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Hormonal cross-talk in plant organogenesis

Final Report Summary - HCPO (Hormonal cross-talk in plant organogenesis)

Plant hormones are important signalling molecules that control many developmental processes, including cell division, cell differentiation, organogenesis, and morphogenesis. They can regulate multitude of apparently unrelated physiological processes, with often overlapping roles and mutual modulation of their effects. This implies that synergistic and antagonistic interactions between different plant hormones play an important role in the regulation of plant development. However, the molecular basis of these hormonal interactions is still largely unknown.
The physiologically best characterized interaction is between the plant hormones auxins and cytokinins. Cytokinin and auxin synergistically interact to promote cell divisions in cell cultures, but antagonistically to regulate lateral root development or lateral bud outgrowth. The main aim of our research is to identify the molecular components and mechanisms that balance the output of auxin and cytokinin pathways to control plant organogenesis. We use lateral root organogenesis in Arabidopsis as an ideally suited model system, because it encompasses fundamental aspects of plant development, such as dedifferentiation, re-entry into the cell cycle, coordinated cell divisions and differentiation, and is regulated in an antagonistic manner by auxin and cytokinin.
Cytokinin modulation of the auxin efflux represents an important mode of the auxin-cytokinin interaction. Focusing on the underlying molecular mechanisms we found that cytokinin contributes to (i) the transcriptional control of auxin efflux carriers of PIN family and (ii) regulates their posttranscriptional stability. We identified unknown cytokinin response elements in the promoters of the AtPIN1 and AtPIN7 auxin efflux carriers. Using a yeast one-hybrid screen, we start to uncover the cytokinin-controlled upstream regulatory pathway. Besides transcriptional regulation, our recent data document the impact of cytokinin on the stability of the AtPIN1 protein and the involvement of posttranscriptional mechanisms. This finding disclosed the existence of an unknown cytokinin activity mode, conceptually different from the known signal transduction cascade, and opened new research directions and questions on hormonal regulation of plant development (Marhavy et al., Dev Cell 2011; Marhavy et al., Cur. Biol 2014).
Furthermore, our recent studies on cytokinin role in lateral root organogenesis reveal how cytokinin contributes to spatiotemporal regulation of lateral root organogenesis and show that the early phases of lateral root organogenesis including priming and initiation take place in the root zone with strongly repressed cytokinin responses (Bielach et al., Plant Cell 2012). Additionally, in our work focused on auxin role in lateral root organogenesis an unexpected function for the endodermis in the regulation of the early phases of lateral root initiation was observed. We demonstrated that a local, developmentally specific auxin re-flux between endodermal and founder cells is established which is required for the progress from founder to lateral root initiation phase (Marhavy et al., EMBO J, 2013).
To identify novel components of the auxin-cytokinin interaction, two main methodologies were applied, transcriptome profiling and forward genetic screening (Bielach et al., Philos Trans R Soc Lond B Biol Sci. 2012). Genes recovered from both the transcriptome profiling and the forward genetic screen represent strong candidates for novel cross-talk components to reveal mechanisms that integrate auxin and cytokinin signalling pathways.
Our previous studies have indicated that the formation of diverse organs, regardless of their developmental origin, share the common auxin-based developmental module as an underlying mechanism. We have demonstrated that there are common principles in the regulation of distinct developmental processes by these two hormones. For example, the stimulatory effect of ethylene on the auxin biosynthesis affects both root growth and apical hook formation. Similarly, in both ethylene-regulated root growth and apical hook development, the ethylene signalling component act upstream of the auxin signalling (Zadnikova et al., Developmment 2010). In addition, we have established several international collaborations to study other organogenic processes, such as ovule, vasculature, apical hook development with the aim to dissect common molecular mechanisms underlying the auxin-cytokinin interaction.