Skip to main content
Physiology and Molecular Biology of Plants logoLink to Physiology and Molecular Biology of Plants
. 2008 Jun 15;14(1-2):1–8. doi: 10.1007/s12298-008-0001-7

Cell maturity gradient determines light regulated accumulation of proteins in pearl millet leaves

M Tamil Selvi 1, Rameshwar Sharma 1,✉
PMCID: PMC3550656  PMID: 23572869

Abstract

Developing pearl millet leaves possess cells of increasing maturity from the leaf base to the tip with oldest cells at the leaf tip. This natural developmental gradient was used to analyze the photoregulation of enzymes located in cytosolic, peroxisomal, and plastidic compartments of the leaf in relation to the cell age. In dark-grown leaves, the level of plastidic protochlorophyllide oxidoreductase A (PORA) (EC 1.3.1.33) protein increased from the leaf base to tip. Exposure to light reduced the level of PORA protein and stiumulated accmulation of PORB protein with increasing level from the base to the leaf tip. Light induced formation of cytosolic PEP carboxylase (EC 4.1.1.31) in the leaf with induction being maximal in the leaf tip. The levels of peroxisomal protein catalase (EC 1.11.1.6) showed gradual increase from the base to leaf tip in dark and light-grown leaves. By contrast, the distribution profile of cytosolic enzyme peroxidase (EC 1.11.1.7) followed reverse pattern in the dark-and light-grown leaves. In dark-grown leaves, peroxidase level showed increase towards the leaf tip, whereas light exposure lowered peroxidase level near the leaf tip and stimulated near the leaf base. These results indicate that the cell maturity gradient in cooperation with plastids modulates in a dual fashion the magnitude and pattern of photoregulation of protein levels in pearl millet leaves. It promotes the level of proteins functionally related to plastids towards the leaf tip and at the same time suppresses the level of cytosolic proteins, restricting them to the leaf base.

Key words: Protochlorophyllide oxidoreductase, Peroxidase, Catalase, Pennisetum americanum, Cell maturity gradient, PEP carboxylase

Full Text

The Full Text of this article is available as a PDF (648.9 KB).

Abbreviations

WL

white light

RL

red light

D

darkness

Chl

chlorophyll

Car

Carotenoids

POR

protochlorophyllide oxidoreductase

PEP

phosphoenolpyruvate

References

  1. Acevedo A., Williamson J.D., Scandalios J.G. Photoregulation of Cat2 and Cat3 catalase genes in pigmented and pigment deficient maize: the circadian regulation of Cat3 is superimposed on its quasiconstitutive expression in maize leaves. Genetics. 1991;127:601–607. doi: 10.1093/genetics/127.3.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bajracharya D., Bergfeld R., Hatzfeld W.-D., Klein S., Schopfer P. Regulatory involvement of plastids in the development of peroxisomal enzymes in the cotyledons of mustard (Sinapsis alba L.) seedlings. J Plant Physiol. 1987;126:421–436. [Google Scholar]
  3. Baker N.R., Leech R.M. Development of photosystem I and photosystem II activities in leaves of light grown maize (Zea mays) Plant Physiol. 1977;60:640–644. doi: 10.1104/pp.60.4.640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chollet R., Vidal J., O’Leary M.H. Phosphoenolpyruvate carboylase: A ubiquitous, highly regulated enzyme in plants. Annu. Rev. Plant Physio. Plant Mol. Biol. 1996;47:273–298. doi: 10.1146/annurev.arplant.47.1.273. [DOI] [PubMed] [Google Scholar]
  5. Datta R., Sharma R. Temporal and spatial regulation of nitrate reductase and nitrite reductase in greening maize leaves. Plant Science. 1999;144:77–83. doi: 10.1016/S0168-9452(99)00057-6. [DOI] [Google Scholar]
  6. Datta R., Vally K.J.M., Sharma R. Sugar mimics the light-mediated β-amylase induction and distribution in maize and pearl millet leaves. J. Plant Physiol. 1999;154:665–672. [Google Scholar]
  7. Davis B. Disc electrophoresis. II. Methods and application to human serum proteins. Ann. NY Acad. Sci. 1964;121:404–427. doi: 10.1111/j.1749-6632.1964.tb14213.x. [DOI] [PubMed] [Google Scholar]
  8. Dean C., Leech R.M. Genome expression during normal leaf development. I. Cellular and chloroplast numbers and DNA, RNA and protein levels in tissues of different ages within seven day old wheat leaf. Plant Physiol. 1982;69:904–910. doi: 10.1104/pp.69.4.904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Griffiths W.T. Protochlorophyllide Photoreduction. In: Scheer H., editor. Chlorophylls. Boca Raton: CRC Press; 1991. pp. 433–450. [Google Scholar]
  10. Holtorf H., Reinbothe S., Reinbothe C., Bereza B., Apel K. Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.) Proc. Natl. Acad. Sci. USA. 1995;92:3254–3258. doi: 10.1073/pnas.92.8.3254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. John P.C.L., Sek F.J., Carmichael J.P., McCurdy D.W. P34cdc2 homologue level, cell division, phytochrome responsiveness and cell differentiation in wheat leaves. J. Cell Sci. 1990;97:627–630. doi: 10.1242/jcs.97.4.627. [DOI] [PubMed] [Google Scholar]
  12. Kemp D.R. The location and site of the extension zone of emerging wheat leaves. New Phytol. 1980;84:729–737. doi: 10.1111/j.1469-8137.1980.tb04785.x. [DOI] [Google Scholar]
  13. Laemmli U.K. Cleavage of structural proteins during the assembly of head of bacteriophage T4. Nature. 1970;222:680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Liaaen-Jensen S., Jensen A. Quantitative determination of carotenoids in photosynthetic tissues. Meths. Enzymol. 1971;235:86–602. [Google Scholar]
  15. Lowry O.H., Rosenbrough N.J., Farr A.H., Randall G.J. Protein measurement with folin-phenol reagent. J. Biol. Chem. 1951;193:256–275. [PubMed] [Google Scholar]
  16. Nelson T., Langdale J.A. Developmental genetics of C4 photosynthesis. Ann. Rev. Plant Physio. Plant Mol. Biol. 1992;43:25–47. doi: 10.1146/annurev.pp.43.060192.000325. [DOI] [Google Scholar]
  17. Poethig R.S. Cellular parameters of leaf morphogenesis in maize and tobacco. In: White R.A., Dickson W.C., editors. Contemporary problems in plant anatomy. New York: Academic Press; 1984. pp. 235–239. [Google Scholar]
  18. Reinbothe S., Reinbothe C., Holtorf H., Apel K. Two NADPH: Protochlorophyllilde oxidoreductase in barley: Evidence for the selective disappearance of POR A during the light induced greening of etiolated seedlings. Plant Cell. 1995;7:1933–1940. doi: 10.1105/tpc.7.11.1933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rodermel S. Pathways of plastid-to-nucleus signaling. Trends Plant Sci. 2001;6:471–478. doi: 10.1016/S1360-1385(01)02085-4. [DOI] [PubMed] [Google Scholar]
  20. Sharma R., Sopory S.K., Guha-Mukherjee S. Phytochrome regulation of peroxidase activities in maize III. Age dependence and subcellular localization. Z. Pflanzenphysiol. 1979;94:371–375. [Google Scholar]
  21. Sylvester A.W., Cande W.L., Freeling M. Division and differentiation during normal and liguleless-1 in maize leaf development. Development. 1990;110:985–1000. doi: 10.1242/dev.110.3.985. [DOI] [PubMed] [Google Scholar]
  22. Thompson P., Bowsher C.G., Tobin A.K. Heterogeneity of Mitochondrial Protein Biogenesis during Primary Leaf Development in Barley. Plant Physiol. 1998;118:1089–1099. doi: 10.1104/pp.118.3.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tobin A.K., Sumar N., Patel M., Moore A.L., Stewart G.R. Development of photorespiration during chloroplast biogenesis in wheat leaves. J. Exp. Bot. 1988;39:833–843. doi: 10.1093/jxb/39.7.833. [DOI] [Google Scholar]
  24. Towbin H., Stahekin T., Gordon J. Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets. Proc. Natl. Acad. Sci. USA. 1979;76:4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Vally K.J.M., Selvi M.T., Sharma R. Light alters cytosolic and plastidic phosphorylase distribution in pearl millet (Pennisetum americanum) leaves. Plant Physiol. 1995;109:517–523. doi: 10.1104/pp.109.2.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Vernon L.P. Spectrophotometric determination of chlorophylls and phaeophytins in plant extracts. Anal. Chem. 1960;32:1144–1150. doi: 10.1021/ac60165a029. [DOI] [Google Scholar]
  27. Viro M., Kloppstech K. Differential expression of the genes for ribulose 1, 5-bisphosphate carboxylase and light harvesting complex chlorophyll a/b protein in the developing barley leaf. Planta. 1980;150:41–45. doi: 10.1007/BF00385613. [DOI] [PubMed] [Google Scholar]
  28. Wernicke W., Milkovits L. Effect of auxins on the mitotic cell cycle in cultured leaf segments at different stages of development in wheat. Physiol. Plant. 1987;69:16–22. doi: 10.1111/j.1399-3054.1987.tb01940.x. [DOI] [Google Scholar]
  29. Wernicke W., Milkovits L. Roles of uptake and metabolism of indole-3-acetic acid and 2–4 dichlorophenoxy acetic acid in cultured leaf segments at different stages of development in wheat. Physiol. Plant. 1987;69:23–28. doi: 10.1111/j.1399-3054.1987.tb01941.x. [DOI] [Google Scholar]

Articles from Physiology and molecular biology of plants : an international journal of functional plant biology are provided here courtesy of Springer

RESOURCES