The role of the Arabidopsis FUSCA3transcription factor during inhibition of seed germination at high temperature

Rex S Chiu,Nicholas J Provart,Sonia Gazzarrini,Hardeep Nahal

doi:10.1186/1471-2229-12-15

Abstract

BackgroundImbibed seeds integrate environmental and endogenous signals to break dormancy and initiate growth under optimal conditions. Seed maturation plays an important role in determining the survival of germinating seeds, for example one of the roles of dormancy is to stagger germination to prevent mass growth under suboptimal conditions. The B3-domain transcription factor FUSCA3 (FUS3) is a master regulator of seed development and an important node in hormonal interaction networks in Arabidopsis thaliana. Its function has been mainly characterized during embryonic development, where FUS3 is highly expressed to promote seed maturation and dormancy by regulating ABA/GA levels.ResultsIn this study, we present evidence for a role of FUS3 in delaying seed germination at supraoptimal temperatures that would be lethal for the developing seedlings. During seed imbibition at supraoptimal temperature, the FUS3 promoter is reactivated and induces de novo synthesis of FUS3 mRNA, followed by FUS3 protein accumulation. Genetic analysis shows that FUS3 contributes to the delay of seed germination at high temperature. Unlike WT, seeds overexpressing FUS3 (ML1:FUS3-GFP) during imbibition are hypersensitive to high temperature and do not germinate, however, they can fully germinate after recovery at control temperature reaching 90% seedling survival. ML1:FUS3-GFP hypersensitivity to high temperature can be partly recovered in the presence of fluridone, an inhibitor of ABA biosynthesis, suggesting this hypersensitivity is due in part to higher ABA level in this mutant. Transcriptomic analysis shows that WT seeds imbibed at supraoptimal temperature activate seed-specific genes and ABA biosynthetic and signaling genes, while inhibiting genes that promote germination and growth, such as GA biosynthetic and signaling genes.ConclusionIn this study, we have uncovered a novel function for the master regulator of seed maturation, FUS3, in delaying germination at supraoptimal temperature. Physiologically, this is important since delaying germination has a protective role at high temperature. Transcriptomic analysis of seeds imbibed at supraoptimal temperature reveal that a complex program is in place, which involves not only the regulation of heat and dehydration response genes to adjust cellular functions, but also the activation of seed-specific programs and the inhibition of germination-promoting programs to delay germination.

Highlights

Imbibed seeds integrate environmental and endogenous signals to break dormancy and initiate growth under optimal conditions
Germination at supraoptimal temperature activates the FUS3 promoter and induces FUS3 mRNA and protein accumulation To test whether FUS3 plays a role during germination under abiotic stresses, we measured FUS3 mRNA levels in WT seeds imbibed on high salt (150 mM NaCl), during osmotic stress (300 mM mannitol) and at low (12°C) and high (32°C) temperatures (Figure 1)
FUS3 mRNA level increases 2-4 fold in seeds imbibed at 32°C for 24 h and 48 h, we investigated the role of FUS3 during seed germination at high temperature in more detail

Summary

Introduction

Imbibed seeds integrate environmental and endogenous signals to break dormancy and initiate growth under optimal conditions. Genetic and molecular studies have shown that seed maturation is orchestrated by the hormone abscisic acid (ABA) and a network of transcription factors, which include the LEAFY COTYLEDON1 (LEC1) CCAAT binding factor and the B3-domain transcription factors, LEC2, FUSCA3 (FUS3) and ABSCISIC ACID INSENSITIVE3 (ABI3) [2,3,4]. These genes are considered global regulators of seed maturation, as loss-of-function mutant embryos skip late-embryonic development and enter the vegetative program prematurely. The promoters of FUS3 and ABI3 are induced by auxin, while auxin biosynthetic genes are positively regulated by LEC2 and FUS3 [17,21,22,23]

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