| 研究生: |
王麗雅 Wang, Li-Ya |
|---|---|
| 論文名稱: |
台灣筷子芥屬植物小分子熱休克基因家族的分子演化研究 Molecular evolution of the small heat shock protein gene family in Arabidopsis in Taiwan |
| 指導教授: |
蔣鎮宇
Chiang, Tzen-Yuh |
| 學位類別: |
碩士 Master |
| 系所名稱: |
生物科學與科技學院 - 生命科學系 Department of Life Sciences |
| 論文出版年: | 2006 |
| 畢業學年度: | 94 |
| 語文別: | 中文 |
| 論文頁數: | 77 |
| 中文關鍵詞: | 制衡性天擇 、多型性 、基因重複 、分子演化 、小分子熱休克蛋白 、筷子芥屬 、熱逆境 |
| 外文關鍵詞: | heat stress, small heat shock protein, molecular evolution, gene duplication, Arabidopsis |
| 相關次數: | 點閱:173 下載:3 |
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大部分生物面臨熱休克壓力時,均有合成熱休克蛋白的情況,但只有植物在熱休克反應下,會合成多個種類的小分子熱休克蛋白。本研究檢測此些分子熱休克蛋白基因家族不同類型的成員間,其遺傳變異程度與分佈模式、受到何種演化力量的影響與差異。根據研究結果發現,在筷子芥屬小分子熱休克蛋白基因家族中,不同類型的sHSP (small heat shock protein)基因在基因譜系圖上各自形成單系群的形式,顯示早在種化之前其各自演化過程便已各自獨立。細胞質第一型(sHsp17.6、sHsp17.4)與內質網型sHsp22,主要是受到balancing selection的影響,在基因片段與基因譜系圖上均呈現保留高度多型性(polymorphism)的情況。且筷子芥屬細胞質第一型sHSP基因可能是藉由多次gene duplication的機制產生多個不同的基因片段。筷子芥屬小分子熱休克蛋白基因家族中,表現於胞器的葉綠體型與粒線體型的sHSP基因片段,其Tajima’s D值呈現顯著負值,由此可知此二類sHSP基因受到強烈的負向天擇作用,核酸序列的變異程度低,可能是因為此二種作用在胞器的基因,在維持植物細胞的正常生理功能上,扮演十分重要的角色,基因序列一旦發生變異就可能造成胺基酸序列的改變,影響蛋白質功能與作用,序列高度保守的特性反映出受到天擇的強烈影響。而在阿拉伯芥細胞質第二型(sHsp17.6II) 基因中,可以發現此基因受到顯著負向天擇的影響,但是在筷子芥屬其他物種裡有不一的情況出現,Arabidopsis halleri ssp. gemmifera 與 Arabidopsis lyrata spp. kamtschatica.的sHsp17.6II有偏向balancing selection的情況,此結果顯示出在物種分化後,同源基因在不同物種中受到不同天擇效應的影響。
Although all the organisms synthesize HSPs (heat shock proteins) upon heat-shock, plants show unique feature of heat-shock response by synthesizing multiple classes of small HSPs (sHSPs). This study focuses on molecular evolution and expression patterns of the genes of the small heat shock proteins in Arabidopsis thaliana and other Arabidopsis species. Natural selection hypothesis was tested and modes of natural selection were identified. Evolutionary genetic analyses revealed that phylogenetic analyses revealed that the sHSP gene family in plants has experienced multiple gene duplications. It is clear that the evolution of the sHSPs rely on knowledge of the evolutionary relationships of the organisms from which the sHSP genes were isolated. Significantly negative Tajima’s D values are detected in the two members of sHSP gene family in Arabidopsis, chloroplast (sHsp21), and mitochondria (sHsp23.5), indicating effects of negative selection. This study demonstrates that these two organelle-localized sHSPs play an important role in molecular adaptation. In contrast, the cytosol I ( sHsp17.6, sHsp17.4) class and the ER (sHsp22) genes are under balancing selection, due to excessive high frequency polymorphisms among nucleotide sequences. The cytosol II gene (sHsp17.6II) is under negative selection in Arabidopsis thaliana, while driven by balancing selection in Arabidopsis halleri ssp. gemmifera and Arabidopsis lyrata spp. kamtschatica. Apparently, different evolutionary forces shaped the sHSP17.6II gene in different Arabidopsis.
Ahn, Y. J., Claussen, K., Zimmerman, J. L. (2004). Genotypic differences in the heat-shock response and thermotolerance in four potato cultivars. Plant Science 166: 901-911.
Azzoni, A. R., Tada, S. F. S., Rosselli, L. K., Paula, D. P., Catani, C. F., Sabino, A. A., Barbosa, J., Guimaraes, B. G., Eberlin, M. N., Medrano, F. J., Souza, A. P. (2004). Expression and purification of a small heat shock protein from the plant pathogen Xylella fastidiosa. Protein Expression and Purification 33: 297-303.
Bakker, E. G., Downs, C. A., Heckathorn, S. A. (2006). Distribution of genetic variation within and among local populations of Arabidopsis thaliana over its species range. Molecular Ecology 15: 1405-1418.
Barua, D., Chang, S. H., Hudson, M. E., Kwan, W. K., Li, J. Q., Estes, B., Knoll, D., Shi, L., Zhu, T. (2003). Variation in chloroplast small heat-shock protein function is a major determinant of variation in thermotolerance of photosynthetic electron transport among ecotypes of Chenopodium album. Functional Plant Biology 30: 1071-1079.
Barua, D. and S. A. Heckathorn (2006). The interactive effects of light and temperature on heat-shock protein accumulation in Solidago altissima (Asteraceae) in the field and laboratory. American Journal of Botany 93(1): 102-109.
Baum, D. A., Yoon, H. S., Oldham, R. L. (2005). Molecular evolution of the transcription factor LEAFY in Brassicaceae. Molecular Phylogenetics and Evolution 37: 1-14.
Beilstein, M. A., Al-Shehbaz, I. A., Kellogg, E. A. (2006). Brassicaceae phylogeny and trichome evolution. American Journal of Botany 93: 607-619.
Bergelson, J., E. Stahl, E., Dudek, S., Kreitman, M. (1998). Genetic variation within and among populations of Arabidopsis thaliana. Genetics 148: 1311-1323.
Chen, W. Q. J., Chang, S. H., Hudson, M. E., Kwan, W. K., Li, J. Q., Estes, B., Knoll, D., Shi, L., Zhu, T. (2005). Contribution of transcriptional regulation to natural variations in Arabidopsis. Genome Biology 6.
Clark, J. I. and P. J. Muchowski (2000). Small heat-shock proteins and their potential role in human disease. Current Opinion in Structural Biology 10(1): 52-59.
Clauss, M. J. and T. Mitchell-Olds (2004). Functional divergence in tandemly duplicated Arabidopsis thaliana trypsin inhibitor genes. Genetics 166(3): 1419-1436.
de Meaux, J., Goebel, U., Pop, A., Mitchell-Olds, T. (2005). Allele-specific assay reveals functional variation in the chalcone synthase promoter of Arabidiopsis thaliana that is compatible with neutral evolution. Plant Cell 17: 676-690.
de Meaux, J. and T. Mitchell-Olds (2003). Evolution of plant resistance at the molecular level: ecological context of species interactions. Heredity 91(4): 345-352.
Dejong, W. W., Leunissen, J. A. M., Voorter, C. E. M. (1993). Evolution of the Alpha-Crystallin Small Heat-Shock Protein Family. Molecular Biology and Evolution 10: 103-126.
Dobes, C., Mitchell-Olds, T., Koch, M. A. (2004). Intraspecific diversification in North American Boechera stricta (=Arabis drummondii), Boechera xdivaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers - An integrative approach. American Journal of Botany 91: 2087-2101.
Dobes, C. H., Mitchell-Olds, T., Koch, M. A. (2004). Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. x divaricarpa, and A-holboellii (Brassicaceae). Molecular Ecology 13: 349-370.
Eichler, T. E., Ransom, R. F., Smoyer, W. E. (2005). Differential induction of podocyte heat shock proteins by prolonged single and combination toxic metal exposure. Toxicological Sciences 84: 120-128.
Eifert, C., Burgio, M. R., Bennett, P. M., Salerno, J. C., Koretz, J. F. (2005). N-terminal control of small heat shock protein oligomerization: Changes in aggregate size and chaperone-like function. Biochimica Et Biophysica Acta-Proteins and Proteomics 1748: 146-156.
Erschadi, S., Haberer, G., Schoniger, M., Torres-Ruiz, R. A. (2000). Estimating genetic diversity of Arabidopsis thaliana ecotypes with amplified fragment length polymorphisms (AFLP). Theoretical and Applied Genetics 100: 633-640.
Fan, C. Y., Ren, H. Y., Lee, P., Caplan, A. J., Cyr, D. M. (2005). The type I Hsp40 zinc finger-like region is required for Hsp70 to capture non-native polypeptides from Ydj1. Journal of Biological Chemistry 280: 695-702.
Finnie, C., Steenholdt, T., Noguera, O. R., Knudsen, S., Larsen, J., Brinch-Pedersen, H., Holm, P. B., Olsen, O., Svensson, B. (2004). Environmental and transgene expression effects on the barley seed proteome. Phytochemistry 65: 1619-1627.
Gomez, E., Royo, J., Guo, Y., Thompson, R., Hueros, G. (2002). Establishment of cereal endosperm expression domains: Identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell 14: 599-610.
Gonzalez-Martinez, S. C., Ersoz, E., Brown, G. R., Wheeler, N. C., Neale, D. B. (2006). DNA sequence variation and selection of tag single-nucleotide polymorphisms at candidate genes for drought-stress response in Pinus taeda L. Genetics 172: 1915-1926.
Goss, E. M., Kreitman, M., Bergelson, J. (2005). Genetic diversity, recombination and cryptic clades in Pseudomonas viridiflava infecting natural populations of Arabidopsis thaliana. Genetics 169: 21-35.
Guan, J. C., Jinn, T. L., Yeh, C. H., Feng, S. P., Chen, Y. M., Lin, C. Y (2004). Characterization of the genomic structures and selective expression profiles of nine class I small heat shock protein genes clustered on two chromosomes in rice (Oryza sativa L.). Plant Molecular Biology 56: 795-809.
Gustavsson, N., Harndahl, U., Emanuelsson, A., Roepstorff, P., Sundby, C. (1999). Methionine sulfoxidation of the chloroplast small heat shock protein and conformational changes in the oligomer. Protein Science 8: 2506-2512.
Haubold, B., Kroymann, J., Ratzka, A., Mitchell-Olds, T., Wiehe, T. (2002). Recombination and gene conversion in a 170-kb genomic region of Arabidopsis thaliana. Genetics 161: 1269-1278.
Heckathorn, S. A., Downs, C. A., Sharkey, T. D., Coleman, J. S. (1998). The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiology 116: 439-444.
Heckathorn, S. A., Mueller, J. K., LaGuidice, S., Zhu, B., Barrett, T., Blair, B., Dong, Y. (2004). Chloroplast small heat-shock proteins protect photosynthesis during heavy metal stress. American Journal of Botany 91: 1312-1318.
Hong, S. W., Lee, U., Vierling, E. (2003). Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiology 132: 757-767.
Iba, K. (2002). Acclimative response to temperature stress in higher plants: Approaches of gene engineering for temperature tolerance. Annual Review of Plant Biology 53: 225-245.
Ito, H., Iwamoto, I., Inaguma, Y., Takizawa, T., Nagata, K., Asano, T., Kato, K. (2005). Endoplasmic reticulum stress induces the phosphorylation of small heat shock protein, Hsp27. Journal of Cellular Biochemistry 95: 932-941.
Johnston, J. S., Pepper, A. E., Hall, A. E., Chen, Z. J., Hodnett, G., Drabek, J., Lopez, R., Price, H. J. (2005). Evolution of genome size in Brassicaceae. Annals of Botany 95: 229-235.
Katoh, Y., Fujimoto, M., Nakamura, K., Inouye, S., Sugahara, K., Izu, H., Nakai, A. (2004). Hsp25, a member of the Hsp30 family, promotes inclusion formation in response to stress. Febs Letters 565: 28-32.
Kerk, D., Bulgrien, J., Smith, D. W., Gribskov, M. (2003). Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiology 131: 1209-1219.
Kim, K. P., Joe, M. K., Hong, C. B. (2004). Tobacco small heat-shock protein, NtHSP18.2, has broad substrate range as a molecular chaperone. Plant Science 167: 1017-1025.
Kim, Y. (2006). Allele frequency distribution under recurrent selective sweeps. Genetics 172: 1967-1978.
Kliebenstein, D. J., Kroymann, J., Mitchell-Olds, T. (2005). The glucosinolate-myrosinase system in an ecological and evolutionary context. Current Opinion in Plant Biology 8: 264-271.
Knight, C. A. and D. D. Ackerly (2003). Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: congeneric species from desert and coastal environments. New Phytologist 160(2): 337-347.
Koch, M. A., Dobes, C., Matschinger, M., Bleeker, W., Vogel, J., Kiefer, M., Mitchell-Olds, T. (2005). Evolution of the trnF(GAA) gene in Arabidopsis relatives and the Brassicaceae family: Monophyletic origin and subsequent diversification of a plastidic pseudogene. Molecular Biology and Evolution 22: 1032-1043.
Koch, M. A., Dobes, C., Mitchell-Olds, T. (2003). Multiple hybrid formation in natural populations: Concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in north American Arabis divaricarpa (Brassicaceae). Molecular Biology and Evolution 20: 338-350.
Koch, M. A., Haubold, B., Mitchell-Olds, T. (2000). Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Molecular Biology and Evolution 17: 1483-1498.
Hong, S. W. and E. Vierling (2000). Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proceedings of the National Academy of Sciences of the United States of America 97: 4392-4397.
Kroymann, J., Donnerhacke, S., Schnabelrauch, D., Mitchell-Olds, T. (2003). Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proceedings of the National Academy of Sciences of the United States of America 100: 14587-14592.
Kroymann, J. and T. Mitchell-Olds (2005). Epistasis and balanced polymorphism influencing complex trait variation. Nature 435: 95-98.
Kuittinen, H., de Haan, A. A., Vogl, C., Oikarinen, S., Leppala, J., Koch, M., Mitchell-Olds, T., Langley, C. H., Savolainen, O. (2004). Comparing the linkage maps of the close relatives Arabidopsis lyrata and A-thaliana. Genetics 168: 1575-1584.
Laksanalamai, P. and F. T. Robb (2004). Small heat shock proteins from extremophiles: a review. Extremophiles 8: 1-11.
Larkindale, J., Hall, J. D., Knight, M. R., Vierling, E. (2005). Heat stress phenotypes of arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiology 138: 882-897.
Lee, G. J., Roseman, A. M., Saibil, H. R., Vierling, E. (1997). A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. Embo Journal 16: 659-671.
Lee, G. J. and E. Vierling (2000). A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiology 122: 189-197.
Lee, U., Wie, C., Escobar, M., Williams, B., Hong, S. W., Vierling, E. (2005). Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. Plant Cell 17: 559-571.
Lopez-Matas, M. A., Nunez, P., Soto, A., Allona, I., Casado, R., Collada, C., Guevara, M. A., Argoncillo, C., Gomez, L. (2004). Protein cryoprotective activity of a cytosolic small heat shock protein that accumulates constitutively in chestnut stems and is up-regulated by low and high temperatures. Plant Physiology 134: 1708-1717.
Lysak, M. A., Berr, A., Pecinka, A., Schmidt, R., McBreen, K., Schubert, I. (2006). Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proceedings of the National Academy of Sciences of the United States of America 103: 5224-5229.
Malik, M. K., Slovin, J. P., Hwang, C. H., Zimmerman, J. L. (1999). Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance. Plant Journal 20: 89-99.
McSteen, P. (2006). Branching out: The ramosa pathway and the evolution of grass inflorescence morphology. Plant Cell 18: 518-522.
Miroshnichenko, S., Tripp, J., zur Nieden, U., Neumann, D., Conrad, U., Manteuffel, R. (2005). Immunomodulation of function of small heat shock proteins prevents their assembly into heat stress granules and results in cell death at sublethal temperatures. Plant Journal 41: 269-281.
Mitchell-Olds, T. (2001). Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends in Ecology & Evolution 16: 693-700.
Mitchell-Olds, T. and C. A. Knight (2002). Evolution: Chaperones as buffering agents? Science 296: 2348-2349.
Murakami, T., Matsuba, S., Funatsuki, H., Kawaguchi, K., Saruyama, H., Tanida, M., Sato, Y. (2004). Over-expression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Molecular Breeding 13: 165-175.
Nam, M. H., Heo, E. J., Kim, J. Y., Kim, S. I., Kwon, K. H., Seo, J. B., Kwon, O., Jong, S. Y., Park, Y. M. (2003). Proteome analysis of the responses of Panax ginseng C.A. Meyer leaves to high light: Use of electrospray ionization quadrupole-time of flight mass spectrometry and expressed sequence tag data. Proteomics 3: 2351-2367.
Neta-Sharir, I., Isaacson, T., Lurie, S., Weiss, D (2005). Dual role for tomato heat shock protein 21: Protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17: 1829-1838.
O'Kane, S. L. and I. A. Al-Shehbaz (2003). Phylogenetic position and generic limits of Arabidopsis (Brassicaceae) based on sequences of nuclear ribosomal DNA. Annals of the Missouri Botanical Garden 90: 603-612.
Opperman, R., Emmanuel, E., Levy, A. A. (2004). The effect of sequence divergence on recombination between direct repeats in Arabidopsis. Genetics 168: 2207-2215.
Piper, P. (1998). Differential role of Hsps and trehalose in stress tolerance. Trends in Microbiology 6: 43-44.
Ramos-Onsins, S. E., Stranger, B. E., Mitchell-Olds, T., Aguade, M. (2004). Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166: 373-388.
Rhoads, D. M., White, S. J., Zhou, Y., Muralidharan, M., Elthon, T. E. (2005). Altered gene expression in plants with constitutive expression of a mitochondrial small heat shock protein suggests the involvement of retrograde regulation in the heat stress response. Physiologia Plantarum 123: 435-444.
Sanmiya, K., Suzuki, K., Egawa, Y., Shono, M. (2004). Mitochondrial small heat-shock protein enhances thermotolerance in tobacco plants. Febs Letters 557: 265-268.
Sanmiya, K., Suzuki, K., Tagiri, A., Egawa, Y., Shono, M. (2005). Ovule-specific expression of the genes for mitochondrial and endoplasmic reticulum localized small heat-shock proteins in tomato flower. Plant Cell Tissue and Organ Culture 83: 245-250.
Scharf, K. D., Siddique, M., Vierling, E. (2001). The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress & Chaperones 6: 225-237.
Schein, M., Yang, Z. H., Mitchell-Olds, T., Schmid, K. J. (2004). Rapid evolution of a pollen-specific oleosin-like gene family from Arabidopsis thaliana and closely related species. Molecular Biology and Evolution 21: 659-669.
Schmid, K. J., Ramos-Onsins, S., Ringys-Beckstein, H., Weisshaar, B., Mitchell-Olds, T. (2005). A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism. Genetics 169: 1601-1615.
Schranz, M. E., Dobes, C., Koch, M. A., Mitchell-Olds, T. (2005). Sexual reproduction, hybridization, apomixis, and polyploidization in the genus Boechera (Brassicaceae). American Journal of Botany 92: 1797-1810.
Seminario, L., Berkowitz, P., Hu, P., Rubenstein, D. (2005). Phosphorylation and subcellular localization of the murine small heat shock protein hsp 25 as a function of cell continence. Journal of Investigative Dermatology 124: A29-A29.
Shimizu, K. K., Cork, J. M., Caicedo, A. L., Mays, C. A., Moore, R. C., Olsen, K. M., Ruzsa, S., Coop, G., Bustamante, C. D., Awadalla, P., Purugganan, M. D. (2004). Darwinian selection on a selfing locus. Science 306: 2081-2084.
Slatkin, M. and J. L. Pollack (2006). The concordance of gene trees and species trees at two linked loci. Genetics 172: 1979-1984.
Stechmann, A. and T. Cavalier-Smith (2003). Phylogenetic analysis of eukaryotes using heat-shock protein Hsp90. Journal of Molecular Evolution 57: 408-419.
Stranger, B. E. and T. Mitchell-Olds (2005). Nucleotide variation at the myrosinase-encoding locus, TGG1, and quantitative myrosinase enzyme activity variation in Arabidopsis thaliana. Molecular Ecology 14: 295-309.
Sule, A., F. Vanrobaeys, F., Hajos, G., Van Beeumen, J., Devreese, B. (2004). Proteomic analysis of small heat shock protein isoforms in barley shoots. Phytochemistry 65: 1853-1863.
Sun, W. N., Van Montagu, M., Verbruggen, N. (2002). Small heat shock proteins and stress tolerance in plants. Biochimica Et Biophysica Acta-Gene Structure and Expression 1577: 1-9.
Sun, Y. and T. H. MacRae (2005). The small heat shock proteins and their role in human disease. Febs Journal 272: 2613-2627.
Sundby, C., Harndahl, U., Gustavsson, N., Ahrman, E., Murphy, D. J. (2005). Conserved methionines in chloroplasts. Biochimica Et Biophysica Acta-Proteins and Proteomics 1703: 191-202.
Suzuki, T. C., Krawitz, D. C., Vierling, E. (1998). The chloroplast small heat-shock protein oligomer is not phosphorylated and does not dissociate during heat stress in vivo. Plant Physiology 116: 1151-1161.
Torjek, O., Berger, D., Meyer, R. C., Mussig, C., Schmid, K. J., Sorensen, T. R., Weisshaar, B., Mitchell-Olds, T., Altmann, T. (2003). Establishment of a high-efficiency SNP-based framework marker set for Arabidopsis. Plant Journal 36: 122-140.
Vierling, E. (1991). The Roles of Heat-Shock Proteins in Plants. Annual Review of Plant Physiology and Plant Molecular Biology 42: 579-620.
Wang, W. X., Vinocur, B., Altman, A. (2003). Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218: 1-14.
Wang, W. X., Vinocur, B., Shoseyov, O., Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9: 244-252.
Waters, E. R. (2003). Molecular adaptation and the origin of land plants. Molecular Phylogenetics and Evolution 29: 456-463.
Waters, E. R. and E. Vierling (1999).a. Chloroplast small heat shock proteins: Evidence for atypical evolution of an organelle-localized protein. Proceedings of the National Academy of Sciences of the United States of America 96: 14394-14399.
Waters, E. R. and E. Vierling (1999).b. The diversification of plant cytosolic small heat shock proteins preceded the divergence of mosses. Molecular Biology and Evolution 16: 127-139.
Windsor, A. J., Reichelt, M., Figuth, A., Svatos, A., Kroymann, J., Kliebenstein, D. J., Gershenzon, J., Mitchell-Olds, T. (2005). Geographic and evolutionary diversification of glucosinolates among near relatives of Arabidopsis thaliana (Brassicaceae). Phytochemistry 66: 1321-1333.
Wright, S. I., Yau, C. B. K., Looseley, M., Meyers, B. C. (2004). Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Molecular Biology and Evolution 21: 1719-1726.
Yeh, C. H., Chen, Y. M., Lin, C. Y. (2002). Functional regions of rice heat shock protein, Oshsp16.9, required for conferring thermotolerance in Escherichia coli. Plant Physiology 128: 661-668.
Yoon, H. J., Kim, K. P., Park, S. M., Hong, C. B. (2005). Functional mode of NtHSP17.6. a cytosolic small heat-shock protein from Nicotiana tabacum. Journal of Plant Biology 48: 120-127.
Young, L. W., Wilen, R. W., Bonham-Smith, P. C. (2004). High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of Experimental Botany 55: 485-495.
Zhang, X. P. and E. Glaser (2002). Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends in Plant Science 7: 14-21.