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Molecular Mechanisms in the Activation of Abscisic Acid Receptor PYR1

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  • Lyudmyla Dorosh
  • Olesya A Kharenko
  • Nandhakishore Rajagopalan
  • Michele C Loewen
  • Maria Stepanova

Abstract

The pyrabactin resistance 1 (PYR1)/PYR1-like (PYL)/regulatory component of abscisic acid (ABA) response (RCAR) proteins comprise a well characterized family of ABA receptors. Recent investigations have revealed two subsets of these receptors that, in the absence of ABA, either form inactive homodimers (PYR1 and PYLs 1–3) or mediate basal inhibition of downstream target type 2C protein phosphatases (PP2Cs; PYLs 4–10) respectively in vitro. Addition of ABA has been shown to release the apo-homodimers yielding ABA-bound monomeric holo-receptors that can interact with PP2Cs; highlighting a competitive-interaction process. Interaction selectivity has been shown to be mediated by subtle structural variations of primary sequence and ligand binding effects. Now, the dynamical contributions of ligand binding on interaction selectivity are investigated through extensive molecular dynamics (MD) simulations of apo and holo-PYR1 in monomeric and dimeric form as well as in complex with a PP2C, homology to ABA insensitive 1 (HAB1). Robust comparative interpretations were enabled by a novel essential collective dynamics approach. In agreement with recent experimental findings, our analysis indicates that ABA-bound PYR1 should efficiently bind to HAB1. However, both ABA-bound and ABA-extracted PYR1-HAB1 constructs have demonstrated notable similarities in their dynamics, suggesting that apo-PYR1 should also be able to make a substantial interaction with PP2Cs, albeit likely with slower complex formation kinetics. Further analysis indicates that both ABA-bound and ABA-free PYR1 in complex with HAB1 exhibit a higher intra-molecular structural stability and stronger inter-molecular dynamic correlations, in comparison with either holo- or apo-PYR1 dimers, supporting a model that includes apo-PYR1 in complex with HAB1. This possibility of a conditional functional apo-PYR1-PP2C complex was validated in vitro. These findings are generally consistent with the competitive-interaction model for PYR1 but highlight dynamical contributions of the PYR1 structure in mediating interaction selectivity suggesting added degrees of complexity in the regulation of the competitive-inhibition.Author Summary: Protein pyrabactin resistance 1 (PYR1) belongs to a group of PYR1-like (PYL) proteins that regulate plant development and responses to conditions of drought and salinity. Recent studies have reported characterization of their molecular structures as well as elucidation of important aspects of their function; highlighting their roles as receptors for the stress responsive phytohormone, abscisic acid (ABA). However details of the molecular mechanisms regulating their receptor signalling remain enigmatic. In this work, we use molecular dynamics simulations complemented by a sophisticated statistical-mechanical analysis to investigate structural and dynamical properties of PYR1 protein and how its interaction with ABA modifies receptor-protein complex formation. Our results provide detailed insight into how the PYR1-mediated inactivation of its downstream phosphatase target is regulated by homodimer formation and yield new hypotheses, supported by in vitro experiments, for further investigation. Ultimately, this knowledge provides insight into how plants respond to stress, with potential applications in the development of crops with improved growth characteristics and higher stress tolerance.

Suggested Citation

  • Lyudmyla Dorosh & Olesya A Kharenko & Nandhakishore Rajagopalan & Michele C Loewen & Maria Stepanova, 2013. "Molecular Mechanisms in the Activation of Abscisic Acid Receptor PYR1," PLOS Computational Biology, Public Library of Science, vol. 9(6), pages 1-17, June.
  • Handle: RePEc:plo:pcbi00:1003114
    DOI: 10.1371/journal.pcbi.1003114
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    1. Karsten Melcher & Ley-Moy Ng & X. Edward Zhou & Fen-Fen Soon & Yong Xu & Kelly M. Suino-Powell & Sang-Youl Park & Joshua J. Weiner & Hiroaki Fujii & Viswanathan Chinnusamy & Amanda Kovach & Jun Li & Y, 2009. "A gate–latch–lock mechanism for hormone signalling by abscisic acid receptors," Nature, Nature, vol. 462(7273), pages 602-608, December.
    2. Ken-ichi Miyazono & Takuya Miyakawa & Yoriko Sawano & Keiko Kubota & Hee-Jin Kang & Atsuko Asano & Yumiko Miyauchi & Mihoko Takahashi & Yuehua Zhi & Yasunari Fujita & Takuya Yoshida & Ken-Suke Kodaira, 2009. "Structural basis of abscisic acid signalling," Nature, Nature, vol. 462(7273), pages 609-614, December.
    3. Julia Santiago & Florine Dupeux & Adam Round & Regina Antoni & Sang-Youl Park & Marc Jamin & Sean R. Cutler & Pedro Luis Rodriguez & José Antonio Márquez, 2009. "The abscisic acid receptor PYR1 in complex with abscisic acid," Nature, Nature, vol. 462(7273), pages 665-668, December.
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