HORT640 - Metabolic Plant Physiology
Quaternary ammonium and tertiary sulfonium compounds
Pathway(s) of choline synthesis
In higher plants, choline is derived from the amino acid serine, by decarboxylation of serine to ethanolamine (Rontein et al, 2001):
serine + H+ ---> CO2 + ethanolamine
The NH2- moiety of ethanolamine (EA) is then N-methylated to (CH3)3-N+- at the level of either free ethanolamine bases, O-phospho-ethanolamine bases, or O-phosphatidyl-ethanolamine bases, catalyzed by S-adenosylmethionine (SAM; AdoMet)-dependent N-methyltransferases (Rhodes and Hanson, 1993; Gorham, 1995; Hanson et al, 1995).
In castor bean, synthesis of phosphatidyl-ethanolamine occurs via the sequence ethanolamine kinase [EC 188.8.131.52], CTP:ethanolaminephosphate cytidylyltransferase [EC 184.108.40.206] and diacylglycerol:CDPethanolamine ethanolaminephosphotransferase [EC 220.127.116.11] (Tang and Moore, 1997).
Datko and Mudd (1988ab) have proposed phosphoethanolamine (P-EA) as a common committing step in the synthesis of choline moieties in plants, implicating ethanolamine kinase as a key enzyme in this pathway:
Ethanolamine kinase [EC 18.104.22.168]
EA + ATP ---> P-EA + ADP
In glycinebetaine-accumulating chenopods the main pathway of choline synthesis appears to be via the phospho-bases; P-EA, P-MMEA, P-DMEA and P-choline (Hanson and Rhodes, 1983; Hanson et al, 1995):
P-EA + SAM ---> P-MMEA + SAHC
P-MMEA + SAM ---> P-DMEA + SAHC
P-DMEA + SAM ---> P-choline + SAHC
(where SAHC = S-adenosylhomocysteine). Consistent with this, a spinach phosphoethanolamine N-methyltransferase (P-EAMT) cDNA was isolated by functional complementation of a Schizosaccharomyces pombe cho2(-) mutant and was shown to encode a protein with P-EAMT activity, but without EA- or Ptd-EA N-methyltransferase activity (Nuccio et al, 2000). P-EAMT catalyzes not only the first N-methylation of P-EA but also the two subsequent N-methylations, yielding P-choline. P-MMEA and P-DMEA were detected as reaction intermediates (Nuccio et al, 2000). A truncated enzyme lacking the C-terminal methyltransferase domain catalyzes only the first methylation (Nuccio et al, 2000). P-choline is an inhibitor of P-EAMT (Nuccio et al, 2000). This is consistent with radiotracer evidence that P-choline may feedback inhibit its own synthesis in sugar beet (Hanson and Rhodes, 1983). Salinization of spinach plants increases P-EAMT mRNA abundance and enzyme activity in leaves by about 10-fold, consistent with the high demand in stressed plants for choline to support glycinebetaine synthesis (Nuccio et al, 2000). This supports evidence that the phospho-base methyltransferase(s) activities are induced by salinity stress in spinach (Weretilnyk and Summers, 1992; Hanson et al, 1995; Weretilnyk et al, 1995). Choline down-regulates its own synthesis at the level of the P-MMEA and P-DMEA N-methyltransferases (Mudd and Datko, 1989ab).
In spinach it is proposed that choline is liberated from P-choline by a phosphocholine phosphatase, or the reverse reaction of choline kinase (Rhodes and Hanson, 1993; Hanson et al, 1995):
P-choline ---> choline + Pi
In tobacco, radiotracer evidence suggests that the first methylation step occurs solely at the phospho-base level (McNeil et al, 2000). The second and third methylations occur mainly (83%-92% and 65%-85%, respectively) at the phospho-base level, with the remainder occurring at the phosphatidyl-base level (McNeil et al, 2000). In tobacco, free choline originates predominantly from Ptd-choline rather than from P-choline (McNeil et al, 2000).
Similarly, in grasses, P-choline is incorporated into Ptd-choline from which choline is then released (Giddings and Hanson, 1982; Hitz et al, 1991), presumably by the action of phospholipase D [EC 22.214.171.124] (Rhodes and Hanson, 1993). Phospholipase D (PLD) is activated by glucose starvation in carrot suspension cells; ethylene is implicated as an element in the signal transduction pathway leading from glucose depletion to PLD activation (Lee et al, 1998) [PLD-deficient transgenic plants of Arabidopsis have a slower rate of ethylene- and ABA-promoted senescence (Fan et al, 1997)].
Datko AH, Mudd SH 1988a Phosphatidylcholine synthesis: differing patterns in soybean and carrot. Plant Physiol. 88: 854-861.
Datko AH, Mudd SH 1988b Enzymes of phosphatidylcholine synthesis in Lemna, soybean and carrot. Plant Physiol. 88: 1338-1348.
Fan L, Zheng S, Wang X 1997 Antisense suppression of phospholipase Dalpha retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9: 2183-2196.
Gorham J 1995 Betaines in higher plants - biosynthesis and role in stress metabolism. In (RM Wallsgrove ed) "Amino acids and Their Derivatives in Higher Plants." Society for Experimental Biology Seminar Series, Vol 56, Cambridge University Press, Cambridge, pp. 173-203.
Hanson AD, Rhodes D 1983 14C-Tracer evidence for synthesis of choline and betaine via phosphoryl base intermediates in salinized sugarbeet leaves. Plant Physiol. 71: 692-700.
Hanson AD, Rivoal J, Burnet M, Rathinasabapathi B 1995 Biosynthesis of quaternary ammonium and tertiary sulphonium compounds in response to water deficit. In (N Smirnoff ed) "Environment and Plant Metabolism: Flexibility and Acclimation" Bios Scientific, Oxford, pp. 189-198.
Hitz WD, Rhodes D, Hanson AD 1981 Radiotracer evidence implicating phosphoryl and phosphatidyl bases as intermediates in betaine synthesis by water-stressed barley leaves. Plant Physiol. 68: 814-822.
Lee SH, Chae HS, Lee TK, Kim SH, Shin SH, Cho BH, Cho SH, Kang BG, Lee WS 1998 Ethylene-mediated phospholipid catabolic pathway in glucose-starved carrot suspension cells. Plant Physiol. 116: 223-229.
McNeil SD, Nuccio ML, Rhodes D, Shachar-Hill Y, Hanson AD 2000 Radiotracer and computer modeling evidence that phosphobase methylation is the main route of choline synthesis in tobacco. Plant Physiol. 123: 371-380.
Mudd SH, Datko AH 1989a Synthesis of methylated ethanolamine moieties. Regulation by choline in Lemna. Plant Physiol. 90: 296-305.
Mudd SH, Datko AH 1989b Synthesis of methylated ethanolamine moieties. Regulation by choline in soybean and carrot. Plant Physiol. 90: 306-310.
Nuccio ML, Ziemak MJ, Henry SA, Weretilnyk EA, Hanson AD 2000 cDNA cloning of phosphoethanolamine N-methyltransferase from spinach by complementation in Schizosaccharomyces pombe and characterization of the recombinant enzyme. J. Biol. Chem. 275: 14095-14101.
Rhodes D, Hanson AD 1993 Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 357-384.
Rontein D, Nishida I, Tashiro G, Yoshioka K, Wu WI, Voelker DR, Basset G, Hanson AD 2001 Plants synthesize ethanolamine by direct decarboxylation of serine using a pyridoxal phosphate enzyme. J. Biol. Chem. 276: 35523-35529.
Tang F, Moore TSJr 1997 Enzymes of the primary phosphatidylethanolamine biosynthetic pathway in postgermination castor bean endosperm. Developmental profiles of the mitochondrial CTP:ethanolaminephosphate cytidylyltransferase. Plant Physiol. 115: 1589-1597.
Weretilnyk EA, Smith DN, Wilch GA, Summers PS 1995 Enzymes of choline synthesis in spinach: Response of phospho-base N-methyltransferase activities to light and salinity. Plant Physiol. 109: 1085-1091.
Weretilnyk EA, Summers PS 1992 Betaine and choline metabolism in higher plants. In (BK Singh, HE Flores, JC Shannon eds) "Biosynthesis and Molecular Regulation of Amino Acids in Plants." American Society of Plant Physiologists, Waverly Press, Baltimore, pp. 89-97.
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