Signaling Role of Fructose Mediated by FINS1/FBP in
Sugars are evolutionarily conserved signaling molecules that regulate the growth and development of both unicellular and multicellular organisms. As sugar-producing photosynthetic organisms, plants utilize glucose as one of their major signaling molecules. However, the details of other sugar signaling molecules and their regulatory factors have remained elusive, due to the complexity of the metabolite and hormone interactions that control physiological and developmental programs in plants. We combined information from a gain-of-function cell-based screen and a loss-of-function reverse-genetic analysis to demonstrate that fructose acts as a signaling molecule in Arabidopsis thaliana. Fructose signaling induced seedling developmental arrest and interacted with plant stress hormone signaling in a manner similar to that of glucose. For fructose signaling responses, the plant glucose sensor HEXOKINASE1 (HXK1) was dispensable, while FRUCTOSE INSENSITIVE1 (FINS1), a putative FRUCTOSE-1,6-BISPHOSPHATASE, played a crucial role. Interestingly, FINS1 function in fructose signaling appeared to be independent of its catalytic activity in sugar metabolism. Genetic analysis further indicated that FINS1–dependent fructose signaling may act downstream of the abscisic acid pathway, in spite of the fact that HXK1–dependent glucose signaling works upstream of hormone synthesis. Our findings revealed that multiple layers of controls by fructose, glucose, and abscisic acid finely tune the plant autotrophic transition and modulate early seedling establishment after seed germination.
Vyšlo v časopise:
Signaling Role of Fructose Mediated by FINS1/FBP in. PLoS Genet 7(1): e32767. doi:10.1371/journal.pgen.1001263
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001263
Souhrn
Sugars are evolutionarily conserved signaling molecules that regulate the growth and development of both unicellular and multicellular organisms. As sugar-producing photosynthetic organisms, plants utilize glucose as one of their major signaling molecules. However, the details of other sugar signaling molecules and their regulatory factors have remained elusive, due to the complexity of the metabolite and hormone interactions that control physiological and developmental programs in plants. We combined information from a gain-of-function cell-based screen and a loss-of-function reverse-genetic analysis to demonstrate that fructose acts as a signaling molecule in Arabidopsis thaliana. Fructose signaling induced seedling developmental arrest and interacted with plant stress hormone signaling in a manner similar to that of glucose. For fructose signaling responses, the plant glucose sensor HEXOKINASE1 (HXK1) was dispensable, while FRUCTOSE INSENSITIVE1 (FINS1), a putative FRUCTOSE-1,6-BISPHOSPHATASE, played a crucial role. Interestingly, FINS1 function in fructose signaling appeared to be independent of its catalytic activity in sugar metabolism. Genetic analysis further indicated that FINS1–dependent fructose signaling may act downstream of the abscisic acid pathway, in spite of the fact that HXK1–dependent glucose signaling works upstream of hormone synthesis. Our findings revealed that multiple layers of controls by fructose, glucose, and abscisic acid finely tune the plant autotrophic transition and modulate early seedling establishment after seed germination.
Zdroje
1. SmeekensS
2000 Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51 49 81
2. RollandF
Baena-GonzalezE
SheenJ
2006 Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annu Rev Plant Biol 57 675 709
3. RamonM
RollandF
SheenJ
2008 Sugar sensing and signaling. The Arabidopsis book (TAB), ISSN: 1543–8120, 1–22
4. SantangeloGM
2006 Glucose signaling in Saccharomyces cerevisiae. Microbiology and Mol Biol Reviews 70 253 282
5. HermanMA
KahnBB
2006 Glucose transport and sensing in the maintenance of glucose homeostasis and metabolic harmony. J Clin Invest 116 1767 1775
6. SchuitFC
HuypensP
HeimbergH
PipeleersDG
2001 Glucose sensing in pancreatic β-cells: A model for the study of other glucose regulated cells in gut, pancrease, hypothalamus. Diabetes 50 1 11
7. MooreB
ZhouL
RollandF
HallQ
ChengWH
2003 Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300 332 336
8. ChoYH
YooSD
SheenJ
2006 Regulatory functions of neclear hexokinase1 complex in glucose signaling. Cell 127 579 589
9. ChoYH
YooSD
SheenJ
2007 Glucose signaling through nuclear hexokinase1 complex in Arabidopsis. Plant Signaling and Behavior 2 123 124
10. ChiouTJ
BushDR
1998 Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci USA 95 4784 4788
11. RookF
GerritsN
KortsteeA
vanKampenM
BorriasM
1998 Sucrose-specific signaling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J 15 253 263
12. VaughnMW
HarringtonGN
BushDR
2002 Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proc Natl Acad Sci USA 99 10876 10880
13. PaulMJ
PrimavesiLF
JhurreeaD
ZhangY
2008 Trehalose metabolism and signaling. Annu Rev Plant Biol 59 417 441
14. Baena-GonzálezE
SheenJ
2008 Convergent energy and stress signaling. Trends in Plant Sci 13 474 482
15. HalfordNG
HeySJ
2009 Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419 247 259
16. GrahamIA
DenbyKJ
LeaverCJ
1994 Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. Plant Cell 6 761 772
17. JangJC
SheenJ
1994 Sugar sensing in higher plants. Plant Cell 6 1665 1679
18. JangJC
LeonP
ZhouL
SheenJ
1997 Hexokinase as a sugar sensor in higher plants. Plant Cell 9 5 19
19. Baena-GonzálezE
RollandF
TheveleinJM
SheenJ
2007 A central integrator of transcription networks in plant stress and energy signalling. Nature 448 938 943
20. ChoYH
SheenJ
YooSD
2010 Low glucose uncouples hexokinase1-dependent sugar signaling from stress and defense hormone abscisic acid and C2H4 responses in Arabidopsis. Plant Physiol 152 1180 1182
21. RutledgeAC
AdeliK
2007 Fructose and the metabolic syndrome: Pathophysiology and molecular mechanisms. Nutrition Reviews 65 S13 S23
22. WeiY
WangD
TopczewskiF
PagliassottiMJ
2007 Fructose-mediated stress signaling in the liver: implications for hepatic insulin resistance. J Nutr Biochem 18 1 9
23. KochK
2004 Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7 235 246
24. PegoJV
SmeekensS
2000 Plant fructokinases: A sweet family get together. Trends in Plant Sci 5 531 536
25. Kato-NoguchiH
TakaokaT
IzumoriK
2005 Psicose inhibits lettuce root growth via a hexokinase-independent pathway. Physiologia Plantarum 125 293 298
26. OdanakaS
BennettAB
KanayamaY
2002 Distinct physiological roles of fructokinase isozymes revealed by gene-specific suppression of Frk1 and Frk2 expression in tomato. Plant Physiol 129 1119 1126
27. GermanMA
DaiN
MatsevitzT
HanaelR
PetreikovM
2003 Suppression of fructokinase encoded by LeFRK2 in tomato stem inhibits growth and causes wilting of young leaves. Plant J 34 837 846
28. DaiN
Kandel-KfirM
PetreikovM
HanaelR
LevinI
2002 The tomato hexokinase LeHXK1 cloning, mapping, expression pattern and phylogenetic relationships. Plant Sci 163 581 590
29. GonzaliS
AlpiA
BlandoF
De BellisL
2002 Arabidopsis thaliana (HXK1 and HXK2) and yeast (HXK2) hexokinases overexpressed in transgenic lines are characterized by different catalytic properties. Plant Sci 163 943 954
30. GranotD
2007 Role of tomato hexose kinases. Functional Plant Biol 34 564 570
31. LeonP
SheenJ
2003 Sugar and hormone connections. Trends in Plant Sci 8 110 116
32. ZhouL
JangJC
JonesT
SheenJ
1998 Glucose and ethylene signal transduction cross-talk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci USA 95 10294 10299
33. ChengWH
EndoA
ZhouL
PenneyJ
ChenH
2002 A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14 2723 2743
34. LinPC
HwangSG
EndoA
OkamotoM
KoshibaT
2007 Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol 143 745 758
35. Arenas-HuerteroF
Arroyo-BecerraA
ZhouL
SheenJ
LeonP
2000 Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes and Dev 14 2085 2096
36. ArroyoA
BossiF
FinkelsteinRR
LeonP
2003 Three genes that affect sugar sensing abscisic acid insensitive 4, abscisic acid insensitive 5, and constitutive triple response 1 are differentially regulated by glucose in Arabidopsis. Plant Physiol 133 231 242
37. HuijserC
KortsteeA
PegoJ
WeisbeekP
WismanE
2000 The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: Involvement of abscisic acid in sugar responses. Plant J 23 577 585
38. LabyRJ
KincaidMS
KimD
GibsonSI
2000 The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23 587 596
39. GibsonSI
LabyRJ
KimD
2001 The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1. Biochem Biophys Res Commun 280 196 203
40. RookF
CorkeF
CardR
MunzG
SmithC
2001 Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J 26 421 433
41. ChaudhuriB
HörmannF
LalondeS
BradySM
OrlandoDA
2008 Protonophore- and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. Plant J 56 948 962
42. LalondeS
EhrhardtDW
FrommerWB
2005 Shining light on signaling and metabolic networks by genetically encoded biosensors. Curr Opin Plant Biol 8 574 581
43. YooSD
ChoYH
SheenJ
2007 Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nature Protocols 2 1565 1572
44. FinkelsteinRR
WangML
LynchTJ
RaoS
GoodmanHM
1998 The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10 1043 1054
45. WeeksCM
RoszakAW
ErmanM
KaiserR
JornvallH
1999 Structure of rabbit liver fructose1,6-bisphosphatase at 2.3A resolution. Acta Cryst D55 93 102
46. SolanoR
StepanovaA
ChaoQ
EckerJR
1998 Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12 3703 3714
47. StrandA
ZrennerR
TrevanionS
StittM
GustafssonP
2000 Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytoplasmic fructose-1-6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 23 759 770
48. SahrawyM
AvilaC
ChuecaA
CánovasFM
López-GorgéJ
2004 Increased sucrose level and altered nitrogen metabolism in Arabidopsis thaliana transgenic plants expressing antisense chloroplastic fructose-1,6-bisphosphatase. J Exp Bot 55 2495 2503
49. LeeSK
JeonJS
BörnkeF
VollL
ChoJI
2008 Loss of cytosolic fructose-1,6-bisphosphatase limits photosynthetic sucrose synthesis and causes severe growth retardations in rice (Oryza sativa). Plant Cell Environ 31 1851 1863
50. HäuslerRE
SchliebenNH
SchulzB
FlüggeUI
1998 Compensation of decreased triose phosphate/phosphate translocator activity by accelerated starch turnover and glucose transport in transgenic tobacco. Planta 204 366 376
51. LundmarkM
CavacoAM
TrevanionS
HurryV
2006 Carbon partitioning and export in transgenic Arabidopsis thaliana with altered capacity for sucrose synthesis grown at low temperature: a role for metabolite transporters. Plant Cell Environ 29 1703 1714
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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