Abstract

Plants growing in any particular geographical location are exposed to variable and diverse environmental conditions throughout their lifespan. The multifactorial environmental pressure resulted into evolution of plant adaptation and survival strategies requiring ability to integrate multiple signals that combine to yield specific responses. These adaptive responses enable plants to maintain their growth and development while acquiring tolerance to a variety of environmental conditions. An essential signaling cascade that incorporates a wide range of exogenous as well as endogenous stimuli is multistep phosphorelay (MSP). MSP mediates the signaling of essential plant hormones that balance growth, development, and environmental adaptation. Nevertheless, the mechanisms by which specific signals are recognized by a commonly-occurring pathway are not yet clearly understood. Here we summarize our knowledge on the latest model of multistep phosphorelay signaling in plants and the molecular mechanisms underlying the integration of multiple inputs including both hormonal (cytokinins, ethylene and abscisic acid) and environmental (light and temperature) signals into a common pathway. We provide an overview of abiotic stress responses mediated via MSP signaling that are both hormone-dependent and independent. We highlight the mutual interactions of key players such as sensor kinases of various substrate specificities including their downstream targets. These constitute a tightly interconnected signaling network, enabling timely adaptation by the plant to an ever-changing environment. Finally, we propose possible future directions in stress-oriented research on MSP signaling and highlight its potential importance for targeted crop breeding.

Highlights

  • Plants growing in any particular geographical location are exposed to variable and diverse environmental conditions throughout their lifespan

  • We summarize our knowledge on the latest model of multistep phosphorelay signaling in plants and the molecular mechanisms underlying the integration of multiple inputs including both hormonal and environmental signals into a common pathway

  • In the light of several recent findings, implicating cytokininregulated multistep phosphorelay (MSP) signaling in the control over context-dependent chromatin accessibility (Potter et al, 2018), the well-documented role of ethylene in histone acetylation and abscisic acid (ABA)-dependent regulation of chromatin-remodeling complexes, we can venture to say that epigenetic regulations form part of the repertoire of transcription regulatory tools available to MSP, possibly mediating environmental “memory” used by the plants in their adaptation to short- and medium-term environmental fluctuations

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Summary

The Cytokinin Signaling Pathway

Due to historic reasons, much of the information about MSP has been on cytokinin signaling. The small and mobile cytosolic proteins, ARABIDOPSIS HISTIDINECONTAINING PHOSPHOTRANSMITTERs (AHPs) 1-5, which shuttle between the cytosol and the nucleus, mediate the step (Hwang and Sheen, 2001; Hutchison et al, 2006; Figure 1) and serve as a substrate for the phosphorylation of the terminal phosphate acceptors, the nuclear-located type-B ARABIDOPSIS RESPONSE REGULATORS (B-ARRs). Once the type B-ARRs are phosphorylated, inhibition on their GARP DNA-binding domain is released. This initiates the transcription of cytokininregulated genes, including the type-A RESPONSE REGULATORS (A-ARRs), the cytokinin primary-response genes, which function as negative feedback regulators of the signaling pathway (Kieber and Schaller, 2018). For more details we would like to point the reader to some excellent comprehensive reviews, e.g., those by Zürcher and Müller (2016) or Kieber and Schaller (2018)

Canonical Ethylene Signaling and Its Crosstalk With Multistep Phosphorelay
Crosstalk Between Light Signaling and Multistep Phosphorelay
Histidine Kinases Not Responsive to Hormone Signals
Canonical ABA Signaling
SENSING ABIOTIC STRESSES VIA MULTISTEP PHOSPHORELAY
Unknown Unknown Negative
Positive Positive Negative
Ethylene and ABA Crosstalk During Osmotic Stress
CONCLUSION AND FUTURE OUTLINES
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