Rates of evolution in stress-related genes are associated with habitat preference in two Cardamine lineages

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages

  Ometto, Lino ^a   Li, Mingai ^a   Bresadola, Luisa ^a   Varotto, Claudio ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

454 next generation sequencing; adaptive traits; Cardamine; habitat preference; Molecular evolution

Indexed keywords

ADAPTATION; COLD TOLERANCE; DICOTYLEDON; EFFECTIVE POPULATION SIZE; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESS; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENOMICS; HABITAT SELECTION; MOLECULAR ANALYSIS; PHOTOSYNTHESIS; PROTEIN;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CARDAMINE; CARDAMINE IMPATIENS; IMPATIENS;

VEGETABLE PROTEIN;

ARTICLE; CARDAMINE; CLASSIFICATION; CODON; ECOSYSTEM; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY;

CARDAMINE; CODON; ECOSYSTEM; EVOLUTION, MOLECULAR; PHYLOGENY; PLANT PROTEINS;

EID: 84862801505     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-7     Document Type: Article

References (141)

1. The genetic theory of adaptation: a brief history. Orr HA, Nat Rev Genet 2005 6 119 127 15716908
2. The genetic basis of adaptive melanism in pocket mice. Nachman MW, Hoekstra HE, D'Agostino SL, Proc Natl Acad Sci USA 2003 100 5268 5273 10.1073/pnas.0431157100 12704245
3. The molecular basis of high-altitude adaptation in deer mice. Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N, Monteiro B, Nachman MW, PLoS Genet 2007 3 45 10.1371/journal.pgen.0030045 17397259
4. Relaxed selection on the CBF/DREB1 regulatory genes and reduced freezing tolerance in the southern range of Arabidopsis thaliana. Zhen Y, Ungerer MC, Mol Biol Evol 2008 25 2547 2555 10.1093/molbev/msn196 18775899
5. Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold hardiness in coastal Douglas Fir (Pseudotsuga menziesii var. menziesii). Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB, Genetics 2009 183 289 298 10.1534/genetics.109.103895 19596906
6. Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Paaby AB, Blacket MJ, Hoffmann AA, Schmidt PS, Mol Ecol 2010 19 760 774 10.1111/j.1365-294X.2009. 04508.x 20074316
7. Nucleotide diversity patterns of local adaptation at drought-related candidate genes in wild tomatoes. Xia H, Camus-Kulandaivelu L, Stephan W, Tellier A, Zhang Z, Mol Ecol 2010 19 4144 4154 10.1111/j.1365-294X.2010.04762.x
8. Integrating evolutionary and functional approaches to infer adaptation at specific loci. Storz JF, Wheat CW, Evolution 2010 64 2489 2509 10.1111/j.1558-5646.2010.01044.x 20500215
9. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Clark AG, Glanowski S, Nielsen R, Thomas PD, Kejariwal A, Todd MA, Tanenbaum DM, Civello D, Lu F, Murphy B, Ferriera S, Wang G, Zheng X, White TJ, Sninsky JJ, Adams MD, Cargill M, Science 2003 302 1960 1963 10.1126/science. 1088821 14671302
10. A scan for positively selected genes in the genomes of humans and chimpanzees. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ, Sninsky JJ, Adams MD, Cargill M, PLoS Biol 2005 3 170 10.1371/journal.pbio.0030170 15869325
11. Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Oetjen K, Reusch TBH, Mol Ecol 2007 16 5156 5167 10.1111/j.1365-294X.2007.03577.x 17986196
12. Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Namroud M-C, Beaulieu J, Juge N, Laroche J, Bousquet J, Mol Ecol 2008 17 3599 3613 10.1111/j.1365-294X. 2008.03840.x 18662225
13. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Gossmann TI, Song B-H, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A, Mol Biol Evol 2010 27 1822 1832 10.1093/molbev/msq079 20299543
14. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA, PLoS Genet 2010 6 1000862 10.1371/journal.pgen.1000862 20195501
15. Körner C, Alpine plant life. Functional plant ecology of high mountain ecosystems Berlin, Germany: Springer 2 2003
16. Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana. Zhen Y, Ungerer MC, New Phytol 2008 177 419 427 17995917
17. Assembly of nonnative floras along elevational gradients explained by directional ecological filtering. Alexander JM, Kueffer C, Daehler CC, Edwards PJ, Pauchard A, Seipel T, MIREN Consortium, Proc Natl Acad Sci USA 2011 108 656 661 10.1073/pnas.1013136108 21187380
18. Changes in climatic water balance drive downhill shifts in plant species' optimum elevations. Crimmins SM, Dobrowski SZ, Greenberg JA, Abatzoglou JT, Mynsberge AR, Science 2011 331 324 327 10.1126/science.1199040 21252344
19. Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. Montesinos-Navarro A, Wig J, Pico FX, Tonsor SJ, New Phytol 2011 189 282 294 10.1111/j.1469-8137.2010.03479.x 20880224
20. A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. Hannah MA, Heyer AG, Hincha DK, PLoS Genet 2005 1 26 10.1371/journal.pgen.0010026 16121258
21. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Vogel JT, Zarka DG, van Buskirk HA, Fowler SG, Thomashow MF, Plant J 2005 41 195 211 15634197
22. Cold signalling and cold acclimation in plants. Ruelland E, Vaultier M-N, Zachowski A, Hurry V, Adv Bot Res 2009 49 35 150
23. Divergent strategies of photoprotection in high-mountain plants. Streb P, Shang W, Feierabend J, Bligny R, Planta 1998 207 313 324 10.1007/s004250050488
24. High resistance to low-temperature photoinhibition in two alpine, snowbank species. Germino M, Smith W, Physiol Plantarum 2000 110 89 95 10.1034/j.1399-3054.2000.110112.x
25. Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Frohnmeyer H, Staiger D, Plant Physiol 2003 133 1420 1428 10.1104/pp.103.030049 14681524
26. Cold- and light-induced changes of metabolite and antioxidant levels in two high mountain plant species Soldanella alpina and Ranunculus glacialis and a lowland species Pisum sativum. Streb P, Aubert S, Gout E, Bligny R, Physiol Plantarum 2003 118 96 104 10.1034/j.1399-3054.2003.00099.x
27. Molecular evolution of phytochromes in Cardamine nipponica (Brassicaceae) suggests the involvement of PHYE in local adaptation. Ikeda H, Fujii N, Setoguchi H, Genetics 2009 182 603 614 10.1534/genetics.109.102152 19363127
28. Aeschimann D, Lauber K, Moser DM, Theurillat J-P, Flora Alpina Bern, Switzerland: Haupt Verlag 2004
29. Comparative Studies on the Reproductive Systems of Cardamine flexuosa, C. impatiens, C. scutata, and C. lyrata, Cruciferae. Kimata M, Bot Mag Tokyo 1983 96 299 312 10.1007/BF02488175
30. Taxonomy and phylogeography of Cardamine impatiens and C. pectinata (Brassicaceae). Kucera J, Lihova J, Marhold K, Bot J Linn Soc 2006 152 169 195 10.1111/j.1095-8339.2006.00559.x
31. Contrasting phylogeographies inferred for the two alpine sister species Cardamine resedifolia and C. alpina (Brassicaceae). Lihova J, Carlsen T, Brochmann C, Marhold K, J Biogeogr 2009 36 104 120 10.1111/j.1365-2699.2008. 01998.x
32. Toward a global phylogeny of the Brassicaceae. Bailey CD, Koch MA, Mayer M, Mummenhoff K, O'Kane SL, Warwick SI, Windham MD, Al-Shehbaz IA, Mol Biol Evol 2006 23 2142 2160 10.1093/molbev/msl087 16916944
33. Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Couvreur TLP, Franzke A, Al-Shehbaz IA, Bakker FT, Koch MA, Mummenhoff K, Mol Biol Evol 2010 27 55 71 10.1093/molbev/msp202 19744998
34. A Simple Sequentially Rejective Multiple Test Procedure. Holm S, Scand J Statist 1979 6 65 70
35. PAML 4: phylogenetic analysis by maximum likelihood. Yang Z, Mol Biol Evol 2007 24 1586 1591 10.1093/molbev/msm088 17483113
36. Human housekeeping genes are compact. Eisenberg E, Levanon EY, Trends Genet 2003 19 362 365 10.1016/S0168-9525(03)00140-9 12850439
37. Gametophytic selection in Arabidopsis thaliana supports the selective model of intron length reduction. Seoighe C, Gehring C, Hurst LD, PLoS Genet 2005 1 13 10.1371/journal.pgen.0010013 16110339
38. Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Ingvarsson PK, Mol Biol Evol 2007 24 836 844 17204548
39. Intergenic and genic sequence lengths have opposite relationships with respect to gene expression. Colinas J, Schmidler SC, Bohrer G, Iordanov B, Benfey PN, PLoS ONE 2008 3 3670 10.1371/journal.pone.0003670 18989364
40. Mutational biases and selective forces shaping the structure of Arabidopsis genes. Camiolo S, Rau D, Porceddu A, PLoS ONE 2009 4 6356 10.1371/journal.pone.0006356 19633720
41. Conservation of core gene expression in vertebrate tissues. Chan ET, Quon GT, Chua G, Babak T, Trochesset M, Zirngibl RA, Aubin J, Ratcliffe MJH, Wilde A, Brudno M, Morris QD, Hughes TR, J Biol 2009 8 33 10.1186/jbiol130 19371447
42. Large scale comparison of global gene expression patterns in human and mouse. Zheng-Bradley X, Rung J, Parkinson H, Brazma A, Genome Biol 2010 11 124 10.1186/gb-2010-11-12-r124 21182765
43. Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower. Chanderbali AS, Yoo M-J, Zahn LM, Brockington SF, Wall PK, Gitzendanner MA, Albert VA, Leebens-Mack J, Altman NS, Ma H, Depamphilis CW, Soltis DE, Soltis PS, Proc Natl Acad Sci USA 2010 107 22570 22575 10.1073/pnas.1013395108 21149731
44. Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Jiao Y, Ma L, Strickland E, Deng XW, Plant Cell 2005 17 3239 3256 10.1105/tpc.105.035840 16284311
45. Use of nuclear genes for phylogeny reconstruction in plants. Small R, Cronn R, Wendel J, Aust Syst Bot 2004 17 145 170 10.1071/SB03015
46. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, Ophir R, Bar-Even A, Horn-Saban S, Safran M, Domany E, Lancet D, Shmueli O, Bioinformatics 2005 21 650 659 10.1093/bioinformatics/ bti042 15388519
47. The effect of linkage on limits to artificial selection. Hill WG, Robertson A, Genet Res 1966 8 269 294 10.1017/S0016672300010156 5980116
48. Hill-Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Kliman RM, Hey J, Genet Res 2003 81 89 90 10.1017/S0016672302006067 12872910
49. Linkage limits the power of natural selection in Drosophila. Betancourt AJ, Presgraves DC, Proc Natl Acad Sci USA 2002 99 13616 13620 10.1073/pnas.212277199 12370444
50. Neutral effect of recombination on base composition in Drosophila. Marais G, Mouchiroud D, Duret L, Genet Res 2003 81 79 87 10.1017/S0016672302006079 12872909
51. Biogeography and phylogeny of Cardamine (Brassicaceae). Carlsen T, Bleeker W, Hurka H, Elven R, Brochmann C, Ann Mo Bot Gard 2009 96 215 236 10.3417/2007047
52. Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S-26S rDNA internal and external transcribed spacers. Andreasen K, Baldwin BG, Mol Biol Evol 2001 18 936 944 11371581
53. Rates of molecular evolution are linked to life history in flowering plants. Smith SA, Donoghue MJ, Science 2008 322 86 89 10.1126/science.1163197 18832643
54. Evolutionary rates in Veronica L. (Plantaginaceae): disentangling the influence of life history and breeding system. Müller K, Albach DC, J Mol Evol 2010 70 44 56 10.1007/s00239-009-9307-5 20024538
55. Broad-scale analysis contradicts the theory that generation time affects molecular evolutionary rates in plants. Whittle C-A, Johnston MO, J Mol Evol 2003 56 223 233 10.1007/s00239-002-2395-0 12574868
56. Breeding systems and genome evolution. Charlesworth D, Wright SI, Curr Opin Genet Dev 2001 11 685 690 10.1016/S0959-437X(00)00254-9 11682314
57. Watching the clock: studying variation in rates of molecular evolution between species. Lanfear R, Welch JJ, Bromham L, Trends Ecol Evol 2010 25 495 503 10.1016/j.tree.2010.06.007 20655615
58. Fundamental concepts in genetics: Effective population size and patterns of molecular evolution and variation. Charlesworth B, Nat Rev Genet 2009
59. Recombination enhances protein adaptation in Drosophila melanogaster. Presgraves DC, Curr Biol 2005 15 1651 1656 10.1016/j.cub.2005.07.065 16169487
60. The positive correlation between dN/dS and dS in mammals is due to runs of adjacent substitutions. Stoletzki N, Eyre-Walker A, Mol Biol Evol 2011 28 1371 1380 10.1093/molbev/msq320 21115654
61. Correlation between Ka/Ks and Ks is related to substitution model and evolutionary lineage. Li J, Zhang Z, Vang S, Yu J, Wong GK-S, Wang J, J Mol Evol 2009 68 414 423 10.1007/s00239-009-9222-9 19308632
62. The population genetics of dN/dS. Kryazhimskiy S, Plotkin JB, PLoS Genet 2008 4 1000304 10.1371/journal.pgen.1000304 19081788
63. Nonlinear dynamics of nonsynonymous (dN) and synonymous (dS) substitution rates affects inference of selection. Wolf JBW, Künstner A, Nam K, Jakobsson M, Ellegren H, Genome Biol Evol 2009 1 308 319 20333200
64. The Arabidopsis Information Resource. http://www.arabidopsis.org
65. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Kreps J, Wu Y, Chang H, Zhu T, Wang X, Harper J, Plant Physiol 2002 130 2129 2141 10.1104/pp.008532 12481097
66. Regulatory network of gene expression in the drought and cold stress responses. Shinozaki K, Yamaguchi-Shinozaki K, Seki M, Curr Opin Plant Biol 2003 6 410 417 10.1016/S1369-5266(03)00092-X 12972040
67. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. Swindell WR, Huebner M, Weber AP, BMC Genomics 2007 8 125 10.1186/1471-2164-8-125 17519032
68. Responses of the plasma membrane to low temperatures. Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y, Physiol Plantarum 2006 126 81 89 10.1111/j.1399-3054.2005.00594.x
69. Natural selection on synonymous and nonsynonymous mutations shapes patterns of polymorphism in Populus tremula. Ingvarsson PK, Mol Biol Evol 2010 27 650 660 10.1093/molbev/msp255 19837657
70. Genome-wide evidence for efficient positive and purifying selection in Capsella grandiflora, a plant species with a large effective population size. Slotte T, Foxe JP, Hazzouri KM, Wright SI, Mol Biol Evol 2010 27 1813 1821 10.1093/molbev/msq062 20194429
71. Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species. Strasburg JL, Scotti-Saintagne C, Scotti I, Lai Z, Rieseberg LH, Mol Biol Evol 2009 26 1341 1355 10.1093/molbev/msp043 19276154
72. The cost of inbreeding in Arabidopsis. Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL, Nature 2002 416 531 534 10.1038/416531a 11932744
73. Selection on amino acid substitutions in Arabidopsis. Foxe JP, Dar V-U-N, Zheng H, Nordborg M, Gaut BS, Wright SI, Mol Biol Evol 2008 25 1375 1383 10.1093/molbev/msn079 18390851
74. Challenges of detecting directional selection after a bottleneck: lessons from Sorghum bicolor. Hamblin MT, Casa AM, Sun H, Murray SC, Paterson AH, Aquadro CF, Kresovich S, Genetics 2006 173 953 964 10.1534/genetics.105.054312 16547110
75. A systematic search for positive selection in higher plants (Embryophytes). Roth C, Liberles DA, BMC Plant Biol 2006 6 12 10.1186/1471-2229-6-12 16784532
76. Effective population size is positively correlated with levels of adaptive divergence among annual sunflowers. Strasburg JL, Kane NC, Raduski AR, Bonin A, Michelmore R, Rieseberg LH, Mol Biol Evol 2011 28 1569 1580 10.1093/molbev/msq270 20952500
77. Adaptive protein evolution at the Adh locus in Drosophila. McDonald JH, Kreitman M, Nature 1991 351 652 654 10.1038/351652a0 1904993
78. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Arabidopsis Genome Initiative, Nature 2000 408 796 815 10.1038/35048692 11130711
79. Modeling gene and genome duplications in eukaryotes. Maere S, de Bodt S, Raes J, Casneuf T, van Montagu M, Kuiper M, van de Peer Y, Proc Natl Acad Sci USA 2005 102 5454 5459 10.1073/pnas.0501102102 15800040
80. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Tuskan GA, Difazio S, Jansson S, et al. Science 2006 313 1596 1604 10.1126/science.1128691 16973872
81. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon A-F, Weissenbach J, Quétier F, Wincker P, French-Italian Public Consortium for Grapevine Genome Characterization, Nature 2007 449 463 467 10.1038/nature06148 17721507
82. The evolutionary dynamics of plant duplicate genes. Moore RC, Purugganan MD, Curr Opin Plant Biol 2005 8 122 128 10.1016/j.pbi.2004.12.001 15752990
83. So what's new in the field of plant cold acclimation? Lots! Thomashow MF, Plant Physiol 2001 125 89 93 10.1104/pp.125.1.89 11154304
84. The role of CBF transcriptional activators in two Citrus species (Poncirus and Citrus) with contrasting levels of freezing tolerance. Champ KI, Febres VJ, Moore GA, Physiol Plantarum 2007 129 529 541 10.1111/j.1399-3054. 2006.00826.x
85. The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements. Pennycooke JC, Cheng H, Roberts SM, Yang Q, Rhee SY, Stockinger EJ, Plant Mol Biol 2008 67 483 497 10.1007/s11103-008-9333-5 18415686
86. Inside the CBF locus in Poaceae. Tondelli A, Francia E, Barabaschi D, Pasquariello M, Pecchioni N, Plant Sci 2011 180 39 45 10.1016/j.plantsci.2010. 08.012 21421345
87. Molecular characterization of a novel intracellular hyaluronan-binding protein. Huang L, Grammatikakis N, Yoneda M, Banerjee SD, Toole BP, J Biol Chem 2000 275 29829 29839 10.1074/jbc.M002737200 10887182
88. The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. Lazzaroni JC, Germon P, Ray MC, Vianney A, FEMS Microbiol Lett 1999 177 191 197 10.1111/j.1574-6968.1999. tb13731.x 10474183
89. Molecular mechanisms of metal hyperaccumulation in plants. Verbruggen N, Hermans C, Schat H, New Phytol 2009 181 759 776 10.1111/j.1469-8137.2008.02748.x 19192189
90. Nickel, chromium and cobalt in plants from italian serpentine areas. Vergnano Gambi O, Gabbrielli R, Pancaro L, Acta Oecol-Oec Plant 1982 3 291 306
91. Biosynthesis and metabolic engineering of glucosinolates. Mikkelsen MD, Petersen BL, Olsen CE, Halkier BA, Amino Acids 2002 22 279 295 10.1007/s007260200014 12083070
92. Evidence for the pathway to pantothenate in plants. Jones C, Dancer J, Smith A, Abell C, Can J Chem 1994 72 261 263 10.1139/v94-039
93. Auxin conjugates: their role for plant development and in the evolution of land plants. Ludwig-Müller J, J Exp Bot 2011 62 1757 1773 10.1093/jxb/erq412 21307383
94. Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Wang L, Allmann S, Wu J, Baldwin IT, Plant Physiol 2008 146 904 915 10.1104/pp.107.109264 18065562
95. JAZ repressors set the rhythm in jasmonate signaling. Chico JM, Chini A, Fonseca S, Solano R, Curr Opin Plant Biol 2008 11 486 494 10.1016/j.pbi.2008.06. 003 18653378
96. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico J-M, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Manuel Franco-Zorrilla J, Pauwels L, Witters E, Isabel Puga M, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano R, Plant Cell 2011 23 701 715 10.1105/tpc.110.080788 21335373
97. Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA, Plant Physiol 2008 146 952 964 10.1104/pp.107.115691 18223147
98. The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein DJ, Gershenzon J, Plant Cell 2001 13 2793 2807 11752388
99. Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching. Haugen R, Steffes L, Wolf J, Brown P, Matzner S, Siemens DH, Oikos 2008 117 231 244 10.1111/j.2007.0030-1299. 16111.x
100. Elevational and seasonal variation in the foliar quality and arthropod community of Acer pensylvanicum. Zehnder CB, Stodola KW, Joyce BL, Egetter D, Cooper RJ, Hunter MD, Environ Entomol 2009 38 1161 1167 10.1603/022.038.0424 19689895
101. Spatial variation in herbivory by forest canopy arthropods along an elevation gradient. Reynolds B, Crossley D, Environ Entomol 1997 26 1232 1239
102. Leaf phenology, seasonal changes in leaf quality and herbivory pattern of Sanguisorba tenuifolia at different altitudes. Suzuki S, Oecologia 1998 117 169 176 10.1007/s004420050645
103. Altitudinal variation in foliar chemistry and anatomy of yunnan pine, Pinus yunnanensis, and pine sawfly (Hym., Diprionidae) performance. Hengxiao G, McMillin J, Wagner M, Zhou J, Zhou Z, Xu X, J Appl Entomol 1999 123 465 471 10.1046/j.1439-0418.1999.00395.x
104. Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, bittercress). Louda S, Rodman J, J Ecol 1996 84 229 237 10.2307/2261358
105. Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Pnueli L, Liang H, Rozenberg M, Mittler R, Plant J 2003 34 185 201
106. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R, Plant Cell 2005 17 268 281 10.1105/tpc.104.026971 15608336
107. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Kim J, Choi D, Kende H, Plant J 2003 36 94 104 10.1046/j.1365-313X.2003.01862.x 12974814
108. A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Kim J, Kende H, Proc Natl Acad Sci USA 2004 101 13374 13379 10.1073/pnas.0405450101 15326298
109. The transcriptional response of Arabidopsis to genotoxic stress-a high-density colony array study (HDCA). Chen I-P, Haehnel U, Altschmied L, Schubert I, Puchta H, Plant J 2003 35 771 786 10.1046/j.1365-313X.2003.01847.x 12969430
110. Selection in the evolution of gene duplications. Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV, Genome Biol 2002 3 ESEARCH0008 11864370
111. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Fowler SG, Thomashow MF, Plant Cell 2002 14 1675 1690 10.1105/tpc.003483 12172015
112. BLAST+: architecture and applications. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL, BMC Bioinformatics 2009 10 421 10.1186/1471-2105-10-421 20003500
113. A genomic perspective on protein families. Tatusov RL, Koonin EV, Lipman DJ, Science 1997 278 631 637 10.1126/science.278.5338.631 9381173
114. Clustal W and Clustal X version 2.0. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, Bioinformatics 2007 23 2947 2948 10.1093/bioinformatics/btm404 17846036
115. Transport of proteins into chloroplasts. Partial purification of a chloroplast protease involved in the processing of important precursor polypeptides. Robinson C, Ellis RJ, Eur J Biochem 1984 142 337 342 10.1111/j.1432-1033.1984.tb08291.x 6430703
116. Protein translocation into and across the chloroplastic envelope membranes. Soll J, Tien R, Plant Mol Biol 1998 38 191 207 10.1023/A: 1006034020192 9738967
117. Domain structure of mitochondrial and chloroplast targeting peptides. von Heijne G, Steppuhn J, Herrmann RG, Eur J Biochem 1989 180 535 545 10.1111/j.1432-1033.1989.tb14679.x 2653818
118. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Emanuelsson O, Nielsen H, von Heijne G, Protein Sci 1999 8 978 984 10.1110/ps.8.5.978 10338008
119. Functional annotation of the Arabidopsis genome using controlled vocabularies. Berardini TZ, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller LA, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee SY, Plant Physiol 2004 135 745 755 10.1104/pp.104.040071 15173566
120. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Chinnusamy V, Ohta M, Kanrar S, Lee B-H, Hong X, Agarwal M, Zhu J-K, Gene Dev 2003 17 1043 1054 10.1101/gad.1077503 12672693
121. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF, Plant J 1998 16 433 442 10.1046/j.1365-313x.1998.00310.x 9881163
122. Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Jaglo-Ottosen KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF, Plant Physiol 2001 127 910 917 10.1104/pp.010548 11706173
123. The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression Is regulated by low temperature but not by abscisic acid or dehydration. Medina J, Bargues M, Terol J, Pérez-Alonso M, Salinas J, Plant Physiol 1999 119 463 470 10.1104/pp.119.2.463 9952441
124. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK, Gene Dev 2001 15 912 924 10.1101/gad.866801 11297514
125. eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Xin Z, Browse J, Proc Natl Acad Sci USA 1998 95 7799 7804 10.1073/pnas.95.13.7799 9636231
126. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Gilmour SJ, Fowler SG, Thomashow MF, Plant Mol Biol 2004 54 767 781 15356394
127. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Lee B-H, Henderson DA, Zhu J-K, Plant Cell 2005 17 3155 3175 10.1105/tpc.105.035568 16214899
128. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D'Angelo C, Bornberg-Bauer E, Kudla J, Harter K, Plant J 2007 50 347 363 10.1111/j.1365-313X.2007.03052.x 17376166
129. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Yang Z, Nielsen R, Goldman N, Pedersen A, Genetics 2000 155 431 449 10790415
130. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Yang Z, Nielsen R, Mol Biol Evol 2000 17 32 43 10666704
131. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Yang Z, Mol Biol Evol 1998 15 568 573 9580986
132. Bayes empirical bayes inference of amino acid sites under positive selection. Yang Z, Wong WSW, Nielsen R, Mol Biol Evol 2005 22 1107 1118 10.1093/molbev/msi097 15689528
133. A direct approach to false discovery rates. Storey J, J Roy Stat Soc B 2002 64 479 498 10.1111/1467-9868.00346
134. R: A Language and Environment for Statistical Computing. R Development Core Team, Vienna, Austria: R Foundation for Statistical Computing 2009
135. Patterns of codon usage bias in Silene latifolia. Qiu S, Bergero R, Zeng K, Charlesworth D, Mol Biol Evol 2011 28 771 780 10.1093/molbev/msq251 20855431
136. A gene expression map of Arabidopsis thaliana development. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU, Nat Genet 2005 37 501 506 10.1038/ng1543 15806101
137. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. Ikemura T, J Mol Biol 1981 151 389 409 10.1016/0022-2836(81)90003-6 6175758
138. CodonW. http://codonw.sourceforge.net/
139. Codon usage and gene function are related in sequences of Arabidopsis thaliana. Chiapello H, Lisacek F, Caboche M, Hénaut A, Gene 1998 209 C1 GC38 10.1016/S0378-1119(97)00671-9 9583944
140. Accounting for background nucleotide composition when measuring codon usage bias. Novembre JA, Mol Biol Evol 2002 19 1390 1394 12140252
141. Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Wright SI, Yau CBK, Looseley M, Meyers BC, Mol Biol Evol 2004 21 1719 1726 10.1093/molbev/msh191 15201397