AHK5 mediates ETR1-initiated multistep phosphorelay in Arabidopsis

Abstract

Plants, like other sessile organisms, need to sense many different signals, and in response to them, modify their developmental programs to be able to survive in a highly changing environment. The multistep phosphorelay (MSP) in plants is a good candidate for a response mechanism that integrates multiple signal types both environmental and intrinsic in origin. Recently, ethylene was shown to control MSP activity via the histidine kinase (HK) activity of ETHYLENE RESPONSE 1 (ETR1)1,2, but the underlying molecular mechanism still remains unclear. Here we show that although ETR1 is an active HK, its receiver domain (ETR1RD) is structurally and functionally unable to accept the phosphate from the phosphorylated His in the ETR1 HK domain (ETR1HK) to initiate the phosphorelay to ARABIDOPSIS HISTIDINE-CONTAINING PHOSPHOTRANSMITTERs (AHPs), the next link downstream members in MSP signaling. Instead, ETR1 interacts with another HK ARABIDOPSIS HISTIDINE KINASE 5 (AHK5) and transfers the phosphate from ETR1HK through the receiver domain of AHK5 (AHK5RD), and subsequently to AHP1, AHP2 and AHP3, independently of the HK activity of AHK5. We show that AHK5 is necessary for ethylene-initiated, but not cytokinin-initiated, MSP signaling in planta and that it thus mediates hormonal control of root growth.

Cytokinins regulate spatially-specific ethylene production to control root growth inArabidopsis

“…Both hormones were shown to control root growth and adaptation by mediating interaction between intrinsic developmental pathways, regulating root development and patterning very early in embryogenesis (Yamoune et al, 2021) and environmental signals (Skalak et al, 2021). This allows the root not only to adapt to immediate conditions including e.g., water availability or soil compaction at the level of root growth and architecture (Chang et al, 2019;Pandey et al, 2021;Park et al, 2018;Saucedo et al, 2012;Szmitkowska et al, 2021;Waidmann and Kleine-Vehn, 2020;Waidmann et al, 2019), but also to anticipate future development and capitalize from past experience via hormone-regulated priming to different stresses (Cortleven et al, 2019;Kosakivska et al, 2022;Skalak et al, 2021;Tiwari et al, 2022). A detailed description of the underlying molecular mechanisms is critical in order to understand the principles activating growth or defense responses in plants and the identification of novel breeding targets.…”

“…Briefly, ETR1 was shown to mediate ethylene-regulated MSP signaling in the root transition zone to control RAM size via ethylene-induced cell differentiation (Street et al, 2015; Zdarska et al, 2019). The action of ETR1 was proposed be mediated via ETR1-induced phosphorylation of the histine kinase AHK5 (Szmitkowska et al, 2021), eventually leading to the phosphorylation of RRB ARR2 (Hass et al, 2004). In rice, the ethylene sensor OsERS2 was shown to interact with the AHK5 orthologue MHZ1/OsHK1 and control its HK activity (Zhao et al, 2020).…”

Shoot phenotyping of cytokinin receptors mutants revealed fluorescence parameters as early markers of drought stress

“…Interestingly, although the cytokinin receptors seem to act as negative regulators of drought tolerance, the cytokinin-independent AHK1 is a positive effector of water-deficiency tolerance and is a potential osmosensor (Tran et al ., 2007; Wohlbach et al ., 2008; Kumar et al ., 2013). Further, AHK5 negatively regulates plant tolerance to osmotic and drought stress, possibly due to its role in ROS-dependent stomatal closure and crosstalk with ethylene and ABA signalling (Iwama et al ., 2006; Desikan et al ., 2008; Pham and Desikan, 2012; Pham et al ., 2012; Szmitkowska et al ., 2021).…”