The -Induced Arabidopsis Transcription Factor Attenuates ABA Signaling and Renders Seedlings Sugar Insensitive when Present in the Nucleus

English version České info

In plants, sugars function as signaling molecules that control important processes such as photosynthesis, growth, carbon distribution over different organs and the production of storage compounds. Sugar signaling requires the phytohormone abscisic acid (ABA) and the ABA-induced regulatory transcription factor ABI4. In this study, a genetic analysis identified the transcription factor ANAC060 as an important component in establishing sugar sensitivity. It was found that, in natural Arabidopsis thaliana populations, the ANAC060 protein may occur as a long or a short version due to differential ANAC060 mRNA splicing caused by a single-nucleotide polymorphism (SNP). The long ANAC060 protein with an intact transmembrane domain (TMD) is excluded from the nucleus, whereas the short version lacking the TMD is always present in the nucleus, where it regulates gene expression. Functional analyses indicated that Col ANAC060 is involved in a novel negative feedback loop in the sugar-ABA signaling pathway. In this feedback loop model, ABI4 activates ANAC060 expression, but the nuclear presence of Col ANAC060 suppresses Glc-induced ABA accumulation and ABI4 expression, thereby reducing responsiveness to sugar signals.

Vyšlo v časopise: The -Induced Arabidopsis Transcription Factor Attenuates ABA Signaling and Renders Seedlings Sugar Insensitive when Present in the Nucleus. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004213
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004213

Souhrn

Zdroje

1. GibsonS (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8: 93–102.

2. RollandF, Baena-GonzalezE, SheenJ (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675–709.

3. SmeekensS (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51: 49–81.

4. EvelandAL, JacksonDP (2012) Sugars, signalling, and plant development. J Exp Bot 63: 3367–3377.

5. PriceJ, LaxmiA, St MartinSK, JangJC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16: 2128–2150.

6. DijkwelPP, HuijserC, WeisbeekPJ, ChuaNH, SmeekensSC (1997) Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell 9: 583–595.

7. MooreB, ZhouL, RollandF, HallQ, ChengWH, et al. (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300: 332–336.

8. Baena-GonzalezE, RollandF, TheveleinJM, SheenJ (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938–942.

9. Bolouri MoghaddamMR, den EndeWV (2013) Sugars, the clock and transition to flowering. Front Plant Sci 4: 22.

10. LeiM, LiuD (2011) Sucrose regulates plant responses to deficiencies in multiple nutrients. Plant Signal Behav 6: 1247–1249.

11. LabyR, KincaidM, KimD, GibsonS (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23: 587–596.

12. ZhouL, JangJ, JonesT, SheenJ (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci USA 95: 10294–10299.

13. Arenas-HuerteroF, ArroyoA, 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 Dev 14: 2085–2096.

14. CarvalhoRF, CarvalhoSD, DuqueP (2010) The plant-specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis. Plant Physiol 154: 772–783.

15. ChenJG, JonesAM (2004) AtRGS1 function in Arabidopsis thaliana. Methods Enzymol 389: 338–350.

16. CuiH, HaoY, KongD (2012) SCARECROW has a SHORT-ROOT-independent role in modulating the sugar response. Plant Physiol 158: 1769–1778.

17. GibsonSI, LabyRJ, KimD (2001) The sugar-insensitive1 (sis1) Mutant of Arabidopsis Is Allelic to ctr1. Biochemical and Biophysical Research Communications 280: 196–203.

18. HuangY, LiCY, PattisonDL, GrayWM, ParkS, et al. (2010) SUGAR-INSENSITIVE3, a RING E3 ligase, is a new player in plant sugar response. Plant Physiol 152: 1889–1900.

19. HuangY, LiCY, BiddleK, GibsonS (2008) Identification, cloning and characterization of sis7 and sis10 sugar-insensitive mutants of Arabidopsis. BMC Plant Biology 8: 104.

20. DekkersB, SchuurmansJ, SmeekensS (2008) Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis. Plant Molecular Biology 67: 151–167.

21. YanagisawaS, YooSD, SheenJ (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425: 521–525.

22. FinkelsteinR, WangM, LynchT, RaoS, GoodmanH (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an Apetala2 domain protein. Plant Cell 10: 1043–1054.

23. HuijserC, KortsteeA, PegoJ, WeisbeekP, WismanE, et al. (2000) The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in sugar responses. Plant J 23: 577–586.

24. RookF, CorkeF, CardR, MunzG, SmithC, et al. (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J 26: 421–433.

25. LeonP, GregorioJ, CordobaE (2012) ABI4 and its role in chloroplast retrograde communication. Front Plant Sci 3: 304.

26. WindJJ, PevianiA, SnelB, HansonJ, SmeekensSC (2013) ABI4: versatile activator and repressor. Trends Plant Sci 18: 125–132.

27. Acevedo-HernándezGJ, LeónP, Herrera-EstrellaLR (2005) Sugar and ABA responsiveness of a minimal RBCS light-responsive unit is mediated by direct binding of ABI4. The Plant Journal 43: 506–519.

28. BossiF, CordobaE, DupreP, MendozaMS, RomanCS, et al. (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. Plant J 59: 359–374.

29. ReevesWM, LynchTJ, MobinR, FinkelsteinRR (2011) Direct targets of the transcription factors ABA-Insensitive(ABI)4 and ABI5 reveal synergistic action by ABI4 and several bZIP ABA response factors. Plant Mol Biol 75: 347–363.

30. Alonso-BlancoC, AartsMG, BentsinkL, KeurentjesJJ, ReymondM, et al. (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21: 1877–1896.

31. TengS, RognoniS, BentsinkL, SmeekensS (2008) The Arabidopsis GSQ5/DOG1 Cvi allele is induced by the ABA-mediated sugar signalling pathway, and enhances sugar sensitivity by stimulating ABI4 expression. Plant J 55: 372–381.

32. LiP, WindJJ, ShiX, ZhangH, HansonJ, et al. (2011) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci U S A 108: 3436–3441.

33. DarvasiA, SollerM (1992) Selective genotyping for determination of linkage between a marker locus and a quantitative trait locus. Theoretical and Applied Genetics 85: 353–359.

34. TorjekO, MeyerRC, ZehnsdorfM, TeltowM, StrompenG, et al. (2008) Construction and analysis of 2 reciprocal Arabidopsis introgression line populations. J Hered 99: 396–406.

35. OokaH, SatohK, DoiK, NagataT, OtomoY, et al. (2003) Comprehensive Analysis of NAC Family Genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10: 239–247.

36. KimS-Y, KimS-G, KimY-S, SeoPJ, BaeM, et al. (2007) Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucl Acids Res 35: 203–213.

37. KleinP, SeidelT, StockerB, DietzKJ (2012) The membrane-tethered transcription factor ANAC089 serves as redox-dependent suppressor of stromal ascorbate peroxidase gene expression. Front Plant Sci 3: 247.

38. ShuK, ZhangH, WangS, ChenM, WuY, et al. (2013) ABI4 Regulates Primary Seed Dormancy by Regulating the Biogenesis of Abscisic Acid and Gibberellins in Arabidopsis. PLoS Genet 9: e1003577.

39. SunY, WangJ, CrouchJ, XuY (2010) Efficiency of selective genotyping for genetic analysis of complex traits and potential applications in crop improvement. Molecular Breeding 26: 493–511.

40. FarkhariM, KrivanekA, XuY, RongT, NaghaviMR, et al. (2013) Root-lodging resistance in maize as an example for high-throughput genetic mapping via single nucleotide polymorphism-based selective genotyping. Plant Breeding 132: 90–98.

41. PrasadM, VarshneyRK, KumarA, BalyanHS, SharmaPC, et al. (1999) A microsatellite marker associated with a QTL for grain protein content on chromosome arm 2DL of bread wheat. Theoretical and Applied Genetics 99: 341–345.

42. AyoubM, MatherDE (2002) Effectiveness of selective genotyping for detection of quantitative trait loci: an analysis of grain and malt quality traits in three barley populations. Genome 45: 1116–1124.

43. FooladMR, StoltzT, DervinisC, RodriguezRL, JonesRA (1997) Mapping QTLs conferring salt tolerance during germination in tomato by selective genotyping. Molecular Breeding 3: 269–277.

44. FooladMR, ZhangLP, LinGY (2001) Identification and validation of QTLs for salt tolerance during vegetative growth in tomato by selective genotyping. Genome 44: 444–454.

45. ZhangLP, LinGY, Niño-LiuD, FooladMR (2003) Mapping QTLs conferring early blight (Alternaria solani) resistance in a Lycopersicon esculentum×L. hirsutum cross by selective genotyping. Molecular Breeding 12: 3–19.

46. CarrLG, ForoudT, BiceP, GobbettT, IvashinaJ, et al. (1998) A Quantitative Trait Locus for Alcohol Consumption in Selectively Bred Rat Lines. Alcoholism: Clinical and Experimental Research 22: 884–887.

47. KimS-G, LeeS, SeoPJ, KimS-K, KimJ-K, et al. (2010) Genome-scale screening and molecular characterization of membrane-bound transcription factors in Arabidopsis and rice. Genomics 95: 56–65.

48. ChenYN, SlabaughE, BrandizziF (2008) Membrane-tethered transcription factors in Arabidopsis thaliana: novel regulators in stress response and development. Curr Opin Plant Biol 11: 695–701.

49. HuangX-Y, ChaoD-Y, GaoJ-P, ZhuM-Z, ShiM, et al. (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes & Development 23: 1805–1817.

50. ZhouCM, ZhangTQ, WangX, YuS, LianH, et al. (2013) Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340: 1097–1100.

51. YooSD, ChoYH, SheenJ (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565–1572.

52. HellensRP, AllanAC, FrielEN, BolithoK, GraftonK, et al. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 13.

53. CzechowskiT, StittM, AltmannT, UdvardiMK, ScheibleW-R (2005) Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis. Plant Physiol 139: 5–17.

54. MullerPY, JanovjakH, MiserezAR, DobbieZ (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32: 1372–1374, 1376, 1378–1379.

55. SimonP (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19: 1439–1440.