Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago truncatula seeds

Plant Journal

Volumn 47, Issue 5, 2006, Pages 735-750

  Buitink, Julia ^a   Leger, Jean J ^b   Guisle, Isabelle ^b   Vu, Benoit Ly ^a   Wuillème, Sylvie ^c   Lamirault, Guillaume ^b   Bars, Alice Le ^b   Meur, Nolwenn Le ^b   Becker, Anke ^d   Küster, Helge ^d   Leprince, Olivier ^a  

^a UNIVERSITÉ D'ANGERS   (France)

^b Parc Scientifique de Luminy   (France)

^c CEMAGREF   (France)

^d BIELEFELD UNIVERSITY   (Germany)

Author keywords

C metabolism; Desiccation tolerance; Gene profiling; Germination; Medicago truncatula; Seeds

Indexed keywords

DROUGHT; GENES; METABOLISM; POLYETHYLENE GLYCOLS; SUGAR (SUCROSE);

C METABOLISM; DESICCATION TOLERANCE (DT); GENE PROFILING; MEDICAGO TRUNCATULA;

SEED;

ABSCISIC ACID; CARBON; MACROGOL DERIVATIVE; MESSENGER RNA; SUCROSE; VEGETABLE PROTEIN;

ARTICLE; BARREL MEDIC; CLASSIFICATION; CLUSTER ANALYSIS; DESICCATION; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; PLANT SEED; PRENATAL DEVELOPMENT;

ABSCISIC ACID; CARBON; CLUSTER ANALYSIS; DESICCATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GERMINATION; KINETICS; MEDICAGO TRUNCATULA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT PROTEINS; POLYETHYLENE GLYCOLS; RNA, MESSENGER; SEEDS; SUCROSE;

DRYING; EMBRYOS; GENES; GERMINATION; SUCROSE;

MEDICAGO TRUNCATULA;

EID: 33747053339     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02822.x     Document Type: Article

References (52)

1. Alpert, P. and Oliver, M.J. (2002) Drying without dying. In Desiccation Tolerance and Survival in Plants: Drying Without Dying (Black, M. and Pritchard, H.W., eds) Oxon, UK: CABI Publishing, pp. 3-43.
2. 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.
3. Baud, S., Boutin, J.-P., Miquel, M., Lepiniec, L. and Rochat, C. (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol. Biochem. 40, 151-160.
4. Bell, C.J., Dixon, R.A., Farmer, A.D. et al. (2001) The Medicago genome initiative: a model legume database. Nucleic Acids Res. 29, 114-117.
5. Black, M., Corbineau, F., Gee, H. and Côme, D. (1999) Water content, raffinose, and dehydrins in the induction of desiccation tolerance in immature wheat embryos. Plant Physiol. 120, 463-472.
6. Boudet, J., Buitink, J., Hoekstra, F.A., Rogniaux, H., Larré, 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.
7. Bray, E.A. (2002) Classification of genes differentially expressed during water-deficit stress in Arabidopsis thaliana: an analysis using microarray an differential expression data. Annu Bot. 89, 803-811.
8. Bruggink, T. and van der Toorn, P. (1995) Induction of desiccation tolerance in germinated seeds. Seed Sci. Res. 5, 1-4.
9. Buitink, J., Ly Vu, B., Satour, P. and Leprince, O. (2003) A physiological model to study the re-establishment of desiccation tolerance in germinated radicles of Medicago truncatula Gaertn. Seeds. Seed Sci. Res. 13, 273-286.
10. Buitink, J., Thomas, M., Gissot, L. and Leprince, O. (2004) Starvation, osmotic stress and desiccation tolerance lead to expression of different genes of the regulatory b and c subunits of the SnRK1 complex in germinating seeds of Medicago truncatula. Plant Cell Environ. 27, 55-67.
11. Butler, W.M. and Cuming, A.C. (1993) Differential molecular responses to abscisic acid and osmotic stress in viviparous maize embryos. Planta, 189, 47-54.
12. Chern, M.S., Bobb, A.J. and Bustos, M.M. (1996) The regulator of MAT2 (ROM2) protein binds to early maturation promoters and represses PvALF-activated transcription. Plant Cell, 8, 305-321.
13. Collet, H., Shen, A., Gardner, M., Farrant, J.M., Denby, K.J. and Illing, N. (2004) Towards transcript profiling of desiccation tolerance in Xerophyta humilis: construction of a normalized 11 k X. humilis xDNA set and microarray expression analysis of 424 cDNAs in response to dehydration. Physiol. Plant. 122, 39-53.
14. Dejardin, A., Solokov, L.N. and Kleczkowsk, L.A. (1999) Sugar/osmoticum levels modulate differential abscisic acid-independent expression of two stress-responsive sucrose synthase genes in Arabidopsis. Biochem. J. 344, 503-509.
15. Dong, J., Keller, W.A., Yan, W. and Georges, F. (2004) Gene expression at early stages of Brassica napus seed development as revealed by transcripts profiling of seed-abundant cDNAs. Planta, 218, 483-491.
16. Flower, D.R. (1996) The lipocalin protein family: structure and function. Biochem. J. 15, 1-14.
17. Geigenberger, P., Reimholz, R., Deiting, U., Sonnewald, U. and Stitt, M. (1999) Decreased expression of sucrose phosphate synthase strongly inhibits the water stress-induced synthesis of sucrose in growing potato tubers. Plant J. 19, 119-129.
18. Girke, T., Todd, J., Ruuska, S., White, J., Benning, C. and Ohlrogge, J. (2000) Microarray analysis of developing Arabidopsis seeds. Plant Physiol. 124, 1570-1581.
19. Golovina, E., Hoekstra, F.A. and Van Aelst, A.C. (2001) The competence to acquire cellular desiccation-tolerance is not dependent on seed morphological development. J. Exp. Bot. 52, 1015-1027.
20. Haslekås, C., Viken, M.K., Grini, P.E., Nygaard, V., Nordgard, S.H., Meza, T.J. and Aalen, R.B. (2003) Seed 1-cysteine peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress. Plant Physiol. 133, 1148-1157.
21. Hennig, L., Gruissem, W., Grossniklaus, U. and Köhler, C. (2004) Transcriptional programs of early reproductive stages in Arabidopsis. Plant Physiol. 135, 1765-1775.
22. Hoekstra, F.A., Haigh, A.M., Tetteroo, F.A.A. and Van Roekel, T. (1994) Changes in soluble sugars in relation to desiccation tolerance in cauliflower seeds. Seed Sci. Res. 4, 143-147.
23. Hoekstra, F.A., Golovina, E.A. and Buitink, J. (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci. 5, 431-438.
24. Hohnjec, N., Vieweg, M.F., Pühler, A., Becker, A. and Küster, H. (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. 137, 1283-1301.
25. Ingram, J. and Bartels, D. (1996) The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 377-403.
26. Kirik, V., Kölle, K., Miséra, S. and Bäumlein, H. (1998) Two novel MYB homologues with changed expression in late embryogenesis- defective Arabidopsis mutants. Plant Mol. Biol. 37, 819-827.
27. Le Meur, N., Lamirault, G., Bihouée, A., Steenman, M., Bédrine-Ferran, H., Teusan, R., Ramstein, G. and Léger, J.J. (2004) A dynamic, web-accessible resource to process raw microarray scan data into consolidated gene expression values. Importance of replication. Nucleic Acids Res. 32, 5349-5358.
28. Leprince, O., Harren, F.J.M., Buitink, J., Alberda, M. and Hoekstra, F.A. (2000) Metabolic dysfunction and unabated respiration precede the loss of membrane integrity during dehydration of germinating radicles. Plant Physiol. 122, 597-608.
29. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell, 10, 1391-1406.
30. MacDonald, J.A. and Storey, K.B. (1999a) Cyclic AMP-dependent protein kinase: role in anoxia and freezing tolerance of the marine periwinkle Littorina littorea. Marine Biol. 133, 193-203.
31. MacDonald, J.A. and Storey, K.B. (1999b) Regulation of ground squirrel Na+K+-ATPase activity by reversible phosphorylation during hibernation. Biochem. Biophs. Res. Comm. 254, 424-429.
32. Mowla, S.B., Thomson, J.A., Farrant, J.M. and Mundree, S.G. (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta, 215, 716-726.
33. Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y. and Nambara, E. (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J. 41, 697-709.
34. Nambara, E., Hayama, R., Tsuchiya, Y., Nishimura, M., Kawaide, H., Kamiya, Y. and Naito, S. (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev. Biol. 220, 412-423.
35. Neale, A.D., Blomstedt, C.K., Bronson, P., Guthridge, K., Evans, J., Gaff, D.J. 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.
36. Oliver, M.J., Dowd, S.E., Zaragoza, J., Mauget, S.A. and Payton, P.R. (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5, 89.
37. Pelah, D., Wang, W.X., Altman, A., Shoseyov, O. and Bartels, D. (1997) Differential accumulation of water-stress related proteins, sucrose synthase and soluble sugars in Populus genotypes which differ in their water-stress response. Physiol. Plant. 99, 153-159.
38. Quackenbush, J. (2001) Computational analysis of microarray data. Nature Rev. Genet. 2, 418-427.
39. Ramanjulu, S. and Bartels, D. (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant, Cell Environ. 25, 141-151.
40. Raz, V., Bergervoet, J.H. and Koornneef, M. (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development, 128, 243-252.
41. Ruuska, S.A., Girke, T., Benning, C. and ohlrogge, J.B. (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell, 14, 1191-1206.
42. Seki, M., Narusaka, M., Ishida, J. et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279-292.
43. Soeda, Y., Konings, M.C.J.M., Vorst, O., van Houwelingen, A.M.M.L., Stoopen, G.M., Maliepaard, C.A., Kodde, J., Bino, R.J., Groot, S.P.C. and van der Geest, A.H.M. (2005) Gene expression programs during Brassica oleracea seed maturation, osmopriming, and germination are indicators of the progression of the germination process and the stress tolerance level. Plant Physiol. 137, 354-368.
44. Staples, J.F. and Hochachka, P.W. (1997) Liver energy metabolism during hybernation in the golden-mantled ground squirrel Spermophilus lateralis. Curr. J. Zoo. 74, 1059-1065.
45. Sturn, A., Quackenbush, J. and Trajanoski, Z. (2002) Genesis: cluster analysis of microarray data. Bioinformatics, 18, 207-208.
46. Thelander, M., Olsson, T. and Ronne, H. (2004) Snf1-related protein kinase 1 is needed for growth in a normal day-light cycle. EMBO J. 23, 1900-1910.
47. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl Acad. Sci. USA, 97, 11632-11637.
48. Verwoerd, T.C., Dekker, B.M. and Hoekema, A. (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17, 2362.
49. Villalobos, M.A., Bartels, D. and Iturruaga, G. (2004) Stress tolerance and glucose insensitive phenotypes in Arabidopsis overexpressing the CpMYB10 transcription factor gene. Plant Physiol. 135, 309-324.
50. Wehmeyer, N. and Vierling, E. (2000) The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol. 122, 1099-1108.
51. Wood, A.J. and Oliver, M.J. (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.
52. Yano, R., Nakamura, M., Yoneyama, T. and Nishid, I. (2005) Starch-related α-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol. 138, 837-846.