Signaling from an altered cell wall to the nucleus mediates sugar-responsive growth and development in Arabidopsis thaliana.
Sugars such as glucose function as signal molecules that regulate gene expression, growth, and development in plants, animals, and yeast. To understand the molecular mechanisms of sugar responses, we isolated and characterized an Arabidopsis thaliana mutant, high sugar response8 (hsr8), which enhances sugar-responsive growth and gene expression. Light-grown hsr8 plants exhibited increased starch and anthocyanin and reduced chlorophyll content in response to glucose treatment. Dark-grown hsr8 seedlings showed glucose-hypersensitive hypocotyl elongation and development. The HSR8 gene, isolated using map-based cloning, was allelic to the MURUS4 (MUR4) gene involved in arabinose synthesis. Dark-grown mur1 and mur3 seedlings also exhibited similar sugar responses to hsr8/mur4. The sugar-hypersensitive phenotypes of hsr8/mur4, mur1, and mur3 were rescued by boric acid, suggesting that alterations in the cell wall cause hypersensitive sugar-responsive phenotypes. Genetic analysis showed that sugar-hypersensitive responses in hsr8 mutants were suppressed by pleiotropic regulatory locus1 (prl1), indicating that nucleus-localized PRL1 is required for enhanced sugar responses in hsr8 mutant plants. Microarray analysis revealed that the expression of many cell wall-related and sugar-responsive genes was altered in mur4-1, and the expression of a significant proportion of these genes was restored to wild-type levels in the mur4-1 prl1 double mutant. These findings reveal a pathway that signals changes in the cell wall through PRL1 to altered gene expression and sugar-responsive metabolic, growth, and developmental changes.
Li
Yunhai
Y
Department of Cell and Developmental Biology, John Ines Centre, Norwich NR4 7UH, United Kingdom.
Smith
Caroline
C
Corke
Fiona
F
Zheng
Leiying
L
Merali
Zara
Z
Ryden
Peter
P
Derbyshire
Paul
P
Waldron
Keith
K
Bevan
Michael W
MW
D000872:Anthocyanins / Q000378:metabolism; D017360:Arabidopsis / Q000166:cytology* / Q000187:drug effects / Q000235:genetics / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D001089:Arabinose / Q000494:pharmacology; D001888:Boric Acids / Q000494:pharmacology; D002241:Carbohydrates / Q000494:pharmacology*; D002467:Cell Nucleus / Q000187:drug effects / Q000378:metabolism*; D002473:Cell Wall / Q000187:drug effects / Q000378:metabolism*; D002734:Chlorophyll / Q000378:metabolism; D003001:Cloning, Molecular; D003624:Darkness; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D005947:Glucose / Q000494:pharmacology; D018546:Hypocotyl / Q000166:cytology / Q000187:drug effects; D009154:Mutation / Q000235:genetics; D010641:Phenotype; D036226:Seedlings / Q000166:cytology / Q000187:drug effects / Q000254:growth & development; D015398:Signal Transduction / Q000187:drug effects*; D013213:Starch / Q000378:metabolism
D000872:Anthocyanins; D029681:Arabidopsis Proteins; D001888:Boric Acids; D002241:Carbohydrates; D002734:Chlorophyll; D013213:Starch; D001089:Arabinose; D005947:Glucose; C032688:boric acid
Trends Plant Sci. 2003 Mar;8(3):110-6
12663220
Plant Physiol. 2002 Feb;128(2):482-90
11842152
Plant Physiol. 2002 Feb;128(2):472-81
11842151
Genes Dev. 2000 Aug 15;14(16):2085-96
10950871
Yeast. 2001 Oct;18(14):1309-16
11571755
Curr Opin Plant Biol. 1998 Jun;1(3):230-4
10066585
Biochem Soc Trans. 2005 Feb;33(Pt 1):269-71
15667323
Plant Physiol. 1949 Jan;24(1):1-15
16654194
Nature. 2002 Nov 21;420(6913):337-40
12447444
EMBO J. 2004 Apr 21;23(8):1900-10
15057278
Plant J. 2004 Mar;37(6):914-39
14996223
Plant J. 2000 Sep;23(5):587-96
10972885
Annu Rev Plant Biol. 2006;57:675-709
16669778
Curr Opin Microbiol. 1999 Apr;2(2):202-7
10322167
Plant Physiol. 2006 Jan;140(1):49-58
16377743
Nature. 2003 Oct 2;425(6957):521-5
14523448
Plant Cell. 2002 Jul;14(7):1557-66
12119374
Plant Mol Biol. 2001 Sep;47(1-2):161-76
11554470
Plant Physiol. 2001 Nov;127(3):842-51
11706167
Plant J. 1996 Jun;9(6):919-25
8696368
Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):2085-90
9050909
Microbiol Mol Biol Rev. 1998 Jun;62(2):334-61
9618445
Science. 1998 Jan 30;279(5351):717-20
9445479
Plant Cell. 2003 Jul;15(7):1662-70
12837954
Curr Biol. 2007 Jun 5;17(11):922-31
17540573
Science. 2003 Aug 15;301(5635):969-72
12920300
Plant J. 2003 May;34(3):351-62
12713541
Anal Biochem. 1979 Jul 15;96(2):282-92
474957
Plant J. 1999 Dec;20(5):581-90
10652130
Plant Cell. 2005 Dec;17(12):3257-81
16299223
Plant Cell. 2006 Apr;18(4):893-906
16517759
Genomics. 1994 Jan 1;19(1):137-44
8188214
Plant Mol Biol. 2004 Jul;55(4):467-77
15604693
Plant Physiol. 1994 Jun;105(2):681-689
12232235
Mol Gen Genet. 1980;178(3):633-7
6993859
Science. 2003 Apr 11;300(5617):332-6
12690200
Science. 1999 Jun 25;284(5423):2148-52
10381874
Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:481-500
15012243
Curr Opin Plant Biol. 2003 Dec;6(6):611-6
14611961
FEBS Lett. 2004 Aug 27;573(1-3):83-92
15327980
Plant Cell. 2006 May;18(5):1226-38
16582010
Biochem J. 1962 Nov;85:383-8
14002491
Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10294-9
9707641
Plant Physiol. 2000 Jan;122(1):3-10
10631243
Plant J. 1993 Aug;4(2):403-10
8106085
Plant J. 1997 Aug;12(2):335-45
9301086
Science. 2001 Oct 26;294(5543):846-9
11679668
Plant Cell. 2006 Jul;18(7):1630-41
16766693
Biochem J. 1967 Oct;105(1):1C-2C
6069833
Genome Res. 2006 Mar;16(3):414-27
16424108
Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5322-7
10220464
Plant Cell. 2003 Feb;15(2):523-31
12566589
Plant Cell. 2004 Aug;16(8):2128-50
15273295
EMBO J. 2001 Jun 1;20(11):2742-56
11387208
Plant Cell. 2002 Nov;14(11):2723-43
12417697
Mol Cell Biol. 2000 Jul;20(13):4513-21
10848578
Plant J. 2006 Jun;46(6):1045-58
16805736
Plant J. 1993 Jan;3(1):1-30
8401598
Plant J. 2006 Jul;47(1):49-62
16740149
Plant J. 2000 Sep;23(5):577-85
10972884
J Exp Bot. 2000 Feb;51 Spec No:407-16
10938849
Plant Mol Biol. 1998 Jul;37(5):735-48
9678569
Plant Cell. 2000 Dec;12(12):2409-2424
11148287
Mol Cell. 2004 Oct 22;16(2):293-9
15494315
Plant Cell. 2002;14 Suppl:S185-205
12045277
Genes Dev. 1998 Oct 1;12(19):3059-73
9765207
Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):3340-5
11854459
Plant Physiol. 1995 Mar;107(3):895-904
7716246
Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):17197-202
12486248
Plant J. 2001 May;26(4):421-33
11439129
Plant Physiol. 2004 Jan;134(1):81-91
14684841
Plant Physiol. 1999 Oct;121(2):383-9
10517829
Plant Cell. 2005 Nov;17(11):3051-65
16199618
Plant J. 2001 Apr;26(2):205-16
11389761
Science. 2004 Dec 24;306(5705):2206-11
15618507
Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540
15012299
Curr Opin Plant Biol. 2005 Feb;8(1):93-102
15653406