Functional analysis of the role of the Arabidopsis NAC transcription factor JUNGBRUNNEN1 (JUB1) in GA and BR signalling
Plant Genetics and Genomics
Final Report Abstract
Abiotic stresses impair the growth, development and productivity of plants. Upon exposure to stress, plant growth decreases rapidly, due to massive allocation of energy and resources toward stress tolerance functions, but it can recover and adapt once the environmental condition become favorable again. This flexibility in plant growth patterns and architecture is partly facilitated by the action of plant hormones. Hormones form a signaling network and in a complex manner, through the crosstalk between different hormonal signaling pathways, control metabolic pathways which are required for growth, development and responses of plants to biotic and abiotic stresses. Gibberellins (GAs) and brassinosteroids (BRs) are two major growth-promoting hormones jointly promoting several similar developmental processes in plants. Identifying the components inhibiting or activating the expression and activities of key enzymes that determine fluxes in GA and BR biosynthesis is of particular agricultural importance. Plant transcription factors are master regulators of gene expression and therefore are involved in a variety of cellular processes including hormone biosynthesis and-/or signaling. Within the frame of this project, we gained a mechanistic understanding of the roles of Arabidopsis NAC transcription factor JUNGBRUNNEN1 (JUB1) in regulation of the crosstalk between growth and stress responses by modulating GA and BR biosynthesis/signaling. Overexpression of JUB1 resulted in typical GA/BR deficiency phenotypes such as short hypocotyls, dark-green curly leaves, dwarfism, late flowering and male sterility. Using JUB1 transgenic lines and employing a comprehensive set of technologies, we found that JUB1 negatively and directly regulates expression of GA3ox1 and DWF4, genes encoding rate-limiting enzymes of the biosynthetic pathways of gibberellic acids (GAs) and brassinosteroids (BRs), respectively. The inhibition of the two genes by JUB1 leads to reduced levels of GAs and BRs and hence the accumulation and activation of DELLA proteins acting as master suppressors of growth. Furthermore, we have shown that JUB1 suppression of growth hormones and accumulation of DELLA proteins is a major cause for enhanced resistance towards various abiotic stresses including salinity and heat stress. Combined overexpression of GA3ox1 and DWF4 in JUB1-OX lines suppressed the GA and BR deficiency as well as the enhanced abiotic stress tolerance phenotypes of JUB1-OX plants. We provided convincing evidence that JUB1-GA/BR regulation of plant development and stress responses are ultimately mediated through DELLA-dependent signalling pathways. In addition, we identified bHLH factor PHYTOCHROME INTERACTING FACTOR4 (PIF4), an important regulator of photomorphogenic development, and BZR1 as direct upstream transcriptional repressors of JUB1, forming feedback loops in the JUB1 regulatory network. We conclude that JUB1 is a central regulator of a complex cellular module that moderates key components of GA and BR synthesis and signaling pathways and is involved in fine-tuning plant growth and stress responses. JUB1 provides a new anchor point for future studies of plant growth and its interaction with stress, which holds great promise for improving the tolerance of plants against abiotic stresses in general. To our knowledge, this is the first report of a transcription factor that simultaneously and directly controls two key hormonal (GA and BR) biosynthesis pathways.
Publications
- (2016) Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nature Plants., 2: 16013
Shahnejat-Bushehri, S., Tarkowska, D., Sakuraba, S., and Balazadeh, S.
(See online at https://doi.org/10.1038/NPLANTS.2016.13) - (2016) JUB1 represses Pseudomonas syringae-induced defence responses through accumulation of DELLA proteins. Plant Signaling & Behavior., 11: e1181245
Shahnejat-Bushehri, S., Nobmann, B., Allu, A.D., and Balazadeh, S.
(See online at https://doi.org/10.1080/15592324.2016.1181245) - (2017) Arabidopsis NAC transcription factor JUNGBRUNNEN1 exerts conserved control over gibberellin and brassinosteroid metabolism and signaling genes in tomato. Frontiers in Plant Science., 8:214
Shahnejat-Bushehri, S., Allu, A.D., Mehterov, N., Thirumalaikumar, V.P., Alseekh, S., Fernie, A.R., Mueller-Roeber, B. and Balazadeh, S.
(See online at https://doi.org/10.3389/fpls.2017.00214)
