title: Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis.
abstract: Here, we report that SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTER (SWEET16) from Arabidopsis (Arabidopsis thaliana) is a vacuole-located carrier, transporting glucose (Glc), fructose (Fru), and sucrose (Suc) after heterologous expression in Xenopus laevis oocytes. The SWEET16 gene, similar to the homologs gene SWEET17, is mainly expressed in vascular parenchyma cells. Application of Glc, Fru, or Suc, as well as cold, osmotic stress, or low nitrogen, provoke the down-regulation of SWEET16 messenger RNA accumulation. SWEET16 overexpressors (35SPro:SWEET16) showed a number of peculiarities related to differences in sugar accumulation, such as less Glc, Fru, and Suc at the end of the night. Under cold stress, 35SPro:SWEET16 plants are unable to accumulate Fru, while under nitrogen starvation, both Glc and Fru, but not Suc, were less abundant. These changes of individual sugars indicate that the consequences of an increased SWEET16 activity are dependent upon the type of external stimulus. Remarkably, 35SPro:SWEET16 lines showed improved germination and increased freezing tolerance. The latter observation, in combination with the modified sugar levels, points to a superior function of Glc and Suc for frost tolerance. 35SPro:SWEET16 plants exhibited increased growth efficiency when cultivated on soil and showed improved nitrogen use efficiency when nitrate was sufficiently available, while under conditions of limiting nitrogen, wild-type biomasses were higher than those of 35SPro:SWEET16 plants. Our results identify SWEET16 as a vacuolar sugar facilitator, demonstrate the substantial impact of SWEET16 overexpression on various critical plant traits, and imply that SWEET16 activity must be tightly regulated to allow optimal Arabidopsis development under nonfavorable conditions.
authors.affiliation: Plant Physiology , University of Kaiserslautern, D-67653 Kaiserslautern, Germany;
authors.forename: Patrick A W
authors.initials: PA
authors.lastname: Klemens
authors.forename: Kathrin
authors.initials: K
authors.lastname: Patzke
authors.forename: Joachim
authors.initials: J
authors.lastname: Deitmer
authors.forename: Lara
authors.initials: L
authors.lastname: Spinner
authors.forename: Rozenn
authors.initials: R
authors.lastname: Le Hir
authors.forename: Catherine
authors.initials: C
authors.lastname: Bellini
authors.forename: Magali
authors.initials: M
authors.lastname: Bedu
authors.forename: Fabien
authors.initials: F
authors.lastname: Chardon
authors.forename: Anne
authors.initials: A
authors.lastname: Krapp
authors.forename: H Ekkehard
authors.initials: HE
authors.lastname: Neuhaus
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics; D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D018533:Biomass; D015152:Blotting, Northern; D002352:Carrier Proteins / Q000235:genetics* / Q000378:metabolism; D003080:Cold Temperature; D015536:Down-Regulation / Q000187:drug effects; D005632:Fructose / Q000378:metabolism / Q000494:pharmacology; D018506:Gene Expression Regulation, Plant; D018525:Germination / Q000235:genetics; D005947:Glucose / Q000378:metabolism / Q000494:pharmacology; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D018613:Microscopy, Confocal; D009004:Monosaccharide Transport Proteins / Q000235:genetics* / Q000378:metabolism; D009154:Mutation; D009584:Nitrogen / Q000378:metabolism / Q000494:pharmacology; D009997:Osmotic Pressure; D030821:Plants, Genetically Modified; D020133:Reverse Transcriptase Polymerase Chain Reaction; D013395:Sucrose / Q000378:metabolism / Q000494:pharmacology; D014617:Vacuoles / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; D002352:Carrier Proteins; D009004:Monosaccharide Transport Proteins; C000589119:SWEET16 protein, Arabidopsis; D049452:Green Fluorescent Proteins; D005632:Fructose; D013395:Sucrose; D005947:Glucose; D009584:Nitrogen
references.citation: FEBS Lett. 2004 Oct 8;576(1-2):169-73
references.pmid: 15474032
references.citation: Plant Cell. 1997 Jan;9(1):5-19
references.pmid: 9014361
references.citation: Biochim Biophys Acta. 2000 May 1;1465(1-2):263-74
references.pmid: 10748259
references.citation: Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2537-42
references.pmid: 17284600
references.citation: Annu Rev Plant Biol. 2004;55:341-72
references.pmid: 15377224
references.citation: Plant J. 2011 Mar;65(5):757-70
references.pmid: 21261761
references.citation: Plant Physiol. 2011 Dec;157(4):1664-76
references.pmid: 21984725
references.citation: Plant Physiol. 2011 Nov;157(3):1255-82
references.pmid: 21900481
references.citation: New Phytol. 2013 May;198(3):777-787
references.pmid: 23488986
references.citation: Biochem J. 1999 Aug 1;341 ( Pt 3):529-35
references.pmid: 10417314
references.citation: Plant Physiol. 2010 May;153(1):260-72
references.pmid: 20207708
references.citation: Planta. 1989 Apr;177(4):535-46
references.pmid: 24212496
references.citation: Plant Mol Biol. 2008 May;67(1-2):151-67
references.pmid: 18278579
references.citation: FEBS Lett. 2007 May 25;581(12):2223-6
references.pmid: 17307167
references.citation: PLoS Genet. 2005 Aug;1(2):e26
references.pmid: 16121258
references.citation: Plant Physiol. 2001 Jan;125(1):61-4
references.pmid: 11154297
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540
references.pmid: 15012299
references.citation: Plant J. 2011 Dec;68(5):890-900
references.pmid: 21838775
references.citation: Plant Physiol. 1995 Feb;107(2):459-467
references.pmid: 12228372
references.citation: Nature. 2010 Nov 25;468(7323):527-32
references.pmid: 21107422
references.citation: Plant Cell. 2013 Feb;25(2):694-714
references.pmid: 23444331
references.citation: Plant Physiol. 1997 Sep;115(1):7-13
references.pmid: 12223788
references.citation: Planta. 1979 Dec;147(2):159-62
references.pmid: 24310973
references.citation: Plant J. 1998 Dec;16(6):735-43
references.pmid: 10069079
references.citation: Planta. 1984 Nov;161(6):562-8
references.pmid: 24253927
references.citation: FEBS Lett. 2005 Aug 1;579(19):4165-74
references.pmid: 16038907
references.citation: Plant Physiol. 2004 Sep;136(1):2483-99
references.pmid: 15375205
references.citation: Trends Biochem Sci. 1993 Jan;18(1):13-20
references.pmid: 8438231
references.citation: Trends Plant Sci. 2004 Dec;9(12):606-13
references.pmid: 15564128
references.citation: Plant Physiol. 2006 May;141(1):196-207
references.pmid: 16581873
references.citation: Plant Physiol. 1987 Feb;83(2):399-407
references.pmid: 16665257
references.citation: Plant Biotechnol J. 2012 Dec;10(9):1011-25
references.pmid: 22607381
references.citation: Plant Mol Biol. 2008 Oct;68(3):289-99
references.pmid: 18618272
references.citation: Nat Protoc. 2007;2(7):1565-72
references.pmid: 17585298
references.citation: Plant J. 2011 Oct;68(1):129-36
references.pmid: 21668536
references.citation: J Exp Bot. 2010 May;61(9):2293-302
references.pmid: 20237091
references.citation: Plant J. 2005 Aug;43(4):568-85
references.pmid: 16098110
references.citation: J Exp Bot. 2007;58(9):2369-87
references.pmid: 17556767
references.citation: Planta. 2004 Feb;218(4):579-88
references.pmid: 14648119
references.citation: Curr Opin Plant Biol. 2010 Dec;13(6):724-30
references.pmid: 20801076
references.citation: Plant Physiol. 1993 Nov;103(3):753-761
references.pmid: 12231977
references.citation: Genes Dev. 2000 Aug 15;14(16):2085-96
references.pmid: 10950871
references.citation: Plant Physiol. 2011 Sep;157(1):109-19
references.pmid: 21771914
references.citation: Annu Rev Plant Biol. 2012;63:183-213
references.pmid: 22404463
references.citation: J Exp Bot. 2007;58(1):83-102
references.pmid: 17110589
references.citation: Science. 2012 Jan 13;335(6065):207-11
references.pmid: 22157085
references.citation: Curr Opin Plant Biol. 2012 Feb;15(1):84-91
references.pmid: 22001935
references.citation: Curr Opin Plant Biol. 2001 Jun;4(3):247-53
references.pmid: 11312136
references.citation: Trends Plant Sci. 2002 May;7(5):193-5
references.pmid: 11992820
references.citation: Annu Rev Plant Biol. 2009;60:207-21
references.pmid: 19025382
references.citation: Plant J. 2007 Dec;52(6):1169-80
references.pmid: 18005230
references.citation: Trends Plant Sci. 2009 Oct;14(10):530-4
references.pmid: 19726217
references.citation: Plant Physiol. 2010 Oct;154(2):665-77
references.pmid: 20709831
references.citation: Plant Cell. 2006 Dec;18(12):3476-90
references.pmid: 17158605
references.citation: Plant Biol (Stuttg). 2012 Mar;14(2):325-36
references.pmid: 21972845
references.citation: Plant J. 2012 Feb;69(3):529-41
references.pmid: 21988472
references.citation: Front Plant Sci. 2013 Mar 12;4:44
references.pmid: 23487525
references.citation: Plant Physiol. 2005 Sep;139(1):5-17
references.pmid: 16166256
references.citation: Curr Biol. 2013 Apr 22;23(8):697-702
references.pmid: 23583552
references.citation: Plant Cell. 2002;14 Suppl:S185-205
references.pmid: 12045277
references.citation: J Biol Chem. 2010 Jan 8;285(2):1138-46
references.pmid: 19901034