Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum.
Studies of the resurrection plant Craterostigma plantagineum have revealed some of the mechanisms which these desiccation-tolerant plants use to survive environments with extreme dehydration and restricted seasonal water. Most resurrection plants are polyploid with large genomes, which has hindered efforts to obtain whole genome sequences and perform mutational analysis. However, the application of deep sequencing technologies to transcriptomics now permits large-scale analyses of gene expression patterns despite the lack of a reference genome. Here we use pyro-sequencing to characterize the transcriptomes of C. plantagineum leaves at four stages of dehydration and rehydration. This reveals that genes involved in several pathways, such as those required for vitamin K and thiamin biosynthesis, are tightly regulated at the level of gene expression. Our analysis also provides a comprehensive picture of the array of cellular responses controlled by gene expression that allow resurrection plants to survive desiccation.
Rodriguez
Maria C Suarez
MCS
Department of Biology, University of Copenhagen, Ole Maaloes vej. 5, 2200, Copenhagen, Denmark.
Edsgärd
Daniel
D
Department of Systems Biology, Technical University of Denmark, Kemitorvet 208, 2800 Lyngby, Denmark.
Hussain
Syed S
SS
Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Kirschallee 1, D-53115 Bonn, Germany.
Alquezar
David
D
Department of Biology, University of Copenhagen, Ole Maaloes vej. 5, 2200, Copenhagen, Denmark.
Rasmussen
Morten
M
Department of Biology, University of Copenhagen, Ole Maaloes vej. 5, 2200, Copenhagen, Denmark.
Gilbert
Thomas
T
Department of Biology, University of Copenhagen, Ole Maaloes vej. 5, 2200, Copenhagen, Denmark.
Nielsen
Bjørn H
BH
Department of Systems Biology, Technical University of Denmark, Kemitorvet 208, 2800 Lyngby, Denmark.
Bartels
Dorothea
D
Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Kirschallee 1, D-53115 Bonn, Germany.
Mundy
John
J
Department of Biology, University of Copenhagen, Ole Maaloes vej. 5, 2200, Copenhagen, Denmark.
D032181:Craterostigma / Q000235:genetics / Q000378:metabolism*; D003681:Dehydration; D020224:Expressed Sequence Tags; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D015723:Gene Library; D018749:RNA, Plant / Q000235:genetics; D017422:Sequence Analysis, DNA; D014867:Water / Q000378:metabolism
D018749:RNA, Plant; D014867:Water
Ahn, I.P., Kim, S. and Lee, Y.H. (2005) Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol. 138, 1505-1515.
Ahn, I.P., Kim, S., Lee, Y.H. and Suh, S.C. (2007) Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiol. 143, 838-848.
Alamillo, J.M., Roncarati, R., Heino, P. et al. (1994) Molecular analysis of desiccation tolerance in barley embryos and in the resurrection plant Craterostigma plantagineum. Agronomie, 2, 161-167.
Alexandersson, E., Fraysse, L., Sjövall-Larsen, S., Gustavsson, S., Fellert, M., Karlsson, M., Johanson, U. and Kjellbom, P. (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol. Biol. 59, 469-484.
Arnoux, P., Morosinotto, T., Saga, G., Bassi, R. and Pignol, D. (2009) A structural basis for the ph-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell, 21, 2036-2044.
Barrat, D. and Clark, J. (1991) Proteins arising during the late stages of embryogenesis in Pisum sativum L. Planta, 184, 14-23.
Bartels, D. (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr. Comp. Biol. 45, 696-701.
Bartels, D. and Salamini, F. (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum. A contribution to the study of drought tolerance at the molecular level. Plant Physiol. 127, 1346-1353.
Bartels, D., Schneider, K., Terstappen, G., Piatkowski, D. and Salamini, F. (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta, 181, 27-34.
Belanger, F.C., Leustek, T., Chu, B. and Kriz, A.L. (1995) Evidence for the thiamine biosynthetic pathway in higher-plant plastids and its developmental regulation. Plant Mol. Biol. 29, 809-821.
Ben-Nissan, G., Lee, J.Y., Borohov, A. and Weiss, D. (2004) GIP, a Petunia hybrida Ga-induced cysteine-rich protein: a possible role in shoot elongation and transition to flowering. Plant J. 37, 229-238.
Bernacchia, G., Schwall, G., Lottspeich, F., Salamini, F. and Bartels, D. (1995) The transketolase gene family of the resurrection plant Craterostigma plantagineum: differential expression during the rehydration phase. EMBO J. 14, 610-618.
Bernacchia, G., Salamini, F. and Bartels, D. (1996) Molecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineum. Plant Physiol. 111, 1043-1050.
Bianchi, G., Gamba, A., Murelli, C., Salamini, F. and Bartels, D. (1991) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantigineum. Plant J. 1, 355-359.
Blanc, G. and Wolfe, K.H. (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell, 16, 1647-1649.
Bockel, C., Salamini, F. and Bartels, D. (1998) Isolation and characterization of genes expressed during early events of the dehydration process in the resurrection plant Craterostigma plantagineum. J. Plant Physiol. 152, 158-166.
Boudet, J., Buitink, J., Hoekstra, F.A., Rogniaux, H., Larre, C., Satour, P. and Leprince, O. (2006) Comparative analysis of the heat stable proteome of radicles of medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol. 140, 1418-1436.
Breton, G., Danyluk, J., Charron, J.B.F. and Sarhan, F. (2003) Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and Arabidopsis. Plant Physiol. 132, 64-74.
Buitink, J., Leger, J., Guisle, I. et al. (2006) Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago Truncatula seeds. Plant J. 47, 735-750.
Chang, W., Huang, L., Shen, M., Webster, C., Burlingame, A. and Roberts, J. (2000) Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. Plant Physiol. 122, 295-318.
Charron, J.B.F. and Sarhan, F. (2006) Plant lipocalins. In Lipocalins (Åkerström, B., Borregaard, N., Flower, D.R. and Salier, J.P., eds), pp. 41-48. Georgetown, TX, USA: Landes Bioscience.
Cohen, Y., Gisi, U. and Mosinger, E. (1991) Systemic resistance of potato plants against Phytophthora infestans induced by unsaturated fatty acids. Physiol. Mol. Plant Pathol. 38, 255-263.
Conley, T.R., Peng, H.P. and Shih, M.C. (1999) Mutations affecting induction of glycolytic and fermentative genes during germination and environmental stresses in Arabidopsis. Plant Physiol. 119, 599-608.
Cosgrove, D.J. (1999) Enzymes and other agents that enhace cell wall extensibility. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 391-417.
Cramer, G., Ergül, A., Grimplet, J. et al. (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct. Integr. Genomics, 7, 111-134.
Demel, R.A. and De Kruyff, B. (1976) The function of sterols in membranes. Biochim. Biophys. Acta, Biomembr. 457, 109-132.
Dixon, D., Lapthorn, A. and Edwards, R. (2002) Plant glutathione transferases. Genome Biol. 3, 3001-3010. reviews 3004.
Downie, B., Gurusinghe, S., Dahal, P., Thacker, R.R., Snyder, J.C., Nonogaki, H., Yim, K., Fukanaga, K., Alvarado, V. and Bradford, K.J. (2003) Expression of a galactinol synthase gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol. 131, 1347-1359.
Frank, W., Munnik, T., Kerkmann, K., Salamini, F. and Bartels, D. (2000) Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell, 12, 111-124.
Furini, A., Koncz, C., Salamini, F. and Bartels, D. (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. EMBO J. 16, 3599-3608.
Gaff, D.F. (1971) Desiccation-tolerant flowering plants in Southern Africa. Science, 174, 1033-1034.
Gallardo, K., Job, C., Groot, S.P.C., Puype, M., Demol, H., Vandekerckhove, J. and Job, D. (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol. 126, 835-848.
Gosti, F., Beaudoin, N., Serizet, C., Webb, A.A.R., Vartanian, N. and Giraudat, J. (1999) Abi1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell, 11, 1897-1910.
Gross, J., Cho, W.K., Lezhneva, L., Falk, J., Krupinska, K., Shinozaki, K., Seki, M., Herrmann, R.G. and Meurer, Jr. (2006) A plant locus essential for phylloquinone (Vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J. Biol. Chem. 281, 17189-17196.
Haerizadeh, F., Wong, C., Bhalla, P., Gresshoff, P. and Singh, M. (2009) Genomic expression profiling of mature soybean (Glycine Max) pollen. BMC Plant Biol. 9, 25.
Hammond, J.P. and White, P.J. (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J. Exp. Bot. 59, 93-109.
Hilbricht, T., Varotto, S., Sgaramella, V., Bartels, D., Salamini, F. and Furini, A. (2008) Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol. 179, 877-887.
Hiroshi, S., Ryoichi, O., Masaru, S., Isamu, I., Kiyoshi, O., Masa-aki, O. and Ken-ichiro, T. (2005) Inactivation and deficiency of core proteins of Photosystems I and II caused by genetical phylloquinone and plastoquinone deficiency but retained lamellar structure in a T-DNA mutant of Arabidopsis. Plant J. 41, 627-637.
Hoekstra, F.A., Golovian, E.A. and Buitink, J. (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci. 6, 431-438.
Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q. and Xiong, L. (2006) Overexpressing a Nam, Ataf, and Cuc (Nac) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl Acad. Sci. USA, 103, 12987-12992.
Ingram, J. and Bartels, D. (1996) The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 377-403.
Iturriaga, G., Cushman, M.A.F. and Cushman, J.C. (2006) An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes. Plant Sci. 170, 1173-1184.
Jabrin, S., Ravanel, S., Gambonnet, B., Douce, R. and Rebeille, F. (2003) One-Carbon metabolism in plants. Regulation of tetrahydrofolate synthesis during germination and seedling development. Plant Physiol. 131, 1431-1439.
Jaillon, O., Aury, J.M., Noel, B. et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature, 449, 463-467.
Karp, P.D., Riley, M., Paley, S.M. and Pellegrini-Toole, A. (2002) The MetaCyc database. Nucleic Acids Res. 30, 59-61.
Kaufman, L. and Rousseeuw, P.J. (1990) Finding Groups in Data: An Introduction to Cluster Analysis. New York: Wiley.
Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D’Angelo, C., Bornberg-Bauer, E., Kudla, J. and Harter, K. (2007) The AtGenexpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347-363.
Kirch, H.H., Nair, A. and Bartels, D. (2001) Novel ABA- and dehydration-inducible aldehyde dehydrogenase genes isolated from the resurrection plant Craterostigma plantagineum and Arabidopsis thaliana. Plant J. 28, 555-567.
Kleines, M., Elster, R.C., Rodrigo, M.J., Blervacq, A.S., Salamini, F. and Bartels, D. (1999) Isolation and expression analysis of two stress-responsive sucrose-synthase genes from the resurrection plant Craterostigma plantagineum (Hochst.). Planta, 209, 13-24.
Koster, K.L. and Leopold, A.C. (1988) Sugars and desiccation tolerance in seeds. Plant Physiol. 88, 829-832.
Kürsteiner, O., Dupuis, I. and Kuhlemeier, C. (2003) The Pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiol. 132, 968-978.
Louise, J. and Simon, M.M. (2004) A role for expansins in dehydration and rehydration of the resurrection plant Craterostigma plantagineum. FEBS Lett. 559, 61-65.
Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A. and Grill, E. (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324, 1064-1068.
Matton, D.P., Prescott, G., Bertrand, C., Camirand, A. and Brisson, N. (1993) Identification of Cis-acting elements involved in the regulation of the pathogenesis-related gene Sth-2 in potato. Plant Mol. Biol. 22, 279-291.
Maury, S., Geoffroy, P. and Legrand, M. (1999) Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoyl-coenzyme a,5-hydroxyferuloyl-coenzyme a 3,5-O-methyltransferase and caffeic acid,5-hydroxyferulic acid 3,5-O-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiol. 121, 215-224.
Medina, J., Catala, R. and Salinas, J. (2001) Developmental and stress regulation of RCI2a and RCI2b, two cold-inducible genes of Arabidopsis encoding highly conserved hydrophobic proteins. Plant Physiol. 125, 1655-1666.
Meyer, E., Aglyamova, G., Wang, S., Buchanan-Carter, J., Abrego, D., Colbourne, J., Willis, B. and Matz, M. (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GsFLX. BMC Genomics, 10, 219.
Neale, A.D., Blomstedt, C.K., Bronson, P., Le, T.N., Guthridge, K., Evans, J., Gaff, D.F. and Hamill, J.D. (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe drought stress. Plant Cell Environ. 23, 265-277.
Norwood, M., Truesdale, M.R., Richter, A. and Scott, P. (2000) Photosynthetic carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. J. Exp. Biol. 51, 159-165.
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H. and Kanehisa, M. (1999) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 27, 29-34.
Oliver, M.J., Tuba, Z. and Mishler, B.D. (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol. 151, 85-100.
Oliver, M., Dowd, S., Zaragoza, J., Mauget, S. and Payton, P. (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics, 5, 89.
Oliver, M.J., Velten, J. and Mishler, B.D. (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr. Comp. Biol. 45, 788-799.
Porembski, S. and Barthlott, W. (2000) Granitic and gneissic outcrops (Inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecol. 151, 19-28.
Poulsen, C. and Verpoorte, R. (1991) Roles of chorismate mutase, isochorismate synthase and anthranilate synthase in plants. Phytochemistry, 30, 377-386.
Proctor, M.C. and Pence, V.C. (2002) Vegetative Tissues: Bryophytes, Vascular Plants and Vegetative Propagules. Wallingford, UK: CABI Publishing.
Pühringer, H., Moll, D., Hoffmann-Sommergruber, K., Watillon, B., Katinger, H. and da Câmara Machado, M.L. (2000) The promoter of an apple Ypr10 gene, encoding the major allergen Mal D1, is stress- and pathogen-inducible. Plant Sci. 152, 35-50.
Rapala-Kozik, M., Kowalska, E. and Ostrowska, K. (2008) Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. J. Exp.Bot. 59, 4133-4143.
Ribeiro, D.T., Farias, L.P., de Almeida, J.D., Kashiwabara, P.M., Ribeiro, A.F.C., Silva-Filho, M.C., Menck, C.F.M. and Van Sluys, M.-A. (2005) Functional characterization of the Thi1 promoter region from Arabidopsis thaliana. J. Exp. Bot. 56, 1797-1804.
Roje, S. (2007) Vitamin B biosynthesis in plants. Phytochemistry, 68, 1904-1921.
Russell, D.A., Wong, D.M.L. and Sachs, M.M. (1990) The anaerobic response of soybean. Plant Physiol. 92, 401-407.
Saravitz, D.M., Pharr, D.M. and Carter, T.E. Jr (1987) Galactinol synthase activity and soluble sugars in developing seeds of four soybean genotypes. Plant Physiol. 83, 185-189.
Schenk, G., Layfield, R., Candy, J.M., Duggleby, R.G. and Nixon, P.F. (1997) Molecular evolutionary analysis of the thiamine-diphosphate-dependent enzyme, transketolase. J. Mol. Evol. 44, 552-572.
Schmitt, D., Pakusch, A.E. and Matern, U. (1991) Molecular cloning, induction and taxonomic distribution of caffeoyl-coA 3-o-methyltransferase, an enzyme involved in disease resistance. J. Biol. Chem. 266, 17416-17423.
Seo, M., Atsushi, H., Ayuko, K. et al. (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J. 48, 354-366.
Settembre, E., Begley, T.P. and Ealick, S.E. (2003) Structural biology of enzymes of the thiamin biosynthesis pathway. Curr. Opin. Struct. Biol. 13, 739-747.
Sherwin, H.W. and Farrant, J.M. (1998) Protection mechanism against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. J. Plant Growth Regul. 24, 203-210.
Shi, L. and Olszewski, N.E. (1998) Gibberellin and abscisic acid regulate Gast1 expression at the level of transcription. Plant Mol. Biol. 38, 1053-1060.
Solomon, M., Belenghi, B., Delledonne, M., Menachem, E. and Levine, A. (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell, 11, 431-444.
Swoboda, I., Karin, H.-S., Gabriel, O.R., Otto, S., Erwin, H.-B. and Oscar, V. (1996) Bet V1 proteins, the major birch pollen allergens and members of a family of conserved pathogenesis-related proteins, show ribonuclease activity in vitro. Physiol. Plant. 96, 433-438.
Taji, T., Ohsumi, C., Luchi, S., Seki, M., Kasuga, M., Kobayashi, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29, 417-426.
Takahashi, S., Bauwe, H. and Badger, M. (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem ii by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol. 144, 487-494.
Tronchet, M., Balague, C., Kroj, T., Jouanin, L. and Roby, D. (2009) Cinnamyl alcohol dehydrogenases-c and d, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol. Plant Pathol. 11, 83-92.
Tunc-Ozdemir, M., Miller, G., Song, L., Kim, J., Sodek, A., Koussevitzky, S., Misra, A.N., Mittler, R. and Shintani, D. (2009) Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol. 151, 421-432.
Urano, K., Maruyama, K., Ogata, Y. et al. (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J. 57, 1065-1078.
Valenzuela-Avendano, J.P., Estrada, I.A., Lizama, G., Souza, R., Valenzuela-Soto, E.M. and Zuniga-Aguilar, J.J. (2005) Use of a simple method to isolate intact RNA from partially hydrated Selaginella lepidophylla plants. Plant Mol. Biol. Rep. 23, 199a-199g.
Velasco, R., Salamini, F. and Bartels, D. (1994) Dehydration and ABA increase mRNA levels and enzyme activity of cytosolic GADPH in the resurrection plant Craterostigma plantagineum. Plant Mol. Biol. 26, 541-546.
Velasco, R., Salamini, F. and Bartels, D. (1998) Gene structure and expression analysis of the drought- and abscisic acid-responsive CDeT11-24 gene family from the resurrection plant Craterostigma plantagineum Hochst. Planta, 204, 459-471.
Vicré, M., Farrant, J.M. and Driouich, A. (2004a) Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species. Plant Cell Environ. 27, 1329-1340.
Vicré, M., Olivier, L., Farrant, J., Lerouge, P. and Driouich, A. (2004b) Composition and Desiccation-induced alterations of the cell wall in the resurrection plant Craterostigma wilmsii. Physiol. Plant. 120, 229-239.
Wang, C., Chin, C.K. and Chen, A. (1998) Expression of the yeast [delta]-9 desaturase gene in tomato enhances its resistance to powdery mildew. Physiol. Mol. Plant Pathol. 52, 371-383.
Watanabe, H., Abe, K., Emori, Y., Hosoyama, H. and Arai, S. (1991) Molecular cloning and gibberellin-induced expression of multiple cysteine proteinases of rice seeds (Oryzains). J. Biol. Chem. 266, 16897-16902.
Wigoda, N., Ben-Nissan, G., Granot, D., Schwartz, A. and Weiss, D. (2006) The gibberellin-induced, cysteine-rich protein Gip2 from Petunia hybrida exhibits in planta antioxidant activity. Plant J. 48, 796-805.
Willige, B.C., Kutzer, M., Tebartz, F. and Bartels, D. (2009) Subcellular localization and enzymatic properties of differentially expressed transketolase genes isolated from the desiccation tolerant resurrection plant Craterostigma plantagineum. Planta, 229, 659-666.
Wood, A. and Oliver, M. (1999) Translational control in plant stress: the formation of messenger ribonucleoprotein particles (Mrnps) in response to desiccation of Tortula ruralis gametophytes. Plant J. 18, 359-370.
Workman, C., Jensen, L.J., Jarmer, H., Berka, R., Gautier, L., Nielsen, H.B., Saxild, H.H., Nielsen, C., Brunak, S. and Knudsen, S. (2002) A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol. 9, 0048.1-0048.16.
Wu, P., Ma, L., Hou, X., Wang, M., Wu, Y., Liu, F. and Deng, X.W. (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 132, 1260-1271.
Zhu, J.K. (2002) Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273.