A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

Elife. 2017 Mar 21;6:e23361. doi: 10.7554/eLife.23361.

Abstract

Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3'-phosphoadenosine 5'- phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost1-2. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to fine-tune physiological responses.

Keywords: 3'-phosphoadenosine 5'-phosphate; A. thaliana; ABA signaling; chloroplast; plant biology; retrograde signaling; seed germination; stomatal closure; xenopus.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Abscisic Acid / metabolism*
  • Adenosine Diphosphate / metabolism*
  • Arabidopsis / physiology*
  • Chloroplasts / metabolism*
  • Gene Expression Regulation, Plant
  • Germination*
  • Plant Growth Regulators / metabolism
  • Plant Stomata / physiology*
  • Signal Transduction*

Substances

  • Plant Growth Regulators
  • Adenosine Diphosphate
  • Abscisic Acid
  • adenosine 3'-phosphate-5'-phosphate