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Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (7): 969-981.doi: 10.3724/SP.J.1006.2019.84175

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Biosynthesis and signaling of ethylene and their regulation on seed germination and dormancy

SONG Song-Quan1,3,*(),LIU Jun2,XU Heng-Heng2,ZHANG Qi2,HUANG Hui3,WU Xian-Jin3   

  1. 1 Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
    2 Agro-Biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China
    3 Key Laboratory of Research and Utilization of Ethnomedicinal Plant Resources of Hunan Province / College of Biological and Food Engineering, Huaihua University, Huaihua 418008, Hunan, China
  • Received:2018-11-22 Accepted:2019-01-19 Online:2019-07-12 Published:2019-04-09
  • Contact: Song-Quan SONG E-mail:sqsong@ibcas.ac.cn
  • Supported by:
    This study was supported by the National Science and Technology Support Program(2012BAC01B05);the National Natural Science Foundation of China(31371715);the National Natural Science Foundation of China(31640059);the Guangdong Science and Technology Program(2016B030303007)

Abstract:

Seed germination, a key ecological and agronomic trait, is determined by both internal and external cues that regulate the dormancy status and the potential for germination in seeds, and plays a critical role during the subsequent growth, development and production of plants. Dormancy is the temporary failure of seed germination under favorable conditions. Ethylene is a simple gaseous phytohormone with multiple roles in regulation of metabolism at molecular, cellular, and whole plant levels. It influences performance of plants under optimal and stressful environments by interacting with other signaling molecules. In the present paper, we mainly summarize ethylene biosynthesis and signaling, the role of ethylene in seed germination and dormancy release, and the interaction of ethylene with phytohormone abscisic acid and gibberellin, and propose some scientific problems to be required to investigate further in order to provide an idea for explaining the molecular mechanism of seed germination and dormancy regulated by ethylene.

Key words: abscisic acid, biosynthesis and signaling, crosstalk, ethylene, gibberellin, seed germination and dormancy

Fig. 1

Ethylene biosynthetic pathway The formation of S-adenosyl methionine (S-AdoMet) from methionine is catalysed by S-AdoMet synthetase at the expense of one molecule of ATP per molecule of S-AdoMet synthesized (1). A rate-limiting step of ethylene synthesis is the conversion of S-AdoMet to ACC by ACC synthase (2). Methylthioadenosine (MTA) is the by-product generated, along with ACC, by ACC synthase. Recycling of MTA back to methionine conserves the methylthio group and is able to maintain a constant concentration of methionine in cells. Malonylation of ACC to malonyl-ACC depletes the ACC pool and reduces ethylene production. ACC oxidase catalyses the final step of ethylene synthesis using ACC as substrate and generates carbon dioxide and cyanide (3). Cyanide is metabolized by β-cyanoalanine synthase to produce non-toxic substances. Transcriptional regulation of both ACC synthase and ACC oxidase by homeotic proteins and developmental and environmental cues is indicated by dashed arrows. From Lin et al. [19]"

Fig. 2

The current model of the ethylene signaling pathway in Arabidopsis Ethylene is perceived by the receptor proteins ETR1, ERS1, ETR2, ERS2, and EIN4 (represented in green), the receptors are negative regulators of ethylene signaling. The receptors interact with other receptors and form higher order complexes in the ER membrane through their GAF domains (represented as pentagons in the receptors’ cytosolic domain). Copper (a cofactor for ethylene binding, red circles) is delivered to the receptors by the copper transporter RAN1 (represented in orange). RTE1 (in pink) is associated with ETR1 and mediates the receptor signal output. (A) In the absence of ethylene, the receptors activate CTR1 (in yellow). CTR1 inactivates EIN2 (in purple) by directly phosphorylating (blue circles) its C-terminal end. EIN2 can directly interact with the kinase domain of the receptors (represented as the larger ovals under the pentagons in the cytosolic domain of the receptors). The levels of EIN2 are negatively regulated by the F-box proteins ETP1 and ETP2 (green star) via the 26S proteasome (gray). In the nucleus, the transcription factors EIN3/EIL1 (in red) are being degraded by two other F-box proteins, EBF1/2 (blue star), through the proteasome. In the absence of EIN3/EIL1, transcription of the ethylene response genes is shut off. (B) In the presence of ethylene, the receptors bind the hormone and become inactivated, which in turn, switches off CTR1. This inactivation prevents the phosphorylation of the positive regulator EIN2. The C-terminal end of EIN2 is cleaved off by an unknown mechanism and moves to the nucleus where it stabilizes EIN3/EIL1 and induces degradation of EBF1/2. The transcription factors EIN3/EIL1 dimerize and activate the expression of ethylene target genes, including the F-box gene EBF2 (dark blue curly line) [which generates a negative feedback loop dampening the activity of the ethylene pathway] or the transcription factor gene ERF1 (light blue line) [which, in turn, initiates a transcriptional cascade resulting in the activation and repression of hundreds of ethylene-regulated genes]. Among the ethylene responsive genes the receptor gene is ETR2 (green line), whose mRNA is up-regulated by ethylene and translated into the new batch of ethylene-free receptor molecules which then activate the negative regulator CTR1, thus providing the means of tuning down ethylene signaling in the absence of additional ethylene. Other regulatory nodes in the pathway are the exoribonuclease EIN5 (light orange), which controls the levels of EBF2 mRNA, and the F-box proteins ETP1 and ETP2 (green star) that are degraded in the presence of ethylene leading to the stabilization of EIN2. Positive and negative arrows represent activation and down-regulation processes, respectively. Molecules shown in fading colors (EIN3/EIL1 in ‘no ethylene’, or ETP1/2 and EBF1/2 in ‘ethylene’) correspond to unstable proteins targeted to proteasome-mediated degradation. Curly lines indicate specific mRNAs, with their colors matching that of the corresponding proteins. From Merchante et al.[51]"

Table 1

Plant species whose seed dormancy is broken by ethylene, ethephon, or 1-aminocyclopropane-1-carboxylic acid (From Corbineau et al.[16])"

初生休眠 Primary dormancy 次生休眠 Secondary dormancy 热休眠 Thermo dormancy
尾穗苋 Amaranthus caudatus 尾穗苋 Amaranthus caudatus 莴苣 Lactuca sativa
反枝苋 Amaranthus retroflexus 繁穗苋 Amaranthus paniculatus
拟南芥 Arabidopsis thaliana 向日葵 Helianthus annuus
花生 Arachis hypogaea 莴苣 Lactuca sativa
Chenopodium album 皱叶酸模 Rumex crispus
欧洲水青冈 Fagus sylvatica 苣头苍耳 Xanthium pennsylvanicum
向日葵 Helianthus annuus
苹果 Malus pumila
南欧盐肤木 Rhus coriaria
皱叶酸模 Rumex crispus
柱花草 Stylosanthes humilis
地三叶 Trifolium subterraneum
苣头苍耳 Xanthium pennsylvanicum

Fig. 3

Interaction among ethylene, abscisic acid, and gibberellin in the regulation of seed germination and dormancy This scheme is based on genetic analyses, microarray data, and physiological studies on seed responsiveness to ethylene, ABA or GA cited in the text. Ethylene down-regulates ABA accumulation by both inhibiting its synthesis and promoting its inactivation or catabolism, and also negatively regulates ABA signaling. ABA inhibits ethylene biosynthesis through ACS and ACO activities. Ethylene also improves the GA metabolism and signaling, and vice versa. “→” and“ ┤” indicate positive and negative interactions between the different elements of the signaling cascade, respectively. Redrew from Corbineau et al. [16]."

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