Enzymatic control of anhydrobiosis-related accumulation of trehalose in the sleeping chironomid, Polypedilum vanderplanki.
Larvae of an anhydrobiotic insect, Polypedilum vanderplanki, accumulate very large amounts of trehalose as a compatible solute on desiccation, but the molecular mechanisms underlying this accumulation are unclear. We therefore isolated the genes coding for trehalose metabolism enzymes, i.e. trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphate phosphatase (TPP) for the synthesis step, and trehalase (TREH) for the degradation step. Although computational prediction indicated that the alternative splicing variants (PvTpsα/β) obtained encoded probable functional motifs consisting of a typical consensus domain of TPS and a conserved sequence of TPP, PvTpsα did not exert activity as TPP, but only as TPS. Instead, a distinct gene (PvTpp) obtained expressed TPP activity. Previous reports have suggested that insect TPS is, exceptionally, a bifunctional enzyme governing both TPS and TPP. In this article, we propose that TPS and TPP activities in insects can be attributed to discrete genes. The translated product of the TREH ortholog (PvTreh) certainly degraded trehalose to glucose. Trehalose was synthesized abundantly, consistent with increased activities of TPS and TPP and suppressed TREH activity. These results show that trehalose accumulation observed during anhydrobiosis induction in desiccating larvae can be attributed to the activation of the trehalose synthetic pathway and to the depression of trehalose hydrolysis.
Mitsumasu
Kanako
K
Anhydrobiosis Research Unit, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan.
Kanamori
Yasushi
Y
Fujita
Mika
M
Iwata
Ken-ichi
K
Tanaka
Daisuke
D
Kikuta
Shingo
S
Watanabe
Masahiko
M
Cornette
Richard
R
Okuda
Takashi
T
Kikawada
Takahiro
T
D000818:Animals; D002683:Chironomidae / Q000201:enzymology* / Q000502:physiology; D003681:Dehydration / Q000201:enzymology* / Q000235:genetics; D005964:Glucosyltransferases / Q000235:genetics; D006868:Hydrolysis; D007814:Larva / Q000502:physiology; D053858:Metabolic Networks and Pathways / Q000235:genetics; D008969:Molecular Sequence Data; D010744:Phosphoric Monoester Hydrolases / Q000235:genetics; D012890:Sleep / Q000502:physiology*; D014198:Trehalase / Q000235:genetics / Q000378:metabolism*
D005964:Glucosyltransferases; C023180:trehalose-6-phosphate synthase; C023178:trehalose-phosphatase; D010744:Phosphoric Monoester Hydrolases; D014198:Trehalase
J Biol Chem. 1998 Dec 11;273(50):33311-9
9837904
J Exp Biol. 2004 Aug;207(Pt 18):3125-9
15299033
Annu Rev Physiol. 1998;60:73-103
9558455
Glycobiology. 2009 Mar;19(3):250-7
19004876
Biochem Biophys Res Commun. 2006 Sep 15;348(1):56-61
16875677
J Exp Biol. 2003 Jul;206(Pt 13):2281-6
12771176
J Insect Physiol. 2005 Jun;51(6):727-31
15993133
J Exp Bot. 2001 Sep;52(362):1817-26
11520870
J Exp Biol. 2002 Sep;205(Pt 18):2799-802
12177145
BMC Genomics. 2003 Nov 13;4(1):45
14614785
Comp Biochem Physiol B Biochem Mol Biol. 2001 Apr;128(4):613-24
11290443
BMC Mol Biol. 2008 May 20;9:51
18492231
Appl Environ Microbiol. 1999 May;65(5):2020-4
10223994
BMC Evol Biol. 2006 Dec 19;6:109
17178000
Biotechnol Prog. 2005 Mar-Apr;21(2):617-20
15801808
J Biol Chem. 1993 Mar 5;268(7):4766-74
8444853
J Biol Chem. 1989 Sep 25;264(27):16165-9
2777784
Plant J. 1998 Mar;13(5):673-83
9681009
Nature. 2003 Oct 23;425(6960):859-64
14574415
Comp Biochem Physiol C Toxicol Pharmacol. 2003 Apr;134(4):513-20
12727301
Arch Microbiol. 2000 Oct;174(4):217-24
11081789
Yeast. 1995 Sep 15;11(11):1015-25
7502577
Biosci Biotechnol Biochem. 2007 Sep;71(9):2256-65
17827701
Biochim Biophys Acta. 2008 Feb;1780(2):289-97
18166160
FEBS J. 2007 Mar;274(5):1192-201
17257172
Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11585-90
17606922
Biochim Biophys Acta. 1994 Aug 2;1218(3):366-74
7519445
Annu Rev Plant Biol. 2008;59:417-41
18257709
Braz J Med Biol Res. 2002 Jan;35(1):11-6
11743609
Insect Biochem Mol Biol. 2008 Aug;38(8):788-95
18625402
Biochimie. 2005 Jun;87(6):565-74
15935281
Int J Parasitol. 2003 Sep 30;33(11):1195-206
13678635
Proc Natl Acad Sci U S A. 2008 Apr 1;105(13):5093-8
18362351
J Biol Chem. 1990 Sep 5;265(25):15034-9
1697585
Mol Microbiol. 1997 May;24(4):687-95
9194697
J Biol Chem. 1987 Sep 25;262(27):13212-8
2820965
Integr Comp Biol. 2005 Nov;45(5):710-4
21676821
Saline Syst. 2008 Dec 12;4:18
19077285
Plant Physiol. 1999 Apr;119(4):1473-82
10198107
Eur J Biochem. 1993 Mar 1;212(2):315-23
8444170
Eur J Biochem. 1992 Nov 1;209(3):951-9
1425702
Zoolog Sci. 2008 Jul;25(7):693-8
18828655
Insect Mol Biol. 2005 Oct;14(5):501-8
16164606
FEBS J. 2008 Jan;275(2):281-8
18070104
Eur J Biochem. 1993 Sep 15;216(3):849-61
8404905
Plant Physiol. 2001 Feb;125(2):1086-93
11161063
FEBS Lett. 2003 Oct 23;553(3):387-90
14572656
J Insect Physiol. 2007 Jun;53(6):573-9
17434182