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Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips

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Abstract

In order to isolate glucose-starvation-related cDNAs in maize (Zea mays L.) root tips, a cDNA library was constructed with poly(A)+ mRNA from 24 h starved root tips. After differential screening of the library, we isolated six different cDNAs (named pZSS2 and pZSS7) which were expressed during glucose starvation. Time course analysis revealed that maximum expression of five of these genes occurs 30 h after the onset of the starvation treatment. On the contrary, the expression of mRNAs corresponding to pZSS4 was maximal at an early stage of starvation and then dramatically decreased. The expression of this gene did not seem to be specific for glucose starvation. The pattern of induction of the genes corresponding to pZSS2, pZSS3, pZSS5, pZSS6 and pZSS7 revealed that non-metabolizable sugars such as L-glucose and mannitol induce mRNA transcription similarly to glucose starvation. When D-glucose or any other metabolizable sugar was supplied, the level of transcripts was reduced. Nucleotide sequence analyses of the six cDNAs allowed identification of five of them by comparison with sequence data bases. The protein encoded by clone pZSS2 is analogous to a wound-induced protein from barley. Clones pZSS4 to pZSS7 encode, respectively, a transmembrane protein, a cysteine protease, a metallothionein-like protein and a chymotrypsin/subtilisin-like protease inhibitor. Clone pZSS3 shares no significant homology with any known sequence.

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References

  1. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology. John Wiley, New York (1990).

    Google Scholar 

  2. Azumi Y, Watanabe A: Evidence for a senescence-associated gene induced by darkness. Plant Physiol 95: 577–583 (1991).

    Google Scholar 

  3. Baker ME, Saier MH: A common ancestor for bovine lens fiber major-intrinsic protein, soybean nodulin-26 protein, and E. coli glycerol facilitator. Cell 60: 185–186 (1990).

    Google Scholar 

  4. Baumgartner B, Chrispeels MJ: Partial characterization of a protease inhibitor which inhibits the major endopeptidase present in the cotyledons of mung beans. Plant Physiol 58: 1–6 (1976).

    Google Scholar 

  5. Baysdorfer C, Van der Woude WJ: Carbohydrate responsive proteins in the roots of Pennisetum americanum. Plant Physiol 87: 566–570 (1988).

    Google Scholar 

  6. Baysdorfer C, Warmbrodt RD, Van der Woude WJ: Mechanism of starvation tolerance in pearl millet. Plant Physiol 88: 1381–1387 (1988).

    Google Scholar 

  7. Brouquisse R, James F, Raymond P, Pradet A: Study of glucose starvation in excised maize root tips. Plant Physiol 96: 619–626 (1991).

    Google Scholar 

  8. Brouquisse R, James F, Pradet A, Raymond P: Asparagine metabolism and nitrogen distribution during protein degradation in sugar-starved maize root tips. Planta 188: 384–395 (1992).

    Google Scholar 

  9. Buchanan-Wollaston V: Isolation of cDNA clones for genes that are expressed during leaf senescence in Brassica napus. Identification of a gene encoding a senescence-specific metallothionein-like protein. Plant Physiol 105: 839–846 (1994).

    Google Scholar 

  10. Chen M-H, Liu L-F, Chen Y-R, Wu H-K, Yu S-M: Expression of α-amylases, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J 6: 625–636 (1994).

    Google Scholar 

  11. Cheng CL, Acedo GN, Cristinsin M, Conkling MA: Sucrose mimics the light induction of Arabidopsis nitrate reductase gene transcription. Proc Natl Acad Sci USA 89: 1861–1864 (1992).

    Google Scholar 

  12. Cordero MJ, Raventos M, San Segundo B: Expression of maize proteinase inhibitor gene is induced in response to wounding and fungal infection: system c wound-response of a monocot gene. Plant J 6: 141–150 (1994).

    Google Scholar 

  13. Criqui MC, Durr A, Parmentier Y, Marrach J, Fleck J, Jamet E: How are photosynthetic genes repressed in freshly-isolated mesophyll protoplasts of Nicotania sylvestris? Plant Physiol Biochem 30: 597–601 (1992).

    Google Scholar 

  14. Dieuaide M, Brouquisse R, Pradet A, Raymond P: Increased fatty acid ⨿-oxidation after glucose starvation in maize root tips. Plant Physiol 99: 595–600 (1992).

    Google Scholar 

  15. Farrar JF: Respiration rate of barley roots: its relation to growth, substrate supply and the illumination of the shoot. Ann Bot 48: 53–63 (1981).

    Google Scholar 

  16. de Framond AJ: A metallothionein-like from maize (Zea mays). Cloning and characterization. FEBS Lett 290: 103–106 (1991).

    Google Scholar 

  17. Fraser RSS: Evidence for the occurrence of the ‘pathogenesis-related’ proteins in leaves of healthy tobacco plants during flowering. Physiol Plant Path 19: 69–76 (1981).

    Google Scholar 

  18. Gancedo JM: Carbon catabolite repression in yeast. Eur J Biochem 206: 297–313 (1992).

    Google Scholar 

  19. Genix P, Bligny R, Martin JB, Douce R: Transient accumulation of asparagine in sycamore cells after a long period of sucrose starvation. Plant Physiol 94: 717–722 (1990).

    Google Scholar 

  20. Graham IA, Baker CJ, Leaver CJ: Analysis of the cucumber malate synthase gene promoter by transient expression and gel retardation assays. Plant J 6: 893–902 (1994).

    Google Scholar 

  21. Graham IA, Denby KJ, Leaver CJ: Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. Plant Cell 6: 761–772 (1994).

    Google Scholar 

  22. Grannell A, Harris N, Pisabarro AG, Carbonell A: Temporal and spatial expression of a thiolprotease gene during pea ovary senescence, and its regulation by gibberellin. Plant J 2: 907–915 (1992).

    Google Scholar 

  23. Guerrero FD, Jones JT, Mullet JE: Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol Biol 15: 11–26 (1990).

    Google Scholar 

  24. Hattori T, Nakagawa S, Nakamura K: High-level expression of tuberous root storage protein genes of sweet potato in stems of plantlets grown in vitro on sucrose medium. Plant Mol Biol 14: 595–604 (1990).

    Google Scholar 

  25. Hensel LL, Grbic V, Baumgarten DA, Bleecker AB: Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5: 533–564 (1993).

    Google Scholar 

  26. James F, Brouquisse R, Pradet A, Raymond P: Changes in proteolytic activities in glucose-starved maize root tips. Regulation by sugars. Plant Physiol Biochem 31: 845–856 (1993).

    Google Scholar 

  27. Jang J-C, Sheen J: Sugar sensing in higher plants. Plant Cell 6: 1665–1679 (1994).

    Google Scholar 

  28. Journet EP, Bligny R, Douce R: Biochemical changes during sucrose deprivation in higher plant cells. J Biol Chem 261: 3193–3199 (1986).

    Google Scholar 

  29. Kerr PS, Rufty TW, Huber SC: Changes in non-structural carbohydrates in different parts of soybean (Glycine max [L.] Merr.) plants during a light/dark cycle and in extended darkness. Plant Physiol 78: 576–581 (1985).

    Google Scholar 

  30. Koch KE, Nolte KD, Duke ER, McCarthy DR, Avigne WT: Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 4: 59–69 (1992).

    Google Scholar 

  31. Koizumi M, Yamaguchi-Shinozaki K, Tsuji H, Shinozaki K: Structure and expression of two genes that encode distinct drought-inducible cysteine proteinases in Arabidopsis thaliana. Gene 129: 175–182 (1993).

    Google Scholar 

  32. Krapp A, Hofmann B, Schäfer C, Stitt M: Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis? Plant J 3: 817–828 (1993).

    Google Scholar 

  33. Lee-Downing W, Mauxion F, Fauvarque M-O, Reviron M-P, de Vienne D, Vartanian N, Giraudat J: A Brassica napus transcript encoding a protein related to the Kunitz protease inhibitor family accumulates upon water stress in leaves, but not seeds. Plant J 2: 685–693 (1992).

    Google Scholar 

  34. Linthorst HJM, Dankash N, Brederode FT, Van Kan JAL, De Wit PJ, Bol JF. Tobacco and tomato PR proteins homologous to win and pro-hevein lack the ‘hevein’ domain. Mol Plant Microb Interact 4: 586–592 (1991).

    Google Scholar 

  35. Linthorst HJM, Van Der Does C, Brederode FT, Bol JF: Circadian expression and induction by wounding of tobacco genes for cysteine proteinase. Plant Mol Biol 21: 685–694 (1993).

    Google Scholar 

  36. Linthorst HJM, van der Does C, van Kan JAL, Bol JF: Nucleotide sequence of a cDNA clone encoding tomato (Lycopersicon esculentum) cysteine proteinase. Plant Physiol 101: 705–706 (1993).

    Google Scholar 

  37. Mason HS, De Wald DB, Creelman RA, Mullet JE: Coregulation of soybean vegetative storage protein gene expression by methyl jasmonate and soluble sugars. Plant Physiol 98: 859–867 (1992).

    Google Scholar 

  38. Müller-Röber BT, Kossman J, Hannah LC, Willmitzer L, Sonnewald U: One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol Gen Genet 224: 136–146 (1990).

    Google Scholar 

  39. Pan A, Tie F, Duau Z, Yang M, Wang Z, Li L, Chen Z, Ru B: α-domain of human metallothionein IA can bind to metals in transgenic tobacco plants. Mol Gen Genet 242: 666–674 (1994).

    Google Scholar 

  40. Perlman D, Halvorson HO: A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J Mol Biol 167: 391–409 (1983).

    Google Scholar 

  41. Sachs MM, Ho THD: Alteration of gene expression during environmental stress in plants. Annu Rev Plant Physiol 37: 363–376 (1986).

    Google Scholar 

  42. Saglio P, Pradet A: Soluble sugars, respiration, and energy charge during aging of excised maize root tips. Plant Physiol 66: 516–519 (1980).

    Google Scholar 

  43. Sambrook J, Fritsch EF, Maniatis T: Molecular cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  44. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    Google Scholar 

  45. Schaffer MA, Fischer R: Analysis of mRNAs that accumulate in response to low temperature identifies a thiol protease gene in tomato. Plant Physiol 87: 431–436 (1988).

    Google Scholar 

  46. Shagan T, Meraro D, Bar-Zvi D: Nucleotide sequence of an Arabidopsis thaliana turgor-responsive TMP-B cDNA clone encoding transmembrane protein with a major intrinsic protein motif. Plant Physiol 102: 689–690 (1993).

    Google Scholar 

  47. Sheen J: Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038 (1990).

    Google Scholar 

  48. Stanford A, Bevan M, Northcote D: Differential expression within a family of novel wound induced genes in potato. Mol Gen Genet 215: 200–208 (1989).

    Google Scholar 

  49. Steffens JC: The heavy metal-binding peptides in plants. Annu Rev Plant Physiol Plant Mol Biol 41: 553–575 (1990).

    Google Scholar 

  50. Svensson B, Svendsen I, Hojrup P, Roepstorff P, Ludvigsen S, Poulsen FM: Primary structure of barwin: a barley seed protein closely related to the C-terminal domain of proteins encoded by wound-induced plant genes. Biochemistry 31: 8767–8770 (1992).

    Google Scholar 

  51. Tassi F, Maestri E, Restivo FM, Marmiroli N: The effects of carbon starvation on cellular metabolism and RNA synthesis in Gerbera callus cultures. Plant Sci 83: 127–136 (1992).

    Google Scholar 

  52. Verwoerd TC, Dekker BMM, Hoekema A: A small-scale procedure for the rapid isolation of plant RNAs. Nucl Acids Res 17: 2362 (1989).

    Google Scholar 

  53. Webster PL, Henry M: Sucrose regulation of protein synthesis in pea root meristem cells. Envir Exp Bot 27: 253–262 (1987).

    Google Scholar 

  54. Williams J, Bulman M, Huttly A, Phillips A, Neill S: Characterization of a cDNA from Arabidopsis thaliana encoding a potential thiol protease whose expression is induced independently by wilting and abscisic acid. Plant Mol Biol 25: 259–270 (1994).

    Google Scholar 

  55. Yu SM, Kuo YH, Sheu G, Sheu YJ, Liu LF: Metabolic depression of α-amylase gene expression in suspension-cultured cells of rice. J Biol Chem 266: 21131–21137 (1991).

    Google Scholar 

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Chevalier, C., Bourgeois, E., Pradet, A. et al. Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips. Plant Mol Biol 28, 473–485 (1995). https://doi.org/10.1007/BF00020395

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