A protein disulfide-thiol interchange protein with NADH: protein disulfide reductase (NADH oxidase) activity as a molecular target for low levels of exposure to organic solvents in plant growth

Abstract

A number of solvents including ethyl, amyl, butyl, octyl and benzyl alcohols, ethylene glycol, ethyl acetate, acetone, diethyl ether, propylene oxide, r-dioxane, benzene, xylene, chloroform and carbon tetrachloride stimulate the growth of plants or plant parts at low concentrations and inhibit at high concentrations. These same solvents, at low dilutions, stimulate the activity of a growth-related protein disulfide-thiol interchange protein (TIP) with NADH: protein disulfide reductase (NADH oxidase) (NOX) activity with plasma membrane vesicles isolated from elongating regions cut from dark grown seedlings of soybeans. Based on these and other findings, we suggest the TIP/NOX protein to be the molecular target of the biological effects of low levels of exposure (hormesis) involved in the stimulation of plant growth.

Keywords

NADH oxidase chemical hormesis plant growth protein disulfide-thiol interchange organic solvents

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References

Calabrese EJ , Baldwin LA. Possible examples of chemical hormesis in a previously published study . J Appl Tox 1993; 13: 169-172 .

Danielli JF. Cell Physiology and Pharmacology, Elsevier, New York , 1950.

Ferguson J , Pirie H. The toxicity of vapours to the grain weevil . Ann Appl Biol 1948; 35: 532-532 .

James WO. The use of respiratory inhibitors . Ann Rev Plant Physiol 1953; 4: 59-90 .

Van Overbeek J , Blondeau R. Mode of action of phytotoxic oils . Weeds 1954; 3: 55-65 .

Morré DJ , Navas P , Penel C , Castillo FJ. Auxin-stimulated NADH oxidase (semidehydroascorbate reductase) of soybean plasma membrane: role in acidification of cytoplasm . Protoplasma 1986; 133: 195-197 .

Morré DJ , Chueh P-J , Morré DM. Capsaicin inhibits preferentially the NADH oxidase and growth of transformed cells in culture . Proc Natl Acad Sci USA 1995; 92: 1831-1835 .

Chueh P-J et al. The hormone-responsive NADH oxidase of the plant plasma membrane has properties of a NADH: protein disulfide reductase . J Biol Chem 1997; 272: 11221-11227 .

DeHahn T , Barr R , Morré DJ. NADH oxidase activity present on both the external and internal surfaces of soybean plasma membranes . Biochim Biophys Acta 1997; 1328: 99-108 .

10.

Morré DJ. Hormone- and growth factor-stimulated NADH oxidase . J Bioenerg Biomemb 1994; 26: 421-433 .

11.

Chueh P-J et al. A 33.5 kD heat-and protease-resistant NADH oxidase inhibited by capsaicin specific to sera of cancer patients . Arch Biochem Biophys 1997; 342: 38-47 .

12.

Morré DJ , Rogers BY , Gamble R. Promotion of plant growth by long chain alcohols and organic solvents . Phyton 1965; 22: 7-12 .

13.

Moskwa Z , Ber A. The influence of organic solvents on the growth of plants . Experientia 1951; 7: 136-136 .

14.

Albertsson P-A , Andersson B , Larsson C , Askerlund H-E. Phase partition - a method for purification and analysis of cell organelles and membrane vesicles . Meth. Biochem. Anal.1982; 28: 115-150 .

15.

Kjellbom P , Larsson C. Preparation and polypeptide composition of chlorophyll-free plasma membranes from leaves of light-grown spinach and barley . Physiol Plant 1984; 62: 501-509 .

16.

Sandelius AS , Morré DJ. Plasma membrane isolation methods, C Larrson , IM Moller , (eds.,) The Plant Plasma Membrane - Structure, Function and Molecular Biology, Springer Verlag: New York . pp. 44-75, 1990.

17.

Mer CL. Growth promoting effect of ethanol on oat seedlings . Nature 1958; 182: 1812-1813 .

18.

MorréDJ et al. Role of plasma membrane redox activities in elongation growth in plants . Physiol Plant 1988; 73: 187-193 .

19.

Morré DJ , Brightman AO. NADH oxidase of plasma membranes . J Bioenerg Biomemb 1991; 23: 469-489 .

20.

Hicks C, Morré DJ (Submitted): Oxidation of NADH by intact segments of soybean hypocotyls and stimulation by 2,4-D.

21.

Morré DJ , de Cabo R , Jacobs E , Morré DM. Auxin-modulated protein disulfide-thiol-interchange activity from soybean plasma membranes . Plant Physiol 1995; 109: 573-578 .

22.

MorréDJ et al. Inhibition of plasma membrane redox activities and elongation growth of soybean . Physiol Plant 1988; 72: 236-240 .

23.

Ries SK. Regulation of plant growth with triacontanol . CRC Crit Rev Plant Sci 1986; 2: 239-285 .

24.

Crosby DG , Vlitos AJ. New auxins from `Maryland Mammoth' tobacco: In Plant Growth Regulation, RM Klein , (ed.) Iowa State University Press: Ames , pp 57-69, 1961.

25.

Vlitos AJ , Crosby DG. Isolation of fatty alcohols with plant-growth promoting activity from Maryland Mammoth tobacco . Nature 1959; 184: 462-463 .

26.

Vlitos AJ , Cutler HG. Plant growth regulating activity of cuticular waxes of sugar cane . Plant Physiol 1960; (Suppl.) 35: VI-VI .

27.

Struckmeyer BE , Roberts RH. The inhibition of abnormal cell proliferation with antiauxin . Am J Bot 1955; 42: 401-401 .

28.

Stowe BB. The stimulation of auxin action by lipides. In: Plant Growth Regulation, RM Klein (ed), Iowa State University Press: Ames , pp 419-429, 1961.

29.

Stowe BB , Obreitter JB. Growth promotion in pea stem sections. II. By natural oils and isoprenoid vitamins . Plant Physiol 1962; 37: 158-164 .

30.

Hemberg T. The effect of vitamin K and vitamin H1 on the root formation in cuttings of Phaseolus vulgaris L . Physiol Plant 1953; 6: 17-20 .

31.

Haagen-Smit AJ , Viglierchio DR. Investigation of plant wound hormones . Rec Trav Chim 1955; 74: 1197-1206 .

32.

Ries SK , Wert VF , Sweeley CC , Leavitt RA. Triacontanol: a new naturally occurring plant growth regulator . Science 1977; 195: 1339-1340 .

33.

Morré DJ , Sellden G , Zhu XZ , Brightman AO. Triacontanol stimulates NADH oxidase of soybean hypocotyl plasma membrane . Plant Sci 1991; 79: 31-36 .

34.

Laughlin RG , Munyon RL , Ries SK , Wert VF. Growth enhancement of plants by femtomole doses of colloidally dispersed-triacontanol . Science 1983; 219: 1219-1221 .

35.

Morré DJ. A lysolipid cascade in signal transduction cycle of growth control, DJ Morré , WF Boss , FA Loewus (eds.). Inositol Metabolism in Plants, Wiley-Liss: New York . pp 227-257, 1990.

36.

Brightman AO , Zhu X-Z , Morré DJ. Activation of plasma membrane NADH oxidase activity by products of phospholipase A . Plant Physiol 1991; 96: 1314-1320 .

37.

Brightman AO et al. A growth factor- and hormone-stimulated NADH oxidase from rat liver membrane . Biochim. Biophys. Acta 1992; 1105: 109-117 .

38.

Bruno et al. Stimulation of NADH oxidase activity from rat liver plasma membranes by growth factors and hormones is decreased or absent with hepatoma plasma membranes . Biochem J 1992; 284: 625-628 .

39.

Morré DJ , Wu L-Y , Morré DM. The antitumor sulfonylurea (N-(4-methylphenylsulfonyl)-N'-(4- chlorophenyl)urea (LY181984) inhibits NADH oxidase activity of HeLa plasma membranes . Biochim. Biophys. Acta 1995; 1240: 11-17 .

40.

Morré DJ. NADH oxidase activity of HeLa plasma membranes inhibited by the antitumor sulfonylurea N-(4-methylphenylsulfonyl)-N'-(4- chlorophenyl) urea (LY181984) at an external site . Biochim. Biophys. Acta 1995; 1240: 201-208 .

41.

MorréDJ et al. Capsaicin inhibits plasma membrane NADH oxidase and growth of human and mouse melanoma lines . Eur J Cancer 1996; 32A: 1995-2003 .

42.

MorréDJ et al. Is the drug-responsive NADH oxidase of the cancer cell plasma membrane a molecular target for adriamycin ? J Bioenerg Biomemb 1997; 29: 269-280 .

43.

Baserga R. The Biology of Cell Reproduction. Cambridge, Harvard University Press , 1985.

44.

Morré DM , Morré DJ. Mechanism of killing of HeLa cells by the antitumor sulfonylurea, N-(4- methylphenylsulfonyl)-N'-(4-chlorophenyl)urea (LY181984) . Protoplasma 1995; 184: 188-195 .

45.

Wolvetang EJ et al. Apoptosis induced by inhibitors of the plasma membrane NADH-oxidase involves Bcl-2 and calcineurin . Cell Growth Diff 1996; 7: 1315-1325 .

46.

Vichi P , Tritton TR. Stimulation of growth in murine and human cells by adriamycin . Can Res 1989; 49: 2679-2682 .

47.

Del Castillo-Olivares A et al. A drug-responsive and protease-resistant 34 kD NADH oxidase from the surface of HeLa cells. In preparation.

48.

MorréDJ et al. Antitumor sulfonylurea-inhibited NADH oxidase of cultured HeLa cells shed into media . Biochim Biophys Acta 1996; 1280: 197-206 .