Structural and functional principles of low potassium signaling and the integration of nutrient sensing and adaptation in Arabidopsis
Plant Physiology
Final Report Abstract
Collectively, the paradigm changing findings emanating from this project dramatically advanced our understanding of K+ sensing/signaling and organ scale K+ fluxes. Our K+ bioimaging approach revealed several surprising and most significant findings: Firstly, the stele comprises the root compartment of highest K+ concentration, which stays constant under HK and LK conditions. Secondly, the epidermis, including root hairs as the cell layer forming the root surface for K+ uptake, displays an unexpectedly low K+ concentration even with high K+ supply. Thirdly, we identified a lateral four-step cytoplasmic concentration pattern for K+, which already displays a significant increase in the cortex compared to the epidermis and further increases in the endodermis. This K+ pattern does not accord with dominant roles of apoplastic K+ fluxes and a dominant K+ distribution-determining function of the CS. Instead, this stepwise cytosolic K+ accumulation that we discovered demand faithfully coordinated celltype specific symplastic K+ fluxes and consequently points to a novel and so far not disclosed role of plasmodesmata and their regulation in establishing organ scale K+ pattern and fluxes. Indeed, in our LK transcriptomic analyses, we discovered at least one gene - whose protein product is known to confer plasmodesmata regulation – as being dramatically upregulated by LK. These findings initiated a novel line of research in which preliminary data indicate that LK exposure indeed induces callose deposition at plasmodesmata and appears to modulate plasmodesmata conductivity. Moreover, this project revealed a novel, sophisticated low-K+-specific signaling system that brings about transformation of K+ availability sensing at the cellular level into complex adaptive responses at the organ and organism scale. Importantly, we uncovered the identity of crucial components and delineated the mechanistic principles of a multilayered signaling axis in which LK-induced Ca2+ transients trigger CIF peptide signals to activate SGN3-LKS4/SGN1 receptor kinases. This in turn brings about ROS signal formation by RBOH NADPH oxidase phosphorylation to culminate in HAK5 K+ uptake transporter induction and CS maturation. In summary, our research uncovered a concept how plants integrate environmental cues with modulation of specific developmental programs at the molecular level. The rapid K+ signal formation in the KSN demanded active K+ transport as underlying mechanism. In novel unpublished work that we intend to continue in the future, we indeed identified a specific K+ channel that appears to be essential for proper K+ signal formation. Another fundamental question arising from this work is how the primary LK-induced Ca2+ signal mechanistically triggers enhanced CIF peptide signaling. This question is addressed in a new joint research project of CAU and WWU and in the course of this project we already identified one specific metacaspase (MC) as being required for LK resilience. Finally, this work revealed important biochemical evidence on how the primary LK-induced Ca2+ signal translates into CBL1/9- CIPK23-mediated activation of AKT1. The proposed differential contribution of individual CBL EF hands to this Ca2+-decoding/AKT1-activation process now becomes accessible for further investigation in in vivo systems.
Publications
- 2019, The transcription factor MYB59 regulates K+/NO3- translocation in the arabidopsis response to low K+ stress. Plant Cell
Du et al.
(See online at https://doi.org/10.1105/tpc.18.00674) - 2021, A potassium-sensing niche in Arabidopsis roots orchestrates signaling and adaptation responses to maintain nutrient homeostasis. Developmental Cell
Wang et al.
(See online at https://doi.org/10.1016/j.devcel.2021.02.027) - 2021, Emerging roles of the CBL-CIPK calcium signaling network as key regulatory hub in plant nutrition, Journal of Plant Physiology
Dong et al.
(See online at https://doi.org/10.1016/j.jplph.2020.153335)
