Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1763, 2013, Pages

  Lovell, John T ^a   Juenger, Thomas E ^b   Michaels, Scott D ^c   Lasky, Jesse R ^b   Platt, Alexander ^d   Richards, James H ^e   Yu, Xuhong ^c   Easlon, Hsien M ^e   Sen, Saunak ^f   Mckay, John K ^a  

^a Department of Ecosystem Science and Sustainability   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c INDIANA UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arabidopsis thaliana; Drought; Flowering time; Water use efficiency

Indexed keywords

ADAPTATION; ALLELE; DICOTYLEDON; DROUGHT; DROUGHT RESISTANCE; FLOWERING; GENETIC VARIATION; PHENOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; PLEIOTROPY; WATER USE EFFICIENCY;

ARABIDOPSIS PROTEIN;

ADAPTATION; ALLELE; ARABIDOPSIS; DROUGHT; EVOLUTION; FLOWER; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE; PHYSIOLOGY; PLANT GENE; PLEIOTROPY;

ADAPTATION, PHYSIOLOGICAL; ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL EVOLUTION; DROUGHTS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC PLEIOTROPY; GENETIC VARIATION; GENOTYPE; PHENOTYPE;

EID: 84892400838     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.1043     Document Type: Article

References (76)

1. Agren J, Schemske DW. 2012 Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytol. 194, 1112-1122. (doi:10.1111/ j.1469-8137.2012.04112.x)
2. Hall MC, Willis JH. 2006 Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution 60, 2466-2477.
3. Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L. 2000 Rapid evolution of a geographic cline in size in an introduced fly. Science 287, 308-309. (doi:10.1126/science.287.5451.308)
4. Moore JS, Hendry AP. 2005 Both selection and gene flow are necessary to explain adaptive divergence: evidence from clinal variation in stream stickleback. Evol. Ecol. Res. 7, 871-886.
5. Reznick DN, Ghalambor CK. 2001 The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112, 183-198. (doi:10.1023/A:1013352109042)
6. Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J. 2004 A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc. Natl Acad. Sci. USA 101, 4712-4717. (doi:10.1073/pnas.0306401101)
7. Lande R. 1984 The genetic correlation between characters maintained by selection, linkage and inbreeding. Genet. Res. 44, 309-320. (doi:10.1017/S0016672300026549)
8. Lande R, Arnold SJ. 1983 The measurement of selection on correlated characters. Evolution 37, 1210-1226. (doi:10.2307/2408842)
9. Rockman MV. 2012 The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 66, 1-17. (doi:10.1111/j. 1558-5646.2011.01486.x)
10. Orr HA. 1998 The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52, 935-949. (doi:10.2307/ 2411226)
11. Lynch M, Walsh B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer.
12. Kirkpatrick M. 2009 Patterns of quantitative genetic variation in multiple dimensions. Genetica 136, 271-284. (doi:10.1007/s10709-008-9302-6).
13. Etterson JR, Shaw RG. 2001 Constraint to adaptive evolution in response to global warming. Science 294, 151-154. (doi:10.1126/science.1063656)
14. Schluter D. 1996 Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766-1774. (doi:10.2307/2410734)
15. Wagner GP, Altenberg L. 1996 Perspective: complex adaptations and the evolution of evolvability. Evolution 50, 967-976. (doi:10. 2307/2410639)
16. Blows MW, Hoffmann AA. 2005 A reassessment of genetic limits to evolutionary change. Ecology 86, 1371-1384. (doi:10.1890/04-1209)
17. Lande R. 1982 A quantitative genetic theory of life-history evolution. Ecology 63, 607-615. (doi:10. 2307/1936778)
18. MitchellOlds T. 1996 Pleiotropy causes long-term genetic constraints on life-history evolution in Brassica rapa. Evolution 50, 1849-1858. (doi:10.2307/2410742)
19. Agrawal AF, Stinchcombe JR. 2009 How much do genetic covariances alter the rate of adaptation? Proc. R. Soc. B 276, 1183-1191. (doi:10.1098/rspb. 2008.1671)
20. Blows MW, Chenoweth SF, Hine E. 2004 Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am. Nat. 163, 329-340. (doi:10.1086/ 381941)
21. Curtsinger JW, Service PM, Prout T. 1994 Antagonistic pleiotropy, reversal of dominance, and genetic-polymorphism. Am. Nat. 144, 210-228. (doi:10.1086/285671)
22. Hedrick PW. 1999 Antagonistic pleiotropy and genetic polymorphism: a perspective. Heredity 82, 126-133. (doi:10.1038/sj.hdy.6884400)
23. Houle D. 1991 Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45, 630-648. (doi:10.2307/2409916)
24. Rose MR. 1982 Antagonistic pleiotropy, dominance, and genetic variation. Heredity 48, 63-78. (doi:10. 1038/hdy.1982.7)
25. Scarcelli N, Cheverud JM, Schaal BA, Kover PX. 2007 Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proc. Natl Acad. Sci. USA 104, 16986-16991. (doi:10.1073/ pnas.0708209104)
26. Otto SP. 2004 Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proc. R. Soc. Lond. B 271, 705-714. (doi:10.1098/rspb. 2003.2635)
27. Ostman B, Hintze A, Adami C. 2012 Impact of epistasis and pleiotropy on evolutionary adaptation. Proc. R. Soc. B 279, 247-256. (doi:10.1098/rspb.2011.0870)
28. Wang Z, Liao B-Y, Zhang J. 2010 Genomic patterns of pleiotropy and the evolution of complexity. Proc. Natl Acad. Sci. USA (doi:10.1073/pnas.1004666107)
29. Hill WG, Zhang XS. 2012 Assessing pleiotropy and its evolutionary consequences: pleiotropy is not necessarily limited, nor need it hinder the evolution of complexity. Nat. Rev. Genet. 13, 295. (doi:10.1038/nrg2949-c1)
30. Bray EA. 1997 Plant responses to water deficit. Trends Plant Sci. 2, 48-54. (doi:10.1016/S1360-1385(97)82562-9)
31. Meyre D, Leonardi A, Brisson G, Vartanian N. 2001 Drought-adaptive mechanisms involved in the escape/tolerance strategies of Arabidopsis Landsberg erecta and Columbia ecotypes and their F1 reciprocal progeny. J. Plant Physiol. 158, 1145-1152. (doi:10.1078/S0176-1617(04)70141-8)
32. Sultan SE, Bazzaz FA. 1993 Phenotypic plasticity in Polygonum persicaria 2. Norms of reaction to soil moisture and the maintenance of genetic diversity. Evolution 47, 1032-1049. (doi:10.2307/2409973)
33. Touchette BW, Iannacone LR, Turner GE, Frank AR. 2007 Drought tolerance versus drought avoidance: a comparison of plant-water relations in herbaceous wetland plants subjected to water withdrawal and repletion. Wetlands 27, 656-667. (doi:10.1672/ 0277-5212(2007)27[656:DTVDAA]2.0.CO;2)
34. Araus JL, Slafer GA, Reynolds MP, Royo C. 2002 Plant breeding and drought in C-3 cereals: what should we breed for? Ann. Bot. 89, 925-940. (doi:10.1093/aob/mcf049)
35. Franks SJ, Sim S, Weis AE. 2007 Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl Acad. Sci. USA 104, 1278-1282. (doi:10.1073/pnas.0608379104)
36. Sherrard ME, Maherali H. 2006 The adaptive significance of drought escape in Avena barbata, an annual grass. Evolution 60, 2478-2489.
37. Donovan LA, Dudley SA, Rosenthal DM, Ludwig F. 2007 Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers. Oecologia 152, 13-25. (doi:10.1007/s00442-006-0627-5)
38. McKay JK, Richards JH, Mitchell-Olds T. 2003 Genetics of drought adaptation in Arabidopsis thaliana.: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol. Ecol. 12, 1137-1151. (doi:10.1046/j.1365-294X.2003. 01833.x)
39. Rosenthal DM, Stiller V, Sperry JS, Donovan LA. 2010 Contrasting drought tolerance strategies in two desert annuals of hybrid origin. J. Exp. Bot. 61, 2769-2778. (doi:10.1093/jxb/erq109)
40. Heschel MS, Riginos C. 2005 Mechanisms of selection for drought stress tolerance and avoidance in Impatiens capensis (Balsaminacea). Am. J. Bot. 92, 37-44. (doi:10.3732/ajb.92.1.37)
41. Heschel MS, Donohue K, Hausmann N, Schmitt J. 2002 Population differentiation and natural selection for water-use efficiency in Impatiens capensis (Balsaminaceae). Int. J. Plant Sci. 163, 907-912. (doi:10.1086/342519)
42. Chaves MM, Maroco JP, Pereira JS. 2003 Understanding plant responses to drought: from genes to the whole plant. Funct. Plant Biol. 30, 239-264. (doi:10.1071/fp02076)
43. Angert AL, Huxman TE, Barron-Gafford GA, Gerst KL, Venable DL. 2007 Linking growth strategies to long-term population dynamics in a guild of desert annuals. J. Ecol. 95, 321-331. (doi:10.1111/j.1365-2745.2006.01203.x)
44. Menendez CM, Hall AE. 1995 Heritability of carbon-isotope discrimination and correlations with earliness in cowpea. Crop Sci. 35, 673-678. (doi:10.2135/cropsci1995.0011183X003500030003x)
45. Geber MA, Dawson TE. 1990 Genetic variation in and covariation between leaf gas-exchange, morphologhy, and development in Polygonum arenastrum, an annual plant. Oecologia 85, 153-158. (doi:10.1007/bf00319396)
46. McKay JK, Richards JH, Nemali KS, Sen S, Mitchell-Olds T, Boles S, Stahl EA, Wayne T, Juenger TE. 2008 Genetics of drought adaptation in Arabidopsis thaliana. II. QTL analysis of a new mapping populations, KAS-1 x TSU-1. Evolution 62, 3014-3026. (doi:10.1111/j.1558-5646.2008.00474.x)
47. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000 Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344-347. (doi:10. 1126/science.290.5490.344)
48. Lee I, Amasino RM. 1995 Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol. 108, 157-162.
49. Lee I, Michaels SD, Masshardt AS, Amasino RM. 1994 The late-flowering phenotype of FRIGIDA and mutations in Luminidependens is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6, 903-909. (doi:10.1046/j.1365-313X.1994. 6060903.x)
50. Michaels SD, Amasino RM. 1999 Flowering locus C encodes a novel MADS domain protein that acts as a repressor of flowering. Cell Online 11, 949-956. (doi:10.1105/tpc.11.5.949)
51. Caemmerer S, Farquhar GD. 1981 Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376-387. (doi:10.1007/bf00384257)
52. 13C, stomatal conductance and transpiration efficiency. Plant Cell Environ. 28, 697-708. (doi:10.1111/j.1365-3040.2004.01313.x)
53. Broman KW, Wu H, Sen S, Churchill GA. 2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889-890. (doi:10.1093/bioinformatics/btg112)
54. Manichaikul A, Moon JY, Sen S, Yandell BS, Broman KW. 2009 A model selection approach for the identification of quantitative trait loci in experimental crosses, allowing epistasis. Genetics 181, 1077-1086. (doi:10.1534/genetics.108. 094565)
55. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D. 2008 Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res. 18, 2024-2033. (doi:10.1101/ gr.080200.108)
56. Atwell S et al. 2010 Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627-631. (doi:10.1038/ nature08800)
57. Horton MW et al. 2012 Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat. Genet. 44, 212-216. (doi:10.1038/ng.1042)
58. 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. (doi:10.1111/j.1365-294X.2012.05709.x)
59. Purcell S et al. 2007 PLINK: a toolset for whole-genome association and population-based linkage analysis. Am. J. Hum. Genet. 81, 559-575. (doi:10.1086/519795)
60. Nord EA, Shea K, Lynch JP. 2011 Optimizing reproductive phenology in a two-resource world: a dynamic allocation model of plant growth predicts later reproduction in phosphorus-limited plants. Ann. Bot. 108, 391-404. (doi:10.1093/aob/mcr143)
61. Reekie EG, Bazzaz FA. 1987 Reproductive effort in plants. 3. Effect of reproduction on vegetative activity. Am. Nat. 129, 907-919. (doi:10.1086/ 284683)
62. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C. 2005 Role of FRIGIDA and flowering locus C in determining variation in flowering time of Arabidopsis. Plant Physiol. 138, 1163-1173. (doi:10.1104/pp.105.061309)
63. Gazzani S, Gendall AR, Lister C, Dean C. 2003 Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132, 1107-1114. (doi:10.1104/pp.103.021212)
64. Geraldo N, Baurle I, Kidou S, Hu XY, Dean C. 2009 FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol. 150, 1611-1618. (doi:10.1104/pp.109.137448)
65. Korves TM, Schmid KJ, Caicedo AL, Mays C, Stinchcombe JR, Purugganan MD, Schmitt J. 2007 Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. Am. Nat. 169, E141-E157. (doi:10.1086/513111)
66. Christman MA, Richards JH, McKay JK, Stahl EA, Juenger TE, Donovan LA. 2008 Genetic variation in Arabidopsis thaliana for night-time leaf conductance. Plant Cell Environ. 31, 1170-1178. (doi:10.1111/j.1365-3040.2008.01833.x)
67. Brock MT, Stinchcombe JR, Weinig C. 2009 Indirect effects of FRIGIDA: floral trait (co)variances are altered by seasonally variable abiotic factors associated with flowering time. J. Evol. Biol. 22, 1826-1838. (doi:10.1111/j.1420-9101.2009.01794.x)
68. Mendez-Vigo B, Pico FX, Ramiro M, Martinez-Zapater JM, Alonso-Blanco C. 2011 Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC Genes in Arabidopsis. Plant Physiol. 157, 1942-1955. (doi:10.1104/pp.111. 183426)
69. Michaels SD, Amasino RM. 2001 Loss of flowering locus C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13, 935-941.
70. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD. 2004 Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc. Natl Acad. Sci. USA 101, 15670-15675. (doi:10.1073/pnas.0406232101)
71. Wilczek AM et al. 2009 Effects of genetic perturbation on seasonal life history plasticity. Science 323, 930-934. (doi:10.1126/science. 1165826)
72. Gan X et al. 2011 Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419-423. (doi:10.1038/nature10414)
73. Zhang XS, Hill WG. 2003 Multivariate stabilizing selection and pleiotropy in the maintenance of quantitative genetic variation. Evolution 57, 1761-1775. (doi:10.1554/02-587)
74. Waxman D, Peck JR. 1998 Pleiotropy and the preservation of perfection. Science 279, 1210-1213. (doi:10.1126/science.279.5354.1210)
75. Le Corre V, Roux F, Reboud X. 2002 DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol. Biol. Evol. 19, 1261-1271. (doi:10.1093/oxfordjournals.molbev.a004187)
76. Toomajian C et al. 2006 A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biol. 4, 732-738. (doi:10.1371/journal.pbio.0040137)