Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme

Abstract

Abscisic acid (ABA) regulates abiotic stress and developmental responses including regulation of seed dormancy to prevent seeds from germinating under unfavorable environmental conditions. ABA HYPERSENSITIVE GERMINATION1 (AHG1) encoding a type 2C protein phosphatase (PP2C) is a central negative regulator of ABA response in germination; however, the molecular function and regulation of AHG1 remain elusive. Here we report that AHG1 interacts with DELAY OF GERMINATION1 (DOG1), which is a pivotal positive regulator in seed dormancy. DOG1 acts upstream of AHG1 and impairs the PP2C activity of AHG1 in vitro. Furthermore, DOG1 has the ability to bind heme. Binding of DOG1 to AHG1 and heme are independent processes, but both are essential for DOG1 function in vivo. Our study demonstrates that AHG1 and DOG1 constitute an important regulatory system for seed dormancy and germination by integrating multiple environmental signals, in parallel with the PYL/RCAR ABA receptor-mediated regulatory system.

Seed germination and dormancy: The classic story, new puzzles, and evolution

“…Loss of function mutations in AHG1 ( ahg1‐5 ) or AHG3 ( ahg3‐2 ) enhances seed dormancy, which is intensified in the double mutant ahg1‐5 ahg3‐2 (Née et al ). Similar results were observed also for the ahg1‐1 ahg3‐1 double mutant seeds (Nishimura et al ). These results indicate that the two AHG genes act redundantly in the dormancy pathway.…”

“…This mechanism is similar to the suppression of the ABA INSENSITIVE1 (ABI1) subfamily PP2Cs, including ABI1, ABI2, HYPERSENSITIVE TO ABI1 (HAB1) and HAB2, by the ABA receptors, such as PYRABACTIN RESISTANCE1 (PYR1) and PYR1‐LIKEs (PYLs), in the ABA perception and signaling pathway (Ma et al ; Park et al ; Cutler et al ) (Figure ). The inhibition of PP2C activity, which is the fundamental role of the ABA receptors, is also observed for the DOG1 protein (Nishimura et al ), although conflicting results were also observed in a separate study probably due to some factors missing in the in vitro experiments (Née et al ). Inactivation of PP2C may be an essential part of DOG1 function for seed dormancy.…”

“…A breakthrough in seed dormancy research in the past few years is that the biochemical function of DOG1, which was a long‐awaited question, was largely unfolded. Now, it is understood that DOG1 physically interacts with ABA HYPERSENSITIVE GERMINATION1 (AHG1) and AHG3, clade A protein phosphatases 2C (PP2Cs) (Née et al ; Nishimura et al ). AHG1 (Nishimura et al ; Nishimura et al ) and AHG3 (Yoshida et al ) are negative regulators of ABA signaling and seed dormancy.…”

“…Loss of function in AHG1 and AHG3 PP2Cs, which are negative regulators of ABA signaling, increases ABA sensitivity in seeds (Née et al ; Nishimura et al ). DOG1 is thought to enhance ABA sensitivity by binding and suppressing AHG1 and AHG3.…”

“…Based on Fujii et al ; Ma et al ; Park et al ; Cutler et al ; Antoni et al ; Née et al . Modified from Nonogaki and Nonogaki ; Nishimura et al . See text for details.…”