ABA signaling is necessary but not sufficient for RD29B transcriptional memory during successive dehydration stresses in Arabidopsis thaliana

Plant Journal

Volumn 79, Issue 1, 2014, Pages 150-161

  Virlouvet, Laetitia ^a   Ding, Yong ^b,c   Fujii, Hiroaki ^d   Avramova, Zoya ^b   Fromm, Michael ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

ABRE; abscisic acid; Arabidopsis thaliana; dehydration stress; RD29B; SnRK2; transcriptional memory

Indexed keywords

ENZYMES; GENES; PROTEINS; TRANSCRIPTION;

ABRE; ABSCISIC ACID; ARABIDOPSIS THALIANA; RD29B; SNRK2;

DEHYDRATION;

ARABIDOPSIS THALIANA;

ABSCISIC ACID; ARABIDOPSIS PROTEIN; COLD SHOCK PROTEIN; PHYTOHORMONE; RD29B PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CYTOLOGY; DEHYDRATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PROMOTER REGION; REPORTER GENE; SEEDLING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; COLD SHOCK PROTEINS AND PEPTIDES; DEHYDRATION; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; MOLECULAR SEQUENCE DATA; MUTATION; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; SEEDLING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84903301309     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12548     Document Type: Article

References (49)

1. Ali, M., Sugimoto, K., Ramadan, A., and, Arimura, G., (2013) Memory of plant communications for priming anti-herbivore responses. Sci. Rep. 3, 1872.
2. Baldwin, I.T., and, Schmelz, E., (1996) Immunological "memory" in the induced accumulation of nicotine in wild tobacco. Ecology, 77, 236-246.
3. Bent, A., (2006) Arabidopsis thaliana floral dip transformation method. Methods Mol. Biol. 343, 87-103.
4. Bruce, T.J., Matthes, M.C., Napier, J.A., and, Pickett, J.A., (2007) Stressful "memories" of plants: evidence for possible mechanisms. Plant Sci. 173, 603-608.
5. Chae, M.J., Lee, J.S., Nam, M.H., Cho, K., Hong, J.Y., Yi, S.A., Suh, S.C., and, Yoon, I.S., (2007) A rice dehydration-inducible SNF1-related protein kinase 2 phosphorylates an abscisic acid responsive element-binding factor and associates with ABA signaling. Plant Mol. Biol. 63, 151-169.
6. Ciolkowski, I., Wanke, D., Birkenbihl, R.P., and, Somssich, I.E., (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol. Biol. 68, 81-92.
7. Conrath, U., (2011) Molecular aspects of defence priming. Trends Plant Sci. 16, 524-531.
8. Conrath, U., Beckers, G.J., Flors, V., et al,. (2006) Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062-1071.
9. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and, Abrams, S.R., (2010) Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.
10. Ding, Y., Avramova, Z., and, Fromm, M., (2011) Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes. Plant Cell, 23, 350-363.
11. Ding, Y., Fromm, M., and, Avramova, Z., (2012) Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat. Commun. 3, 740.
12. Fujii, H., and, Zhu, J.K., (2009b) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl Acad. Sci. USA, 106, 8380-8385.
13. Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.Y., Cutler, S.R., Sheen, J., Rodriguez, P.L., and, Zhu, J.K., (2009a) In vitro reconstitution of an abscisic acid signalling pathway. Nature, 462, 660-664.
14. Fujii, H., Verslues, P.E., and, Zhu, J.K., (2011) Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc. Natl Acad. Sci. USA, 108, 1717-1722.
15. Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M.M., Seki, M., Hiratsu, K., Ohme-Takagi, M., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell, 17, 3470-3488.
16. Fujita, Y., Nakashima, K., Yoshida, T., et al,. (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50, 2123-2132.
17. Fujita, Y., Fujita, M., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant. Res. 124, 509-525.
18. Fujita, Y., Yoshida, T., and, Yamaguchi-Shinozaki, K., (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol. Plant. 147, 15-27.
19. Goh, C.H., Nam, H.G., and, Park, Y.S., (2003) Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. Plant J. 36, 240-255.
20. Guan, Q., Haroon, S., Bravo, D.G., Will, J.L., and, Gasch, A.P., (2012) Cellular memory of acquired stress resistance in Saccharomyces cerevisiae. Genetics, 192, 495-505.
21. Hirayama, T., and, Shinozaki, K., (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci. 12, 343-351.
22. Jaskiewicz, M., Conrath, U., and, Peterhansel, C., (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12, 50-55.
23. Kang, J.Y., Choi, H.I., Im, M.Y., and, Kim, S.Y., (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell, 14, 343-357.
24. Kim, S., Kang, J.Y., Cho, D.I., Park, J.H., and, Kim, S.Y., (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J. 40, 75-87.
25. Kim, J.M., To, T.K., Ishida, J., Matsui, A., Kimura, H., and, Seki, M., (2012) Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol. 53, 847-856.
26. Klingler, J.P., Batelli, G., and, Zhu, J.K., (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. J. Exp. Bot. 61, 3199-3210.
27. Kulik, A., Wawer, I., Krzywinska, E., Bucholc, M., and, Dobrowolska, G., (2011) SnRK2 protein kinases-key regulators of plant response to abiotic stresses. OMICS, 15, 859-872.
28. Kundu, S., and, Peterson, C.L., (2010) Dominant role for signal transduction in the transcriptional memory of yeast GAL genes. Mol. Cell. Biol. 30, 2330-2340.
29. Laine, J.P., Singh, B.N., Krishnamurthy, S., and, Hampsey, M., (2009) A physiological role for gene loops in yeast. Genes Dev. 23, 2604-2609.
30. Light, W.H., Brickner, D.G., Brand, V.R., and, Brickner, J.H., (2010) Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and IN01 transcriptional memory. Mol. Cell, 40, 112-125.
31. Light, W.H., Freaney, J., Sood, V., Thompson, A., D'Urso, A., Horvath, C.M., and, Brickner, J.H., (2013) A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol. 11, e1001524.
32. Livak, K.J., and, Schmittgen, T.D., (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402-408.
33. Nakashima, K., and, Yamaguchi-Shinozaki, K., (2013) ABA signaling in stress-response and seed development. Plant Cell Rep. 32, 959-970.
34. Nakashima, K., Fujita, Y., Katsura, K., Maruyama, K., Narusaka, Y., Seki, M., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2006) Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol. Biol. 60, 51-68.
35. Nambara, E., Kawaide, H., Kamiya, Y., and, Naito, S., (1998) Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. Plant Cell Physiol. 39, 853-858.
36. Narusaka, Y., Nakashima, K., Shinwari, Z.K., Sakuma, Y., Furihata, T., Abe, H., Narusaka, M., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 34, 137-148.
37. Stuitje, A.R., Verbree, E.C., van der Linden, K.H., Mietkiewska, E.M., Nap, J.P., and, Kneppers, T.J., (2003) Seed-expressed fluorescent proteins as versatile tools for easy (co)transformation and high-throughput functional genomics in Arabidopsis. Plant Biotechnol. J. 1, 301-309.
38. Sun, X.-L., Li, Y., Bai, X., Ji, W., Jii, Z.-J., and, Zhu, Y.-M., (2011) Arabidopsis bZIP1 transcription factor binding to ABRE cis-element regulates abscisic acid signal transduction. Acta Agron. Sin. 37, 612-619.
39. Tan-Wong, S.M., Wijayatilake, H.D., and, Proudfoot, N.J., (2009) Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev. 23, 2610-2624.
40. Ton, J., Jakab, G., Toquin, V., Flors, V., Iavicoli, A., Maeder, M.N., Metraux, J.P., and, Mauch-Mani, B., (2005) Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell, 17, 987-999.
41. Ton, J., D'Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., Mauch-Mani, B., and, Turlings, T.C., (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49, 16-26.
42. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl Acad. Sci. USA, 97, 11632-11637.
43. Virlouvet, L., Jacquemot, M.P., Gerentes, D., et al,. (2011) The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiol. 157, 917-936.
44. Xie, T., Ren, R., Zhang, Y.Y., et al,. (2012) Molecular mechanism for inhibition of a critical component in the Arabidopsis thaliana abscisic acid signal transduction pathways, SnRK2.6, by protein phosphatase ABI1. J. Biol. Chem. 287, 794-802.
45. Yamaguchi-Shinozaki, K., and, Shinozaki, K., (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol. Gen. Genet. 236, 331-340.
46. Yamaguchi-Shinozaki, K., and, Shinozaki, K., (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell, 6, 251-264.
47. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61, 672-685.
48. Yunta, C., Martinez-Ripoll, M., Zhu, J.K., and, Albert, A., (2011) The structure of Arabidopsis thaliana OST1 provides insights into the kinase regulation mechanism in response to osmotic stress. J. Mol. Biol. 414, 135-144.
49. Zacharioudakis, I., Gligoris, T., and, Tzamarias, D., (2007) A yeast catabolic enzyme controls transcriptional memory. Curr. Biol. 17, 2041-2046.