Planta

, Volume 194, Issue 4, pp 541–549

Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: Enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings

  • Peter J. Christie
  • Mark R. Alfenito
  • Virginia Walbot
Article

Abstract

Changes in anthocyanin content and transcript abundance for genes whose products function in general phenylpropanoid metabolism and the anthocyanin pathway were monitored in maize (Zea mays L.) seedlings during short-term, low-temperature treatment. Anthocyanin and mRNA abundance in sheaths of maize seedlings increased with the severity and duration of cold. Anthocyanin accumulation was found in all tested lines that were genotypically capable of any anthocyanin production. Within 24 h of transferring 7-d maize (B37N) seedlings to 10° C, phenylalanine ammonia-lyase (Pal) (EC 4.3.1.5)-homologous and chalcone synthase (C2) (EC 2.3.1.74) transcript levels increased at least 8- and 50-fold, respectively, and 4-coumarate:CoA ligase (4Cl) (EC 6.2.1.12)-homologous and chalcone isomerase (Chi) (EC 5.5.1.6)-homologous transcripts increased at least 3-fold over levels in unstressed plants. Time-course studies showed thatPal (EC 4.3.1.5) andC2-transcript levels remained relatively constant for the first 12 h of cold stress, dramatically increased over the next 12 h, and declined to pretreatment levels within 2 d of returning coldstressed seedlings to ambient (25° C) temperature. Transcripts4Cl (EC 6.2.1.12) andChi (EC 5.5.1.6) increased in abundance within 6 h of cold stress, exhibited no further increase over the next 36 h, and declined to pretreatment levels upon returning seedlings to 25° C. Transcripts homologous to two regulatory (R, C1) and three structural (A1,A2, andBz2) anthocyanin genes increased at least 7- to 10-fold during cold treatment, exhibiting similar kinetics of accumulation as forPal (EC 4.3.1.5) andC2 transcripts. Transcripts encoded byBz1, the anthocyanin structural gene for UDP:glucose-flavonol glucosyltransferase (EC 2.4.1.91), were relatively abundant in control tissues and exhibited only a transient increase during the cold period. Our studies suggest that the genes of the anthocyanin biosynthetic pathway can be consideredcor (Cold-Regulation) genes, and because this pathway is well defined, it is an excellent subject for characterizing plant molecular responses to low temperatures.

Key words

Anthocyanin Cold stress mRNA Zea mays 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bodeau, J., Walbot, V. (1992) Regulated transcription of the maizeBronze-2 promoter in electroporated protoplasts requires the Cl andR gene products. Mol. Gen. Genet.233, 379–387Google Scholar
  2. Chandler, V.L., Radicella, J.P., Robbins, T.P., Chen, J., Turks, D. (1988) Two regulatory genes of the maize anthocyanin pathway are homologous: Isolation ofB utilizingR genomic sequences. Plant Cell1, 1175–1183Google Scholar
  3. Chen, S.-M., Coe, E.H. Jr. (1977) Control of anthocyanin synthesis by theC locus in maize. Biochem. Genet.15, 333–346Google Scholar
  4. Christie, P.J., Hahn, M., Walbot, V. (1991) Low-temperature accumulation ofAlcohol dehydrogenase-1 mRNA and protein activity in maize and rice seedlings. Plant Physiol.95, 699–706Google Scholar
  5. Cocciolone, S.M., Cone, K.C. (1993)Pl-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics135, 575–588Google Scholar
  6. Coe, E.H. Jr., Neuffer, M.G., Hoisington, D.A. (1988) The genetics of corn. In: Corn and corn improvement, pp. 181–258, Sprague, G.F., Dudley, J.W., eds. Am. Soc. Agronomy, MadisonGoogle Scholar
  7. Cone, K.C., Burr, B. (1989) Molecular and genetic analysis of the light requirement for anthocyanin synthesis in maize. In: Genetics of flavonoids, pp. 143–145, Styles, D.E., Gavazzi, G.A., Racchi, M.L., eds. Unicopli, MilanGoogle Scholar
  8. Dellaporta, S.L., Greenblatt, I., Kermicle, J.L., Hicks, J.B., Wessler, S.R. (1987) Molecular cloning of the maizeR-nj allele by transposon tagging withAc. In: Chromosome structure and function: Impact of new concepts, 18th Stadler Genetics Symposium, pp. 263–282, Gustafson, J.P., Appels, R., eds. Plenum Press, New YorkGoogle Scholar
  9. Dixon, R.A., Harrison, M.J. (1990) Activation, structure, and organization of genes involved in microbial defense in plants. Adv. Genet.28, 165–234Google Scholar
  10. Dooner, H.K. (1983) Coordinate genetic regulation of flavonoid biosynthetic enzymes in maize. Mol. Gen. Genet.189, 136–141Google Scholar
  11. Emerson, R.A. (1921) The genetic relations of plant colors in maize. Cornell University Press, Ithaca, New YorkGoogle Scholar
  12. Fedoroff, N.V., Furtek, D.B., Nelson, O.E. Jr. (1984) Cloning of thebronze locus in maize by a simple and generalizable procedure using the transposable controlling elementActivator (Ac). Proc. Natl. Acad. Sci. USA81, 3825–3829Google Scholar
  13. Guy, C.L. (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu. Rev. Plant Physiol.41, 187–223Google Scholar
  14. Hahlbrock, K., Scheel, D. (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu. Rev. Plant Physiol. Mol. Biol.40, 347–369Google Scholar
  15. Hahn, M., Walbot, V. (1990) Effects of cold-treatment on protein synthesis and mRNA levels in rice leaves. Plant Physiol.91, 930–938Google Scholar
  16. Hajela, R.K., Horvath, D.P., Gilmour, S.J., Tomashow, M.F. (1990) Molecular cloning and expression ofcor (cold-regulated) genes inArabidopsis thaliana. Plant Physiol.93, 1246–1252Google Scholar
  17. Jackson, J., Culinaez-Macia, F., Prescott, A.G., Roberts, K., Martin, C. (1991) Expression patterns ofmyb genes fromAntirrhinum flowers. Plant Cell3, 115–125Google Scholar
  18. Kho, K.F.F., Bolsman-Louwen, A.C., Vuik, J.C., Bennink, G.J.H. (1977) Anthocyanin synthesis in a white flowering mutant ofPetunia hybrida. Planta135, 109–118Google Scholar
  19. Klein, T.M., Roth, B.A., Fromm, M.E. (1989) Regulation of anthocyanin biosynthetic genes introduced into intact maize tissues by microprojectiles. Proc. Natl. Acad. Sci. USA86, 6681–6685Google Scholar
  20. Levitt, J. (1980) Responses of plants to environmental stresses, vol I: Chilling, freezing, and high temperature stresses. Academic Press, New YorkGoogle Scholar
  21. Ludwig, S.R., Habera, L.F., Dellaporta, S.L., Wessler, S.R. (1989) Lc, a member of the maizeR gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains themyc-homology region. Proc. Natl. Acad. Sci. USA86, 7092–7096Google Scholar
  22. McLaughlin, M., Walbot, V. (1987) Cloning of a mutablebz2 allele of maize by transposon tagging and differential hybridization. Genetics117, 771–776Google Scholar
  23. Mennssen, A., Höhmann, S., Martin, W., Schnable, P.S., Peterson, P.A., Saedler, H., Gierl, A. (1990) TheEn/Spm transposable element ofZea mays contains splice sites at the termini generating a novel intron from adSpm element in theA2 gene. EMBO J.9, 3051–3057Google Scholar
  24. Nash, J., Luehrsen, K., Walbot, V. (1990)Bronze-2 gene of maize: Reconstruction of a wild-type allele and analysis of transcription and splicing. Plant Cell2, 1039–1049Google Scholar
  25. Ortiz, D.F., Strommer, J.N. (1990) TheMu1 maize transposable element induces tissue-specific aberrant splicing and polyadenylation in two Adh1 mutants. Mol. Cell Biol.10, 2090–2095Google Scholar
  26. Paz-Ares, J., Wienand, U., Peterson, P.A., Saedler, H. (1986) Molecular cloning of thec locus ofZea mays: A locus regulating the anthocyanin pathway. EMBO J.5, 829–833Google Scholar
  27. Perrot, G.H., Cone, K.C. (1989) Nucleotide sequence of the maizeR-S gene. Nucleic Acids Res.17, 8003Google Scholar
  28. Reddy, A.R., Britsch, L., Salamini, F., Saedler, H., Rohde, W. (1987) TheA1 (anthocyanin-1) locus inZea mays encodes dihydroquercetin reductase. Plant Sci.52, 7–13Google Scholar
  29. Roth, B.A., Goff, S.A., Klein, T.M., Fromm, M.E. (1991)C- andR-dependent expression of the maizeBz1 gene requires sequences with homology to mammalianmyb andmyc binding sites. Plant Cell3, 317–325Google Scholar
  30. Shah, D.M., Hightower, R.C., Meagher, R.B. (1983) Genes encoding actin in higher plants: Intron positions are highly conserved but the coding sequences are not. J. Mol. Appl. Genet.2, 111–126Google Scholar
  31. Shichijo, C., Hamada, T., Hiraoka, M., Johnson, C.B., Hashimoto, T. (1993) Enhancement of red-light-induced anthocyanin synthesis in sorghum first internodes by moderate low temperature given in the pre-irradiation culture period. Planta191, 238–245Google Scholar
  32. Taylor, L.P., Briggs, W.R. (1990) Genetic regulation and photocontrol of anthocyanin accumulation in maize seedlings. Plant Cell2, 115–127Google Scholar
  33. van Tunen, A.J., Koes, R.E., Spelt, C.E., van der Krol, A.R., Stuitje, A.R., Mol, J.N.M. (1988) Cloning of the two chalcone flavanone isomerase genes fromPetunia hybrida: Coordinate, light-regulated and differential expression of flavonoid genes. EMBO J.7, 1257–1263Google Scholar
  34. Wienand, U., Weydemann, U., Niesbach-Klögen, U., Peterson, P.A., Saedler, H. (1986) Molecular cloning of thec2 locus ofZea mays, the gene coding for chalcone synthase. Mol. Gen. Genet.203, 202–207Google Scholar
  35. Winter, J., Wright, R., Duck, N., Gasser, C., Fraley, R., Shah, D. (1988) The inhibition of petuniahsp70 mRNA processing during CdCl2 stress. Mol. Gen. Genet.211, 315–319Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Peter J. Christie
    • 1
  • Mark R. Alfenito
    • 1
  • Virginia Walbot
    • 1
  1. 1.Department of Biological SciencesStanford UniversityStanfordUSA
  2. 2.Department of Microbiology and Molecular Genetics 6431 FanninUniversity of Texas Health Sciences Center at HoustonHoustonUSA

Personalised recommendations