期刊论文详细信息
BMC Evolutionary Biology
Rates of evolution in stress-related genes are associated with habitat preference in two Cardamine lineages
Claudio Varotto1  Luisa Bresadola1  Mingai Li1  Lino Ometto1 
[1]Department of Biodiversity and Molecular Ecology, IASMA Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010 San Michele all'Adige (TN), Italy
关键词: Cardamine;    habitat preference;    adaptive traits;    454 next generation sequencing;    Molecular evolution;   
Others  :  1141579
DOI  :  10.1186/1471-2148-12-7
 received in 2011-06-14, accepted in 2012-01-18,  发布年份 2012
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【 摘 要 】

Background

Elucidating the selective and neutral forces underlying molecular evolution is fundamental to understanding the genetic basis of adaptation. Plants have evolved a suite of adaptive responses to cope with variable environmental conditions, but relatively little is known about which genes are involved in such responses. Here we studied molecular evolution on a genome-wide scale in two species of Cardamine with distinct habitat preferences: C. resedifolia, found at high altitudes, and C. impatiens, found at low altitudes. Our analyses focussed on genes that are involved in stress responses to two factors that differentiate the high- and low-altitude habitats, namely temperature and irradiation.

Results

High-throughput sequencing was used to obtain gene sequences from C. resedifolia and C. impatiens. Using the available A. thaliana gene sequences and annotation, we identified nearly 3,000 triplets of putative orthologues, including genes involved in cold response, photosynthesis or in general stress responses. By comparing estimated rates of molecular substitution, codon usage, and gene expression in these species with those of Arabidopsis, we were able to evaluate the role of positive and relaxed selection in driving the evolution of Cardamine genes. Our analyses revealed a statistically significant higher rate of molecular substitution in C. resedifolia than in C. impatiens, compatible with more efficient positive selection in the former. Conversely, the genome-wide level of selective pressure is compatible with more relaxed selection in C. impatiens. Moreover, levels of selective pressure were heterogeneous between functional classes and between species, with cold responsive genes evolving particularly fast in C. resedifolia, but not in C. impatiens.

Conclusions

Overall, our comparative genomic analyses revealed that differences in effective population size might contribute to the differences in the rate of protein evolution and in the levels of selective pressure between the C. impatiens and C. resedifolia lineages. The within-species analyses also revealed evolutionary patterns associated with habitat preference of two Cardamine species. We conclude that the selective pressures associated with the habitats typical of C. resedifolia may have caused the rapid evolution of genes involved in cold response.

【 授权许可】

   
2012 Ometto et al; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Orr HA: The genetic theory of adaptation: a brief history. Nat Rev Genet 2005, 6:119-127.
  • [2]Nachman MW, Hoekstra HE, D'Agostino SL: The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 2003, 100:5268-5273.
  • [3]Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N, Monteiro B, Nachman MW: The molecular basis of high-altitude adaptation in deer mice. PLoS Genet 2007, 3:e45.
  • [4]Zhen Y, Ungerer MC: Relaxed selection on the CBF/DREB1 regulatory genes and reduced freezing tolerance in the southern range of Arabidopsis thaliana. Mol Biol Evol 2008, 25:2547-2555.
  • [5]Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB: 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). Genetics 2009, 183:289-298.
  • [6]Paaby AB, Blacket MJ, Hoffmann AA, Schmidt PS: Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Mol Ecol 2010, 19:760-774.
  • [7]Xia H, Camus-Kulandaivelu L, Stephan W, Tellier A, Zhang Z: Nucleotide diversity patterns of local adaptation at drought-related candidate genes in wild tomatoes. Mol Ecol 2010, 19:4144-4154.
  • [8]Storz JF, Wheat CW: Integrating evolutionary and functional approaches to infer adaptation at specific loci. Evolution 2010, 64:2489-2509.
  • [9]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: Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 2003, 302:1960-1963.
  • [10]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: A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 2005, 3:e170.
  • [11]Oetjen K, Reusch TBH: Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Mol Ecol 2007, 16:5156-5167.
  • [12]Namroud M-C, Beaulieu J, Juge N, Laroche J, Bousquet J: Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Mol Ecol 2008, 17:3599-3613.
  • [13]Gossmann TI, Song B-H, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A: Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol Biol Evol 2010, 27:1822-1832.
  • [14]Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA: Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 2010, 6:e1000862.
  • [15]Körner C: Alpine plant life. Functional plant ecology of high mountain ecosystems. 2nd edition. Berlin, Germany: Springer; 2003.
  • [16]Zhen Y, Ungerer MC: Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana. New Phytol 2008, 177:419-427.
  • [17]Alexander JM, Kueffer C, Daehler CC, Edwards PJ, Pauchard A, Seipel T, MIREN Consortium: Assembly of nonnative floras along elevational gradients explained by directional ecological filtering. Proc Natl Acad Sci USA 2011, 108:656-661.
  • [18]Crimmins SM, Dobrowski SZ, Greenberg JA, Abatzoglou JT, Mynsberge AR: Changes in climatic water balance drive downhill shifts in plant species' optimum elevations. Science 2011, 331:324-327.
  • [19]Montesinos-Navarro A, Wig J, Pico FX, Tonsor SJ: Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytol 2011, 189:282-294.
  • [20]Hannah MA, Heyer AG, Hincha DK: A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 2005, 1:e26.
  • [21]Vogel JT, Zarka DG, van Buskirk HA, Fowler SG, Thomashow MF: Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 2005, 41:195-211.
  • [22]Ruelland E, Vaultier M-N, Zachowski A, Hurry V: Cold signalling and cold acclimation in plants. Adv Bot Res 2009, 49:35-150.
  • [23]Streb P, Shang W, Feierabend J, Bligny R: Divergent strategies of photoprotection in high-mountain plants. Planta 1998, 207:313-324.
  • [24]Germino M, Smith W: High resistance to low-temperature photoinhibition in two alpine, snowbank species. Physiol Plantarum 2000, 110:89-95.
  • [25]Frohnmeyer H, Staiger D: Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 2003, 133:1420-1428.
  • [26]Streb P, Aubert S, Gout E, Bligny R: 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. Physiol Plantarum 2003, 118:96-104.
  • [27]Ikeda H, Fujii N, Setoguchi H: Molecular evolution of phytochromes in Cardamine nipponica (Brassicaceae) suggests the involvement of PHYE in local adaptation. Genetics 2009, 182:603-614.
  • [28]Aeschimann D, Lauber K, Moser DM, Theurillat J-P: Flora Alpina. Bern, Switzerland: Haupt Verlag; 2004.
  • [29]Kimata M: Comparative Studies on the Reproductive Systems of Cardamine flexuosa, C. impatiens, C. scutata, and C. lyrata, Cruciferae. Bot Mag Tokyo 1983, 96:299-312.
  • [30]Kucera J, Lihova J, Marhold K: Taxonomy and phylogeography of Cardamine impatiens and C. pectinata (Brassicaceae). Bot J Linn Soc 2006, 152:169-195.
  • [31]Lihova J, Carlsen T, Brochmann C, Marhold K: Contrasting phylogeographies inferred for the two alpine sister species Cardamine resedifolia and C. alpina (Brassicaceae). J Biogeogr 2009, 36:104-120.
  • [32]Bailey CD, Koch MA, Mayer M, Mummenhoff K, O'Kane SL, Warwick SI, Windham MD, Al-Shehbaz IA: Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 2006, 23:2142-2160.
  • [33]Couvreur TLP, Franzke A, Al-Shehbaz IA, Bakker FT, Koch MA, Mummenhoff K: Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol Biol Evol 2010, 27:55-71.
  • [34]Holm S: A Simple Sequentially Rejective Multiple Test Procedure. Scand J Statist 1979, 6:65-70.
  • [35]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591.
  • [36]Eisenberg E, Levanon EY: Human housekeeping genes are compact. Trends Genet 2003, 19:362-365.
  • [37]Seoighe C, Gehring C, Hurst LD: Gametophytic selection in Arabidopsis thaliana supports the selective model of intron length reduction. PLoS Genet 2005, 1:e13.
  • [38]Ingvarsson PK: Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Mol Biol Evol 2007, 24:836-844.
  • [39]Colinas J, Schmidler SC, Bohrer G, Iordanov B, Benfey PN: Intergenic and genic sequence lengths have opposite relationships with respect to gene expression. PLoS ONE 2008, 3:e3670.
  • [40]Camiolo S, Rau D, Porceddu A: Mutational biases and selective forces shaping the structure of Arabidopsis genes. PLoS ONE 2009, 4:e6356.
  • [41]Chan ET, Quon GT, Chua G, Babak T, Trochesset M, Zirngibl RA, Aubin J, Ratcliffe MJH, Wilde A, Brudno M, Morris QD, Hughes TR: Conservation of core gene expression in vertebrate tissues. J Biol 2009, 8:33. BioMed Central Full Text
  • [42]Zheng-Bradley X, Rung J, Parkinson H, Brazma A: Large scale comparison of global gene expression patterns in human and mouse. Genome Biol 2010, 11:R124. BioMed Central Full Text
  • [43]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: Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower. Proc Natl Acad Sci USA 2010, 107:22570-22575.
  • [44]Jiao Y, Ma L, Strickland E, Deng XW: Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell 2005, 17:3239-3256.
  • [45]Small R, Cronn R, Wendel J: Use of nuclear genes for phylogeny reconstruction in plants. Aust Syst Bot 2004, 17:145-170.
  • [46]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: Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 2005, 21:650-659.
  • [47]Hill WG, Robertson A: The effect of linkage on limits to artificial selection. Genet Res 1966, 8:269-294.
  • [48]Kliman RM, Hey J: Hill-Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genet Res 2003, 81:89-90.
  • [49]Betancourt AJ, Presgraves DC: Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci USA 2002, 99:13616-13620.
  • [50]Marais G, Mouchiroud D, Duret L: Neutral effect of recombination on base composition in Drosophila. Genet Res 2003, 81:79-87.
  • [51]Carlsen T, Bleeker W, Hurka H, Elven R, Brochmann C: Biogeography and phylogeny of Cardamine (Brassicaceae). Ann Mo Bot Gard 2009, 96:215-236.
  • [52]Andreasen K, Baldwin BG: Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S-26S rDNA internal and external transcribed spacers. Mol Biol Evol 2001, 18:936-944.
  • [53]Smith SA, Donoghue MJ: Rates of molecular evolution are linked to life history in flowering plants. Science 2008, 322:86-89.
  • [54]Müller K, Albach DC: Evolutionary rates in Veronica L. (Plantaginaceae): disentangling the influence of life history and breeding system. J Mol Evol 2010, 70:44-56.
  • [55]Whittle C-A, Johnston MO: Broad-scale analysis contradicts the theory that generation time affects molecular evolutionary rates in plants. J Mol Evol 2003, 56:223-233.
  • [56]Charlesworth D, Wright SI: Breeding systems and genome evolution. Curr Opin Genet Dev 2001, 11:685-690.
  • [57]Lanfear R, Welch JJ, Bromham L: Watching the clock: studying variation in rates of molecular evolution between species. Trends Ecol Evol 2010, 25:495-503.
  • [58]Charlesworth B: Fundamental concepts in genetics: Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 2009.
  • [59]Presgraves DC: Recombination enhances protein adaptation in Drosophila melanogaster. Curr Biol 2005, 15:1651-1656.
  • [60]Stoletzki N, Eyre-Walker A: The positive correlation between dN/dS and dS in mammals is due to runs of adjacent substitutions. Mol Biol Evol 2011, 28:1371-1380.
  • [61]Li J, Zhang Z, Vang S, Yu J, Wong GK-S, Wang J: Correlation between Ka/Ks and Ks is related to substitution model and evolutionary lineage. J Mol Evol 2009, 68:414-423.
  • [62]Kryazhimskiy S, Plotkin JB: The population genetics of dN/dS. PLoS Genet 2008, 4:e1000304.
  • [63]Wolf JBW, Künstner A, Nam K, Jakobsson M, Ellegren H: Nonlinear dynamics of nonsynonymous (dN) and synonymous (dS) substitution rates affects inference of selection. Genome Biol Evol 2009, 1:308-319.
  • [64]The Arabidopsis Information Resource [http://www.arabidopsis.org] webcite
  • [65]Kreps J, Wu Y, Chang H, Zhu T, Wang X, Harper J: Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 2002, 130:2129-2141.
  • [66]Shinozaki K, Yamaguchi-Shinozaki K, Seki M: Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 2003, 6:410-417.
  • [67]Swindell WR, Huebner M, Weber AP: Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 2007, 8:125. BioMed Central Full Text
  • [68]Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y: Responses of the plasma membrane to low temperatures. Physiol Plantarum 2006, 126:81-89.
  • [69]Ingvarsson PK: Natural selection on synonymous and nonsynonymous mutations shapes patterns of polymorphism in Populus tremula. Mol Biol Evol 2010, 27:650-660.
  • [70]Slotte T, Foxe JP, Hazzouri KM, Wright SI: Genome-wide evidence for efficient positive and purifying selection in Capsella grandiflora, a plant species with a large effective population size. Mol Biol Evol 2010, 27:1813-1821.
  • [71]Strasburg JL, Scotti-Saintagne C, Scotti I, Lai Z, Rieseberg LH: Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species. Mol Biol Evol 2009, 26:1341-1355.
  • [72]Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL: The cost of inbreeding in Arabidopsis. Nature 2002, 416:531-534.
  • [73]Foxe JP, Dar V-U-N, Zheng H, Nordborg M, Gaut BS, Wright SI: Selection on amino acid substitutions in Arabidopsis. Mol Biol Evol 2008, 25:1375-1383.
  • [74]Hamblin MT, Casa AM, Sun H, Murray SC, Paterson AH, Aquadro CF, Kresovich S: Challenges of detecting directional selection after a bottleneck: lessons from Sorghum bicolor. Genetics 2006, 173:953-964.
  • [75]Roth C, Liberles DA: A systematic search for positive selection in higher plants (Embryophytes). BMC Plant Biol 2006, 6:12. BioMed Central Full Text
  • [76]Strasburg JL, Kane NC, Raduski AR, Bonin A, Michelmore R, Rieseberg LH: Effective population size is positively correlated with levels of adaptive divergence among annual sunflowers. Mol Biol Evol 2011, 28:1569-1580.
  • [77]McDonald JH, Kreitman M: Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991, 351:652-654.
  • [78]Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
  • [79]Maere S, de Bodt S, Raes J, Casneuf T, van Montagu M, Kuiper M, van de Peer Y: Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 2005, 102:5454-5459.
  • [80]Tuskan GA, Difazio S, Jansson S, et al.: The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313:1596-1604.
  • [81]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: The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449:463-467.
  • [82]Moore RC, Purugganan MD: The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 2005, 8:122-128.
  • [83]Thomashow MF: So what's new in the field of plant cold acclimation? Lots! Plant Physiol 2001, 125:89-93.
  • [84]Champ KI, Febres VJ, Moore GA: The role of CBF transcriptional activators in two Citrus species (Poncirus and Citrus) with contrasting levels of freezing tolerance. Physiol Plantarum 2007, 129:529-541.
  • [85]Pennycooke JC, Cheng H, Roberts SM, Yang Q, Rhee SY, Stockinger EJ: The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements. Plant Mol Biol 2008, 67:483-497.
  • [86]Tondelli A, Francia E, Barabaschi D, Pasquariello M, Pecchioni N: Inside the CBF locus in Poaceae. Plant Sci 2011, 180:39-45.
  • [87]Huang L, Grammatikakis N, Yoneda M, Banerjee SD, Toole BP: Molecular characterization of a novel intracellular hyaluronan-binding protein. J Biol Chem 2000, 275:29829-29839.
  • [88]Lazzaroni JC, Germon P, Ray MC, Vianney A: The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 1999, 177:191-197.
  • [89]Verbruggen N, Hermans C, Schat H: Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 2009, 181:759-776.
  • [90]Vergnano Gambi O, Gabbrielli R, Pancaro L: Nickel, chromium and cobalt in plants from italian serpentine areas. Acta Oecol-Oec Plant 1982, 3:291-306.
  • [91]Mikkelsen MD, Petersen BL, Olsen CE, Halkier BA: Biosynthesis and metabolic engineering of glucosinolates. Amino Acids 2002, 22:279-295.
  • [92]Jones C, Dancer J, Smith A, Abell C: Evidence for the pathway to pantothenate in plants. Can J Chem 1994, 72:261-263.
  • [93]Ludwig-Müller J: Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 2011, 62:1757-1773.
  • [94]Wang L, Allmann S, Wu J, Baldwin IT: 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. Plant Physiol 2008, 146:904-915.
  • [95]Chico JM, Chini A, Fonseca S, Solano R: JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 2008, 11:486-494.
  • [96]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: The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 2011, 23:701-715.
  • [97]Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA: Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 2008, 146:952-964.
  • [98]Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein DJ, Gershenzon J: The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 2001, 13:2793-2807.
  • [99]Haugen R, Steffes L, Wolf J, Brown P, Matzner S, Siemens DH: Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching. Oikos 2008, 117:231-244.
  • [100]Zehnder CB, Stodola KW, Joyce BL, Egetter D, Cooper RJ, Hunter MD: Elevational and seasonal variation in the foliar quality and arthropod community of Acer pensylvanicum. Environ Entomol 2009, 38:1161-1167.
  • [101]Reynolds B, Crossley D: Spatial variation in herbivory by forest canopy arthropods along an elevation gradient. Environ Entomol 1997, 26:1232-1239.
  • [102]Suzuki S: Leaf phenology, seasonal changes in leaf quality and herbivory pattern of Sanguisorba tenuifolia at different altitudes. Oecologia 1998, 117:169-176.
  • [103]Hengxiao G, McMillin J, Wagner M, Zhou J, Zhou Z, Xu X: Altitudinal variation in foliar chemistry and anatomy of yunnan pine, Pinus yunnanensis, and pine sawfly (Hym., Diprionidae) performance. J Appl Entomol 1999, 123:465-471.
  • [104]Louda S, Rodman J: Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, bittercress). J Ecol 1996, 84:229-237.
  • [105]Pnueli L, Liang H, Rozenberg M, Mittler R: Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 2003, 34:185-201.
  • [106]Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R: Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 2005, 17:268-281.
  • [107]Kim J, Choi D, Kende H: The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 2003, 36:94-104.
  • [108]Kim J, Kende H: A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci USA 2004, 101:13374-13379.
  • [109]Chen I-P, Haehnel U, Altschmied L, Schubert I, Puchta H: The transcriptional response of Arabidopsis to genotoxic stress-a high-density colony array study (HDCA). Plant J 2003, 35:771-786.
  • [110]Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV: Selection in the evolution of gene duplications. Genome Biol 2002, 3:RESEARCH0008.
  • [111]Fowler SG, Thomashow MF: Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 2002, 14:1675-1690.
  • [112]Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL: BLAST+: architecture and applications. BMC Bioinformatics 2009, 10:421. BioMed Central Full Text
  • [113]Tatusov RL, Koonin EV, Lipman DJ: A genomic perspective on protein families. Science 1997, 278:631-637.
  • [114]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: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
  • [115]Robinson C, Ellis RJ: Transport of proteins into chloroplasts. Partial purification of a chloroplast protease involved in the processing of important precursor polypeptides. Eur J Biochem 1984, 142:337-342.
  • [116]Soll J, Tien R: Protein translocation into and across the chloroplastic envelope membranes. Plant Mol Biol 1998, 38:191-207.
  • [117]von Heijne G, Steppuhn J, Herrmann RG: Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 1989, 180:535-545.
  • [118]Emanuelsson O, Nielsen H, von Heijne G: ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 1999, 8:978-984.
  • [119]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: Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 2004, 135:745-755.
  • [120]Chinnusamy V, Ohta M, Kanrar S, Lee B-H, Hong X, Agarwal M, Zhu J-K: ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Gene Dev 2003, 17:1043-1054.
  • [121]Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF: Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 1998, 16:433-442.
  • [122]Jaglo-Ottosen KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF: Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 2001, 127:910-917.
  • [123]Medina J, Bargues M, Terol J, Pérez-Alonso M, Salinas J: 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. Plant Physiol 1999, 119:463-470.
  • [124]Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK: The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Gene Dev 2001, 15:912-924.
  • [125]Xin Z, Browse J: eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc Natl Acad Sci USA 1998, 95:7799-7804.
  • [126]Gilmour SJ, Fowler SG, Thomashow MF: Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 2004, 54:767-781.
  • [127]Lee B-H, Henderson DA, Zhu J-K: The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 2005, 17:3155-3175.
  • [128]Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D'Angelo C, Bornberg-Bauer E, Kudla J, Harter K: The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 2007, 50:347-363.
  • [129]Yang Z, Nielsen R, Goldman N, Pedersen A: Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155:431-449.
  • [130]Yang Z, Nielsen R: Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17:32-43.
  • [131]Yang Z: Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 1998, 15:568-573.
  • [132]Yang Z, Wong WSW, Nielsen R: Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005, 22:1107-1118.
  • [133]Storey J: A direct approach to false discovery rates. J Roy Stat Soc B 2002, 64:479-498.
  • [134]R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2009.
  • [135]Qiu S, Bergero R, Zeng K, Charlesworth D: Patterns of codon usage bias in Silene latifolia. Mol Biol Evol 2011, 28:771-780.
  • [136]Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU: A gene expression map of Arabidopsis thaliana development. Nat Genet 2005, 37:501-506.
  • [137]Ikemura T: 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. J Mol Biol 1981, 151:389-409.
  • [138]CodonW [http://codonw.sourceforge.net/] webcite
  • [139]Chiapello H, Lisacek F, Caboche M, Hénaut A: Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene 1998, 209:GC1-GC38.
  • [140]Novembre JA: Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol 2002, 19:1390-1394.
  • [141]Wright SI, Yau CBK, Looseley M, Meyers BC: Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol Biol Evol 2004, 21:1719-1726.
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