AtRH57, a DEAD-box RNA helicase, is involved in feedback inhibition of glucose-mediated abscisic acid accumulation during seedling development and additively affects pre-ribosomal RNA processing with high glucose

Plant Journal

Volumn 77, Issue 1, 2014, Pages 119-135

  Hsu, Yi Feng ^a   Chen, Yun Chu ^a   Hsiao, Yu Chun ^a   Wang, Bing Jyun ^a   Lin, Shih Yun ^b   Cheng, Wan Hsing ^b   Jauh, Guang Yuh ^b   Harada, John J ^c   Wang, Co Shine ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

abscisic acid; Arabidopsis thaliana seeds; glucose hypersensitive; RNA helicase; rRNA biogenesis; seedling growth

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS THALIANA; GLUCOSE-HYPERSENSITIVE; RNA HELICASES; RRNA BIOGENESIS; SEEDLING GROWTH;

BIOCHEMISTRY; BIOSYNTHESIS; FORESTRY; GENES; GLUCOSE; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; PROTEINS; SIGNALING;

RNA;

ALLIUM CEPA; ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID; ARABIDOPSIS PROTEIN; DEAD BOX PROTEIN; GLUCOSE; PHYTOHORMONE; RH57 PROTEIN, ARABIDOPSIS; RIBOSOME RNA; RNA PRECURSOR;

ARABIDOPSIS; BIOLOGICAL MODEL; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHENOTYPE; PHYSIOLOGY; PLANT SEED; PROTEIN MOTIF; RIBOSOME; SEEDLING; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ABSCISIC ACID; AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DEAD-BOX RNA HELICASES; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GERMINATION; GLUCOSE; MODELS, BIOLOGICAL; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PLANT GROWTH REGULATORS; PLANTS, GENETICALLY MODIFIED; RIBOSOMES; RNA PRECURSORS; RNA, RIBOSOMAL; SEEDLING; SEEDS; SIGNAL TRANSDUCTION;

EID: 84891003347     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12371     Document Type: Article

References (67)

1. Abbasi, N., Kim, H.B., Park, N.I., Kim, H.S., Kim, Y.K., Park, Y.I., and, Choi, S.B., (2010) APUM23, a nucleolar Puf domain protein, is involved in pre-ribosomal RNA processing and normal growth patterning in Arabidopsis. Plant J. 64, 960-976.
2. Arenas-Huertero, F., Arroyo, A., Zhou, L., Sheen, J., and, Leõn, P., (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.
3. Arroyo, A., Bossi, F., Finkelstein, R.R., and, Leõn, P., (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.
4. Asakura, Y., Galarneau, E., Watkins, K.P., Barkan, A., and, van Wijk, K.J., (2012) Chloroplast RH3 DEAD-box RNA helicases in maize and Arabidopsis function in splicing of specific group II introns and affect chloroplast ribosome biogenesis. Plant Physiol. 159, 961-974.
5. Bossi, F., Cordoba, E., Dupré, P., Mendoza, M.S., Román, C.S., and, Leõn, P., (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.
6. Boudet, N., Aubourg, S., Toffano-Nioche, C., Kreis, M., and, Lecharny, A., (2001) Evolution of intron/exon structure of DEAD helicase family genes in Arabidopsis, Caenorhabditis, and Drosophila. Genome Res. 11, 2101-2114.
7. Bu, Q., Li, H., Zhao, Q., et al. (2009) The Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiol. 150, 463-481.
8. Carvalho, R.F., Carvalho, S.D., and, Duque, P., (2010) The plant-specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis. Plant Physiol. 154, 772-783.
9. Cheng, W.H., Endo, A., Zhou, L., et al. (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell, 14, 2723-2743.
10. Chernoff, Y.O., Vincent, A., and, Liebman, S.W., (1994) Mutations in eukaryotic 18S ribosomal RNA affect translational fidelity and resistance to aminoglycoside antibiotics. EMBO J. 13, 906-913.
11. Chi, W., He, B., Mao, J., Li, Q., Ma, J., Ji, D., Zou, M., and, Zhang, L., (2012) The function of RH22, a DEAD RNA helicase, in the biogenesis of the 50S ribosomal subunits of Arabidopsis chloroplasts. Plant Physiol. 158, 693-707.
12. Chung, E., Cho, C.W., Yun, B.H., Choi, H.K., So, H.A., Lee, S.W., and, Lee, J.H., (2009) Molecular cloning and characterization of the soybean DEAD-box RNA helicase gene induced by low temperature and high salinity stress. Gene, 443, 91-99.
13. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
14. Cordin, O., Banroques, J., Tanner, N.K., and, Linder, P., (2006) The DEAD-box protein family of RNA helicases. Gene, 367, 17-37.
15. Dekkers, B.J., Schuurmans, J.A., and, Smeekens, S.C., (2008) Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis. Plant Mol. Biol. 67, 151-167.
16. Dong, H., Zhen, Z., Peng, J., Chang, L., Gong, Q., and, Wang, N.N., (2011) Loss of ACS7 confers abiotic stress tolerance by modulating ABA sensitivity and accumulation in Arabidopsis. J. Exp. Bot. 62, 4875-4887.
17. Finkelstein, R.R., Wang, M.L., Lynch, T.J., Rao, S., and, Goodman, H.M., (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell, 10, 1043-1054.
18. Gabashvili, I.S., Gregory, S.T., Valle, M., Grassucci, R., Worbs, M., Wahl, M.C., Dahlberg, A.E., and, Frank, J., (2001) The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol. Cell, 8, 181-188.
19. Galimand, M., Gerbaud, G., and, Courvalin, P., (2000) Spectinomycin resistance in Neisseria spp. due to mutations in 16S rRNA. Antimicrob. Agents Chemother. 44, 1365-1366.
20. Gibson, S.I., (2005) Control of plant development and gene expression by sugar signaling. Curr. Opin. Plant Biol. 8, 93-102.
21. Gong, Z., Lee, H., Xiong, L., Jagendorf, A., Stevenson, B., and, Zhu, J.K., (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc. Natl Acad. Sci. USA, 99, 11507-11512.
22. Gong, Z., Dong, C.H., Lee, H., Zhu, J., Xiong, L., Gong, D., Stevenson, B., and, Zhu, J.K., (2005) A DEAD-box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell, 17, 256-267.
23. Guo, J., Wang, S., Valerius, O., Hall, H., Zeng, Q., Li, J.F., Weston, D.J., Ellis, B.E., and, Chen, J.G., (2011) Involvement of Arabidopsis RACK1 in protein translation and its regulation by abscisic acid. Plant Physiol. 155, 370-383.
24. Honoré, N., and, Cole, S.T., (1994) Streptomycin resistance in mycobacteria. Antimicrob. Agents Chemother. 38, 238-242.
25. Hsu, Y.F., Yu, S.C., Yang, C.Y., and, Wang, C.S., (2011) Lily ASR protein-conferred cold and freezing resistance in Arabidopsis. Plant Physiol. Biochem. 49, 937-945.
26. Huang, C.K., Huang, L.F., Huang, J.J., Wu, S.J., Yeh, C.H., and, Lu, C.A., (2010a) A DEAD-box protein, AtRH36, is essential for female gametophyte development and is involved in rRNA biogenesis in Arabidopsis. Plant Cell Physiol. 51, 694-706.
27. Huang, Y., Li, C.Y., Pattison, D.L., Gray, W.M., Park, S., and, Gibson, S.I., (2010b) SUGAR-INSENSITIVE3, a RING E3 ligase, is a new player in plant sugar response. Plant Physiol. 152, 1889-1900.
28. Kant, P., Kant, S., Gordon, M., Shaked, R., and, Barak, S., (2007) STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol. 145, 814-830.
29. Kemp, C., and, ImLer, J.L., (2009) Antiviral immunity in drosophila. Curr. Opin. Immunol. 21, 3-9.
30. Kim, J.S., Kim, K.A., Oh, T.R., Park, C.M., and, Kang, H., (2008) Functional characterization of DEAD-box RNA helicases in Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol. 49, 1563-1571.
31. Kojima, H., Suzuki, T., Kato, T., et al. (2007) Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development. Plant J. 49, 1053-1063.
32. Koussevitzky, S., Nott, A., Mockler, T.C., Hong, F., Sachetto-Martins, G., Surpin, M., Lim, J., Mittler, R., and, Chory, J., (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science, 316, 715-719.
33. Laby, R.J., Kincaid, M.S., Kim, D., and, Gibson, S.I., (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J. 23, 587-596.
34. Le, B.H., Cheng, C., Bui, A.Q., et al. (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl Acad. Sci. USA, 107, 8063-8070.
35. Lee, S.A., Yoon, E.K., Heo, J.O., Lee, M.H., Hwang, I., Cheong, H., Lee, W.S., Hwang, Y.S., and, Lim, J., (2012) Analysis of Arabidopsis glucose-insensitive growth mutants reveals the involvement of the plastidial copper transporter PAA1 in glucose-induced intracellular signaling. Plant Physiol. 159, 1001-1012.
36. Leon, P., and, Sheen, J., (2003) Sugar and hormone connections. Trends Plant Sci. 8, 110-116.
37. Linder, P., (2006) Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res. 34, 4168-4180.
38. Linder, P., and, Jankowsky, E., (2011) From unwinding to clamping-the DEAD-box RNA helicase family. Nat. Rev. Mol. Cell Biol. 12, 505-516.
39. Liu, H.H., Liu, J., Fan, S.L., Song, M.Z., Han, X.L., Liu, F., and, Shen, F.F., (2008) Molecular cloning and characterization of a salinity stress-induced gene encoding DEAD-box helicase from the halophyte Apocynum venetum. J. Exp. Bot. 59, 633-644.
40. Liu, M., Shi, D.Q., Yuan, L., Liu, J., and, Yang, W.C., (2010) SLOW WALKER3, encoding a putative DEAD-box RNA helicase, is essential for female gametogenesis in Arabidopsis. J. Integr. Plant Biol. 52, 817-828.
41. Lopez-Molina, L., Mongrand, S., and, Chua, N.H., (2001) A post-germination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl Acad. Sci. USA, 98, 4782-4787.
42. Lopez-Molina, L., Mongrand, S., McLachlin, D.T., Chait, B.T., and, Chua, N.H., (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J. 32, 317-328.
43. Maliga, P., Klessig, D.F., Cashmore, A.R., Gruissem, W., and, Varner, J.E., (1995) Methods in Plant Molecular Biology: A Laboratory Course Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
44. Murashige, T., and, Skoog, F., (1962) A revised medium for rapid growth and bioassays with tobacco. Physiol. Plant. 15, 473-497.
45. Oleinick, N.L., (1977) Initiation and elongation of protein synthesis in growing cells: differential inhibition by cycloheximide and emetine. Arch. Biochem. Biophys. 182, 171-180.
46. Owttrim, G.W., (2006) RNA helicases and abiotic stress. Nucleic Acids Res. 34, 3220-3230.
47. Penfield, S., Li, Y., Gilday, A.D., Graham, S., and, Graham, I.A., (2006) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell, 18, 1887-1899.
48. Qiu, Y., and, Yu, D., (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ. Exp. Bot. 65, 35-47.
49. Rajjou, L., Gallardo, K., Debeaujon, I., Vandekerckhove, J., Job, C., and, Job, D., (2004) The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol. 134, 1598-1613.
50. Rolland, F., Moore, B., and, Sheen, J., (2002) Sugar sensing and signaling in plants. Plant Cell, 14 (Suppl), S185-S205.
51. Rosado, A., Sohn, E.J., Drakakaki, G., Pan, S., Swidergal, A., Xiong, Y., Kang, B.H., Bressan, R.A., and, Raikhel, N.V., (2010) Auxin-mediated ribosomal biogenesis regulates vacuolar trafficking in Arabidopsis. Plant Cell, 22, 143-158.
52. Sahni, A., Wang, N., and, Alexis, J.D., (2010) UAP56 is an important regulator of protein synthesis and growth in cardiomyocytes. Biochem. Biophys. Res. Commun. 393, 106-110.
53. Sanan-Mishra, N., Pham, X.H., Sopory, S.K., and, Tuteja, N., (2005) Pea DNA helicase 45 over-expression in tobacco confers high salinity tolerance without affecting yield. Proc. Natl Acad. Sci. USA, 102, 509-514.
54. Sanford, J.C., Smith, F.D., and, Russell, J.A., (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol. 217, 483-509.
55. Stone, S.L., Williams, L.A., Farmer, L.M., Vierstra, R.D., and, Callis, J., (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell, 18, 3415-3428.
56. Stonebloom, S., Burch-Smith, T., Kim, I., Meinke, D., Mindrinos, M., and, Zambryski, P., (2009) Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proc. Natl Acad. Sci. USA, 106, 17229-17234.
57. Tai, C.L., Chi, W.K., Chen, D.S., and, Hwang, L.H., (1996) The helicase activity associated with hepatitis C virus nonstructural protein 3 (NS3). J. Virol. 70, 8477-8484.
58. Ullah, H., Chen, J.G., Wang, S., and, Jones, A.M., (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol. 129, 897-907.
59. Vashisht, A.A., and, Tuteja, N., (2006) Stress-responsive DEAD-box helicases, a new pathway to engineer plant stress tolerance. J. Photochem. Photobiol. B, 84, 150-160.
60. Vashisht, A.A., Pradhan, A., Tuteja, R., and, Tuteja, N., (2005) Cold- and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J. 44, 76-87.
61. Verslues, P.E., and, Bray, E.A., (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J. Exp. Bot. 57, 201-212.
62. Xiong, L., Ishitani, M., Lee, H., and, Zhu, J.K., (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell, 13, 2063-2083.
63. Yang, C.Y., Chen, Y.C., Jauh, G.Y., and, Wang, C.S., (2005) A lily ASR protein involves abscisic acid signaling and confers drought and salt resistance in Arabidopsis. Plant Physiol. 139, 836-846.
64. Yoine, M., Ohto, M.A., Onai, K., Mita, S., and, Nakamura, K., (2006) The lba1 mutation of UPF1 RNA helicase involved in nonsense-mediated mRNA decay causes pleiotropic phenotypic changes and altered sugar signalling in Arabidopsis. Plant J. 47, 49-62.
65. Yu, E., and, Owttrim, G.W., (2000) Characterization of the cold stress-induced cyanobacterial DEAD-box protein CrhC as an RNA helicase. Nucleic Acids Res. 28, 3926-3934.
66. Zanetti, M.E., Chang, I.-F., Gong, F., Galbraith, D.W., and, Bailey-Serres, J., (2005) Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression. Plant Physiol. 138, 624-635.
67. Zhou, L., Jang, J.C., Jones, T.L., and, Sheen, J., (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc. Natl Acad. Sci. USA, 95, 10294-10299.