41:299-307
4. Bakker EG, Toomajian C, Kreitman M, Bergelson J.(2006).A genome-wide survey of R gene polymorphisms in Arabidopsis.Plant Cell 18: 1803-1818
5. Baurle I, Dean C.(2006).The timing of developmental transitions in plants.Cell 125:655-664
6. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES.(2007).TASSEL: software for association mapping of complex traits in diverse samples.Bioinformatics 23:2633-2635
7. Bradshaw AD.(1965).Evolutionary significance of phenotypic plasticity in plants.Adv Genet.13:115-155
8. Caldwell KS, Michelmore RW.(2009).Arabidopsis thaliana genes encoding defense signaling and recognition proteins exhibit contrasting evolutionary dynamics.Genetics 181:671-684
9. Carroll SB. (2008).Evo-devo and An Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution.Cell 134:25-36
10. Charlesworth B, Nordborg M, Charlesworth D.(1997).The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations.Genet Res.70:155-174
11. Charlesworth D.(2006).Balancing selection and its effects on sequences in nearby genome regions.PLoS Genet.2:e64
12. Chaves MM, Maroco JP, Pereira J.(2003).Understanding plant responses to drought-from genes to the whole plant.Funct Plant Biol.30: 239-264
13. Choi H-i, Hong J-h, Ha J-o, Kang J-y, Kim SY.(2000).ABFs, a family of ABAresponsive element binding proteins.J Biol Chem.275:1723-1730
14. Clough SJ, Bent A.(1998).Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Plant J.16:735-743
15. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR.(2010).Abscisic acid: emergence of a core signaling network.Annu Rev Plant Biol.61: 651-679
16. Des Marais DL, Hernandez KH, Juenger TE.(2013).Genotype-by-environment interaction and plasticity: exploring genomic responses of plants to the abiotic environment.Annu Rev Ecol Evol Syst.44:5-29
17. DesMarais DL, McKay JK, Richards JH, Sen S, Wayne T, Juenger TE.(2012).Physiological genomics of response to soil drying in diverse Arabidopsis accessions.Plant Cell 24:893-914
18. Du J, Gu T, Tian H, Araki H, Yang YH, Tian D.(2008).Grouped nucleotide polymorphism: a major contributor to genetic variation in Arabidopsis.Gene 426:1-6
19. Du J, Wang X, Zhang M, Tian D, Yang Y-H.(2007).Unique nucleotide polymorphism of ankyrin gene cluster in Arabidopsis.J Genet.86: 27-35
20. Finkelstein RR, Rock CD. (2013).The Arabidopsis Book.11:e0166; Doi: 10.1199/tab.0166
21. Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, Wilczek AM.(2011).Amap of local adaptation in Arabidopsis thaliana.Science 334:86-89
22. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K.(2005).AREB1 Is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis.Plant Cell 17: 3470-3488
23. Fujita Y, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K.(2009).Transcription factors involved in the crosstalk between abiotic and biotic stress-signaling networks.In: Yoshioka K, Shinozaki K, editors.Signal crosstalk in plant stress responses.Ames Iowa: Wiley-Blackwell.p.43-58
24. Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, et al.(2009).Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis.Plant Cell Physiol.50:2123-2132
25. Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K.(2006).Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1.Proc Natl Acad Sci U S A.103:1988-1993
26. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, et al.(2011).Multiple reference genomes and transcriptomes for Arabidopsis thaliana.Nature 477:419-423
27. Geisler M, Kleczkowski LA, Karpinski S.(2006).A universal algorithm for genome-wide in silicio identification of biologically significant gene promoter putative cis-regulatory-elements; identification of new elements for reactive oxygen species and sucrose signaling in Arabidopsis.Plant J.45:384-398
28. Gibson G.(2008).The environmental contribution to gene expression profiles.Nat Rev Genet.9:575-581
29. Guiltinan MJ, MarcotteWR Jr, Quatrano RS.(1990).A plant leucine zipper protein that recognizes an abscisic acid response element.Science 250:267-271
30. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK.(2006).Natural genetic variation of freezing tolerance in Arabidopsis.Plant Physiol.142:98-112
31. Hereford J.(2009).A quantitative survey of local adaptation and fitness trade-offs.Am Nat.173:579-588
32. Hodgins-Davis A, Townsend JP.(2009).Evolving gene expression: from G to E to GxE.Trends Ecol Evol.24:649-658
33. Hoekstra HE, Coyne JA.(2007).The locus of evolution: evo devo and the genetics of adaptation.Evolution 61:995-1016
34. Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S, Auton A, Muliyati NW, Platt A, Sperone FG, Vilhjalmsson BJ, et al.(2012).Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel.Nat Genet.44:212-216
35. Huard-Chauveau C, Perchepied L, Debieu M, Rivas S, Kroj T, Kars I, Bergelson J, Roux F, Roby D.(2013).An atypical kinase under balancing selection confers broad-spectrum disease resistance in Arabidopsis.PLoS Genet.9:e1003766
36. Innocenti P, Chenoweth SF.(2013).Interspecific divergence of transcription networks along lines of genetic variance in Drosophila: dimensionality, evolvability, and constraint.Mol Biol Evol.30:1358-1367
37. Kang J-y, Choi H-i, Im M-y, Kim SY.(2002).Arabidopsis basic leucine zipper proteins thatmediate stress-responsive abscisic acid signaling.Plant Cell 14:343-357
38. Karasov TL, Kniskern JM, Gao L, DeYoung BJ, Ding J, Dubiella U, Lastra RO, Nallu S, Roux F, Innes RW, et al.(2014).The long-Term maintenance of a resistance polymorphism through diffuse interactions.Nature 512:436-440
39. Kelly AJ, Willis JH.(1998).Polymorphic microsatellite loci in Mimulus guttatus and related species.Mol Ecol Notes.7:769-774
40. Kim S, Kang J-y, Cho D-I, Park JH, Kim SY.(2004).ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signalling and its overexpression affects multiple stress tolerance.Plant J.40:75-87
41. Kim S, Plagnol V, Hu T, Toomajian C, Clark RM, Ossowsksi S, Ecker J, Weigel D, Nordborg M.(2007).Recombination and linkage disequilibrium in Arabidopsis thaliana.Nat Genet.39:1151-1155
42. Korves T, Bergelson J.(2004).A novel cost of R gene resistance in the presence of disease.Am Nat.163:489-504
43. Kroymann J, Donnerhacke S, Schnabelrauch D, Mitchell-Olds T.(2003).Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus.Proc Natl Acad Sci U S A.100:14587-14592
44. Kroymann J, Mitchell-Olds T.(2005).Epistasis and balanced polymorphism influencing complex trait variation.Nature 435:95-98
45. Lasky JR, Des Marais DL, Lowry DB, Povolotskaya I, McKay J, Richards JH, Keitt TH, Juenger TE.(2014).Natural variation in abiotic stress responsive gene expression and local adaptation to climate in Arabidopsis thaliana.Mol Biol Evol.31:2283-2296
46. Lasky JR, Des Marais DL, McKay JK, Richards JH, Juenger TE, Keitt TH.(2012).Characterizing genomic variation of Arabidopsis thaliana: the roles of geography and climate.Mol Ecol.21:5512-5529
47. Li H, Durbin R.(2009).Fast and accurate short read alignment with Burrows-Wheeler transform.Bioinformatics 25:1754-1760
48. Lowry DB, Logan TL, Santuari L, Hardtke CS, Richards JH, DeRose-Wilson LJ, McKay JK, Sen S, Juenger TE.(2013).Expression quantitative trait locus mapping across water availability environments reveals contrasting associations with genomic features in Arabidopsis.Plant Cell 25:3266-3279
49. Luscombe NM, Babu MM, Yu H, Snyder M, Teichmann SA, Gerstein M.(2004).Genomic analysis of regulatory network dynamics reveals large topological changes.Nature 431:308-312
50. Maddison WP, Maddison DR.(2009).Mesquite: a modular system for evolutionary analysis.Version 2.7 http://mesquiteproject.org
51. Mauricio R, Stahl EA, Korves T, Tian D, Kreitman M, Bergelson J.(2003).Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana.Genetics 163:735-746
52. McDonald JH.(1998).Improved tests for heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence.Mol Biol Evol.15:377-384
53. Meyer E, Aglyamova GV, Matz MV.(2011).Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure.Mol Ecol.20:3599-3616
54. Meyer E, Aspinwall MJ, Lowry DB, Palacio-Mejia JD, Logan T, Fay PA, Juenger TE.(2014).Integrating transcriptional, metabolomic, and physiological responses to drought stress and recovery in switchgrass (Panicum virgatum L.).BMC Genomics 15:527
55. Mundy J, Yamaguchi-Shinozaki K, Chua NH.(1990).Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene.Proc Natl Acad Sci U S A.87:1406-1410
56. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, et al.(2005).The pattern of polymorphism in Arabidopsis thaliana.PLoS Biol.3:e196
57. O'Connor TR, Dyreson C, Wyrick JJ.(2005).Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences.Bioinformatics 21:4411-4413
58. Reininga JM, Nielsen D, Purugganan MD.(2009).Functional and geographical differentiation of candidate balanced polymorphisms in Arabidopsis thaliana.Mol Ecol.18:2844-2855
59. Rengel D, Arribat S, Maury P, Martin-Magniette ML, Hourlier T, Laporte M, Vares D, Carrere S, Grieu P, Balzergue S, et al.(2012).A genephenotype network based on genetic variability for drought responses reveals key physiological processes in controlled and natural environments.PLoS One 7:e45249
60. Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, et al.(2002).Monitoring the expression pattern of around 7, 000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray.Funct Integr Genomics.2: 282-291
61. Shepard KA, Purugganan M.(2003).Molecular population genetics of the Arabidopsis CLAVATA2 region: the genomic scale of variation and selection in a selfing species.Genetics 163:1083-1095
62. Smith EN, Kruglyak L.(2008).Gene-environment interaction in yeast gene expression.PLoS Biol.6:e83
63. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J.(1999).Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis.Nature 400:667-671
64. Stern DL, Orgogozo V.(2008).The Loci of evolution: how predictable is genetic evolution?.Evolution 62:2155-2177
65. Tian D, Araki H, Stahl EA, Bergelson J, Kreitman M.(2002).Signature of balancing selection in Arabidopsis.Proc Natl Acad Sci U S A.99: 11525-11530
66. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M, Epple P, Kuhns C, Sureshkumar S, Schwartz C, Lanz C, et al.(2010).Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana.Nature 465:632-636
67. Ton J, Flors V, Mauch-Mani B.(2009).The multifaceted role of ABA in disease resistance.Trends Plant Sci.14:310-317
68. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K.(2000).Arabidopsis basic helix leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions.Proc Natl Acad Sci U S A.97:11632-11637
69. Vandepoele K, Quimbaya M, Casneuf T, De Veylder L, Van de Peer Y.(2009).Unraveling transcriptional control in Arabidopsis using cisregulatory elements and coexpression networks.Plant Physiol.150: 535-546
70. Weigel D, Mott R.(2009).The 1001 genomes project for Arabidopsis thaliana.Genome Biol.10:107
71. Wray GA.(2007).The evolutionary significance of cis-regulatory mutatons.Nat Rev Genet.8:206-216
72. Yamaguchi-Shinozaki K, Shinozaki K.(1994).A novel cis-Acting element in an Arabidopsis gene is involved in responsiveness to drought, lowtemperature, or high-salt stress.Plant Cell 6:251-264
73. Yamaguchi-Shinozaki K, Shinozaki K.(2006).Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses.Annu Rev Plant Biol.57:781-803
74. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K.(2010).AREB1, AREB2 and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation.Plant J.61:672-685
75. Yu D, Chen C, Chen Z.(2001).Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression.Plant Cell 13:1527-1540
76. Zhou D, Xin Z, Yi L, Zhenhai Z, Zhen S.(2010).agriGO: a GO analysis toolkit for the agricultural community.Nucleic Acids Res.38: W64-W70