Role of NAC transcription factors in plant senescence
Final Report Abstract
The execution of senescence is accompanied by massive transcriptional reprogramming, whereby NAC transcription factors (TFs) play crucial roles as regulators of gene expression during senescence. Within FOR948 we studied the roles of several NAC TFs for plant senescence, using Arabidopsis thaliana as model. Our results show that the various NACs control largely different sets of target genes and, hence, different physiological pathways relevant to the induction and execution of senescence. Notably, while most senescence-enhanced NAC genes appear to encode positive regulators of senescence (e.g. ORE1, ORS1, ATAF1, SHYG), others function as negative regulators (e.g. JUB1). More specifically, we made the following observations: ORE1 positively affects senescence by directly binding to the promoters of a number of well-known senescence-associated genes (SAGs), including e.g. BFN1, SAG29, and SINA1. Other groups showed direct binding of ORE1 to ACS2 (involved in ethylene biosynthesis) and various chlorophyll catabolite genes (CCGs). We observed that ORE1 not only controls age-dependent (i.e. developmental) senescence, but also senescence induced by salinity: plants overexpressing ORE1 showed enhanced senescence under salt stress, while delayed senescence is observed in the ore1 mutant. We discovered that ORE1 interacts at the protein level with the Golden-like 2 TFs GLK1 and GLK2, both of which are required for chloroplast development and maintenance. Through this interaction, ORE1 inhibits the GLKs and thus lowers their capacity to maintain chloroplast function. Thus, ORE1, which is not expressed in young leaves but shows increased expression when leaves age, functions in a dual manner to control senescence, i.e. by activating SAGs and by inhibiting GLKs. We further discovered that the NAC TF ATAF1 binds to the promoters of GLK1 and ORE1. However, while ATAF1 rapidly represses the expression of GLK1, it activates the expression of ORE1, thereby shifting the leaf´s physiology towards senescence. Furthermore, ATAF1 induces a carbon starvation transcriptome and metabolome, in part through direct control of the TREHALASE1 (TRE1) gene, which encodes the only known trehalase in Arabidopsis. Notably, ATAF1 itself is induced in conditions that lead to carbon/energy starvation (e.g. drought, extended night, low CO2 concentration), indicating the presence of a positive feedback loop in which ATAF1 acts. Finally, we found that autophagy (ATG) genes are induced by ATAF1, consistent with the role of autophagy in protein recycling during developmental leaf senescence and adverse environmental conditions that trigger senescence. We also discovered, that a NAC TF whose expression rises relatively early during leaf senescence, extends plant longevity when overexpressed, which led us to name it JUNGBRUNNEN1 (JUB1). In addition, overexpression of JUB1 increases the plant´s tolerance to different abiotic stresses, including salinity and heat stress. JUB1 directly regulates key stress-related genes, including DREB2A. Furthermore, it dampens the cellular concentration of H2O2, which in part may explain the delay in senescence and the enhanced stress tolerance. In summary, the project funded within FOR948 has led to considerable progress of our understanding of the role of NAC transcription factors for transcriptional reprogramming during senescence and has established a solid basis for further research.
Publications
- (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 62: 250-264
Balazadeh, S., Siddiqui, H., Allu, A.D., Matallana-Ramirez, L.P., Caldana, C., Mehrnia, M, Zanor, M.I., Kohler, B. and Mueller-Roeber, B.
(See online at https://doi.org/10.1111/j.1365-313X.2010.04151.x) - (2010) Salt-triggered expression of the ANAC092- dependent senescence regulon in Arabidopsis thaliana. Plant Sign. Behav. 5: 1-13
Balazadeh, S, Wu, A. and Mueller-Roeber, B.
(See online at https://doi.org/10.4161/psb.5.6.11694) - (2011) ORS1, a H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol. Plant. 8:1-15
Balazadeh, S., Kwasniewski, M., Caldana, C., Merhnia, M., Zanor, M.-I., Xue, G.-P. and Mueller- Roeber, B.
(See online at https://doi.org/10.1093/mp/ssq080) - (2011) Regulation of photosynthesis and transcription factor expression by leaf shading and re-illumination in Arabidopsis thaliana leaves. J. Plant Physiol. 168: 1311-1319
Parlitz, S., Kunze, R., Mueller-Roeber, B., and Balazadeh, S.
(See online at https://doi.org/10.1016/j.jplph.2011.02.001) - (2012) Expression of ROS- responsive genes and transcription factors after metabolic formation of H2O2 in chloroplasts. Front. Plant Sci. 3:234
Balazadeh, S., Jaspert, N., Arif, M., Mueller-Roeber, B. and Maurino, VG.
(See online at https://doi.org/10.3389/fpls.2012.00234) - (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell. 24: 482-506
Wu, A., Allu, AD., Garapati, P., Siddiqui, H., Dortay, H., Zanor, M-I., Asensi-Fabado, MA., Munné- Bosch, S., Antonio, C., Tohge, T., Fernie, A., Kaufmann, K., Xue, G-P., Mueller-Roeber, B. and Balazadeh, S.
(See online at https://doi.org/10.1105/tpc.111.090894) - (2012) Overproduction of chlorophyll b retards senescence through transcriptional re-programming in Arabidopsis. Plant & Cell Physiol. 53: 505-517
Sakuraba, Y., Balazadeh, S., Tanaka, R., Mueller-Roeber, B., and Tanaka, A.
(See online at https://doi.org/10.1093/pcp/pcs006) - (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol. 162:1290-1310
Watanabe M., Balazadeh S., Tohge T., Erban A., Giavalisco P., Kopka J., Mueller-Roeber B., Fernie A.R., Hoefgen R.
(See online at https://doi.org/10.1104/pp.113.217380) - (2013) NAC transcription factor ORE1 and BIFUNCTIONAL NUCLEASE1 (BFN1) constitute a regulatory cascade during senescence in Arabidopsis. Mol. Plant. 6: 1432-52
Matallana-Ramirez, L-P., Rauf, M., Farage-Barhom, S., Dortay, H., Xue, G-P., Dröge-Laser, W., Lers, A., Balazadeh, S. and Mueller-Roeber, B.
(See online at https://doi.org/10.1093/mp/sst012) - (2013) ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO Rep. 14: 382-388
Rauf, M., Muhammad, A., Dortay, H., Matallana-Ramírez, L-P., Waters, M., Nam, H-G., Lim, P-O., Mueller-Roeber, B. and Balazadeh, S.
(See online at https://doi.org/10.1038/embor.2013.24) - (2014) Reversion of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences. J. Exp. Bot. 65: 3975-3992
Balazadeh, S., Schildhauer, J., Wagner LA., Munné-Bosch, S., Fernie, AR., Proost, S., Humbeck, K. and Mueller-Roeber, B.
(See online at https://doi.org/10.1093/jxb/eru119) - (2014) Salt stress and senescence: Identification of crosstalk regulatory components. J. Exp. Bot. 65: 3993-4008
Allu, AD., Soja, AM., Wu, A., Szymanski, J. and Balazadeh, S.
(See online at https://doi.org/10.1093/jxb/eru173) - (2014) Stay-green not always stays green. Spotlight article. Mol. Plant 7: 1264-1266
Balazadeh S.
(See online at https://doi.org/10.1093/mp/ssu076) - (2015) GLYCOLATE OXIDASE3, a glycolate oxidase homolog of yeast L-lactate cytochrome c oxidoreductase, supports L-lactate oxidation in roots of Arabidopsis. Plant Physiol. 169: 1042-1061
Engqvist, M.K., Schmitz, J., Gertzmann, A., Florian, A., Jaspert, N., Arif, M., Balazadeh, S., Mueller- Roeber, B., Fernie, A.R. and Maurino, V.G.
(See online at https://doi.org/10.1104/pp.15.01003) - (2015) Transcription factor Arabidopsis Activating Factor1 integrates carbon starvation responses with trehalose metabolism. Plant Physiol. 169: 379-390
Garapati, P., Feil, R., Lunn, J.E., Van Dijck, P., Balazadeh, S., and Mueller-Roeber, B.
(See online at https://doi.org/10.1104/pp.15.00917) - (2015) Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiol. 168: 1122-1139
Garapati P, Xue GP, Munné-Bosch S, Balazadeh S
(See online at https://doi.org/10.1104/pp.15.00567) - (2015) Transcriptomic analysis of nitrogen starvation and cultivar-specific leaf senescence in winter oilseed rape (Brassica napus L.). Plant Sci. 233: 174-185
Koeslin-Findeklee, F., Rizi, V.S., Becker, M.A., Parra-Londono, S., Arif, M., Balazadeh, S., Mueller- Roeber, S., Kunze, R. and Horst, W.J.
(See online at https://doi.org/10.1016/j.plantsci.2014.11.018)
