NAC transcription factor ORE1 and Senescence-Induced BIFUNCTIONAL NUCLEASE1 (BFN1) constitute a regulatory cascade in arabidopsis

Molecular Plant

Volumn 6, Issue 5, 2013, Pages 1438-1452

  Matallana Ramirez, Lilian P ^a   Rauf, Mamoona ^a   Farage Barhom, Sarit ^b   Dortay, Hakan ^a   Xue, Gang Ping ^c   Dröge Laser, Wolfgang ^d   Lers, Amnon ^b   Balazadeh, Salma ^a,e   Mueller Roeber, Bernd ^a,e  

^a UNIVERSITY OF POTSDAM   (Germany)

^b VOLCANI CENTER   (Israel)

^c CSIRO   (Australia)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Arabidopsis thaliana; BFN1; ORE1; promoter; senescence; transcription factor

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; BFN1 PROTEIN, ARABIDOPSIS; DEOXYRIBONUCLEASE; ORE1 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; PROTEIN BINDING;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BFN1; BINDING SITE; BIOLOGICAL MODEL; CYTOLOGY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MESOPHYLL CELL; METABOLISM; MUTATION; ORE1; PROMOTER REGION; PROTEIN BINDING; PROTOPLAST; SENESCENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSGENIC PLANT;

ARABIDOPSIS THALIANA; BFN1; ORE1; PROMOTER; SENESCENCE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; DEOXYRIBONUCLEASES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, PLANT; MESOPHYLL CELLS; MODELS, BIOLOGICAL; MUTATION; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTOPLASTS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84885033397     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst012     Document Type: Article

References (46)

1. Alonso, J.M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J.R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science. 284, 2148-2152.
2. Arvidsson, S., Kwasniewski, M., Riaño-Pachón, D.M., and Mueller- Roeber, B. (2008). QuantPrime: a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics. 9, 465.
3. Balazadeh, S., Kwasniewski, M., Caldana, C., Mehrnia, M., Zanor, M.I., Xue, G.P., and Mueller-Roeber, B. (2011). ORS1, an H2O2- responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol. Plant. 4, 346.
4. Balazadeh, S., Riaño-Pachón, D.M., and Mueller-Roeber, B. (2008). Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol. 10, 63-75.
5. Balazadeh, S., Siddiqui, H., Allu, A.D., Matallana-Ramirez, L.P., Caldana, C., Mehrnia, M., Zanor, M.I., Köhler, B., and Mueller- Roeber, B. (2010). A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during saltpromoted senescence. Plant J. 62, 250-264.
6. Bisson, M.M., Bleckmann, A., Allekotte, S., and Groth, G. (2009). EIN2, the central regulator of ethylene signalling, is localized at the ER membrane where it interacts with the ethylene receptor ETR1. Biochem. J. 424, 1-6.
7. Breeze, E., Harrison, E., McHattie, S., Hughes, L., Hickman, R., Hill, C., Kiddle, S., Kim, Y.S., Penfold, C.A., Jenkins, D., et al. (2011). High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell. 23, 873-894.
8. Buchanan-Wollaston, V., Page, T., Harrison, E., Breeze, E., Lim, P.O., Nam, H.G., Lin, J.F., Wu, S.H., Swidzinski, J., and Ishizaki, K. (2005). Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42, 567-585.
9. Caldana, C., Scheible, W.R., Mueller-Roeber, B., and Ruzicic, S. (2007). A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods. 3, 7.
10. Chen, L.Q., Qu, X.Q., Hou, B.H., Sosso, D., Osorio, S., Fernie, A.R., and Frommer, W.B. (2012). Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 335, 207-211.
11. Farage-Barhom, S., Burd, S., Sonego, L., Mett, A., Belausov, E., Gidoni, D., and Lers, A. (2011). Localization of the Arabidopsis senescence- and cell death-associated BFN1 nuclease: from the ER to fragmented nuclei. Mol. Plant. 4, 1062-1073.
12. Farage-Barhom, S., Burd, S., Sonego, L., Perl-Treves, R., and Lers, A. (2008). Expression analysis of the BFN1 nuclease gene promoter during senescence, abscission, and programmed cell death-related processes. J. Exp. Bot. 59, 3247.
13. Gregersen, P.L., and Holm, P.B. (2007). Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotech J. 5, 192-206.
14. Guo, Y., and Gan, S. (2006). AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601-612.
15. Guo, Y., Cai, Z., and Gan, S. (2004). Transcriptome of Arabidopsis leaf senescence. Plant Cell Envir. 27, 521-549.
16. He, X.J., Mu, R.L., Ca, W.H., Zhang, Z.G., Zhang, J.S., and Chen, S.Y. (2005). AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J. 44, 903-916.
17. Ito, J., and Fukuda, H. (2002). ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell. 14, 3201-3211.
18. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
19. Jensen, M.K., Kjaersgaard, T., Nielsen, M.M., Galberg, P., Petersen, K., O'Shea, C., and Skriver, K. (2010). The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. Biochem J. 426, 183-196.
20. Karimi, M., Inzé, D., and Depicker, A. (2002). Gateway vectors for Agrobacterium- mediated plant transformation. Trends Plant Sci. 7, 193-195.
21. Kim, J.H., Woo, H.R., Kim, J., Lim, P.O., Lee, I.C., Choi, S.H., Hwang, D., and Nam, H.G. (2009). Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science. 323, 1053-1057.
22. Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., Mimura, T., Fukuda, H., and Demura, T. (2005). Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev. 19, 1855-1860.
23. Lai, A.G., Doherty, C.J., Mueller-Roeber, B., Kay S.A., Schippers, J.H., and Dijkwel, P.P. (2012). CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc. Natl Acad. Sci. U S A. 109, 17129-17134.
24. Lers, A., Sonego, L., Green, P.J., and Burd, S. (2006). Suppression of LX ribonuclease in tomato results in a delay of leaf senescence and abscission. Plant Physiol. 142, 710-721.
25. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
26. Olsen, A.N., Ernst, H.A., Leggio, L.L., and Skriver, K. (2005). DNAbinding specificity and molecular functions of NAC transcription factors. Plant Sci. 169, 785-797.
27. Ooka, H., Satoh, K., Doi, K., Nagata, T., Otomo, Y., Murakami, K., Matsubara, K., Osato, N., Kawai, J., Carninci, P., et al. (2003). Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. 10, 239-247.
28. Panavas, T., Pikula, A., Reid, P.D., Rubinstein, B., and Walker, E.L. (1999). Identification of senescence-associated genes from daylily petals. Plant Mol. Biol. 40, 237-248.
29. Parlitz, S., Kunze, R., Mueller-Roeber, B., and Balazadeh, S. (2011). Regulation of photosynthesis and transcription factor expression by leaf shading and re-illumination in Arabidopsis thaliana leaves. J. Plant Physiol. 168, 1311-1319.
30. Pérez-Amador, M.A., Abler, M.L., De Rocher, E.J., Thompson, D.M., van Hoof, A., LeBrasseur, N.D., Lers, A., and Green, P.J. (2000). Identification of BFN1, a bifunctional nuclease induced during leaf and stem senescence in Arabidopsis. Plant Physiol. 122, 169-180.
31. Plesch, G., Ehrhardt, T., and Mueller-Roeber, B. (2001). Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expression. Plant J. 28, 455-464.
32. Rauf, M., Arif, M., Dortay, H., Matallana-Ramírez, L.P., Waters, M. T., Nam, H.G., Lim, P.-O., Mueller-Roeber, B.and Balazadeh, S. (2013). ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO Rep., in press.
33. Sambrook, J., Fritsche, E.F., and Maniatis, T. (2001). Molecular Cloning: A Laboratory Manual, 3rd edn (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
34. Seo, P.J., Park, J.M., Kang, S.K., Kim, S.G., and Park, C.M. (2011). An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta. 233, 189-200.
35. Sheen J. (2002). A transient expression assay using Arabidopsis mesophyll protoplasts. Available online at http://genetics.mgh. harvard.edu/sheenweb/.
36. Skirycz, A., Reichelt, M., Burow, M., Birkemeyer, C., Rolcik, J., Kopka, J., Zanor, M.I., Gershenzon, J., Strnad, M., Szopa, J., et al. (2006). DOF transcription factor AtDof1. 1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J. 47, 10-24.
37. Van der Graaff, E., Schwacke, R., Schneider, A., Desimone, M., Flügge, U.I., and Kunze, R. (2006). Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 141, 776-792.
38. Wagstaff, C., Yang, T.J.W., Stead, A.D., Buchanan-Wollaston, V., and Roberts, J.A. (2009). A molecular and structural characterization of senescing Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. Plant J. 57, 690-705.
39. Wu, A., Allu, A.D., Garapati, P., Siddiqui, H., Dortay, H., Zanor, M.- I., Asensi-Fabado, M.A., Munné-Bosch, S., Antonio, C., Tohge, T., et al. (2012). JUNGBRUNNEN1, a reactive oxygen speciesresponsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell. 24, 482-506.
40. Xue, G.P. (2002). Characterisation of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid, quantitative and high-throughput analysis of the DNA-binding activity. Nucleic Acids Res. 30, e77.
41. Xue, G.P. (2005). A CELD-fusion method for rapid determination of the DNA-binding sequence specificity of novel plant DNAbinding proteins. Plant J. 41, 638-649.
42. Xue, G.-P., Bower, N.I., McIntyre, C.L., Riding, G.A., Kazan, K., and Shorter, R. (2006). TaNAC69 from the NAC superfamily of transcription factors is up-regulated by abiotic stresses in wheat and recognises two consensus DNA-binding sequences. Funct. Plant Biol. 33, 43-57.
43. Yang, S.D., Seo, P.J., Yoon, H.K., and Park, C.M. (2011). The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell. 23, 2155-2168.
44. Zhang, K., and Gan, S.S. (2012). An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol. 158, 961-969.
45. Zhong, R., Demura, T., and Ye, Z.H. (2006). SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell. 18, 3158-3170.
46. Zhong, R., Lee, C., and Ye, Z.H. (2010). Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol. Plant. 3, 1087-1103.