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Seed Dormancy: Molecular Control of Its Induction and Alleviation
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Seed Dormancy: Molecular Control of Its Induction and Alleviation

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (30 April 2020) | Viewed by 34549

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A printed edition of this Special Issue is available here.

Special Issue Editor

Prof. Dr. Angel J. Matilla

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Guest Editor
Departamento de Biología Funcional (Área Fisiología Vegetal), Facultad de Farmacia, Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain
Interests: molecular and physiological aspects of seeds development
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The seed, a key entity in the life cycle of higher plants, allows and ensures its survival by acquiring primary dormancy, which is hormonally induced and then maintained and strictly regulated by the modulation of a suitable hormonal signaling network. The dormancy of some seeds can be relieved through a tightly regulated process called after-ripening (AR) that occurs in dry, mature, and viable seeds stored in dry conditions. As a result of AR, abundant changes of transcripts take place and the window of environmental conditions that allow seed germination widens. The events occurring during this loss of dormancy are of significant functional, ecological, and agricultural interest. Genetic, –omics, and physiological studies about AR have shown the key role of the balance between gibberellins (GAs) and abscisic acid (ABA) metabolism and sensitivity. Recent evidence also supports a possible role of ethylene in AR execution and modulation. However, hormone-independent signals (e.g., reactive oxygen species (ROS) and nitrate) also appear to be involved in the triggering and maintenance of AR. The way in which hormone- and non-hormone-signaling pathways affect each other is still scarcely known. With all these aforementioned factors put together, the implementation of AR involves genes associated with the completion of germination. Nevertheless, the complexity and diversity of mechanisms that trigger and control AR is a great puzzle, with the majority of its pieces still missing.

Prof. Angel J. Matilla
Guest Editor

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Keywords

  • AR mutants
  • cell wall degradation
  • monocot- and dicot-seeds
  • phytohormones
  • RBOHD genes
  • ROS homeostasis mutants
  • seed pathogenesis
  • specific regulators of AR
  • tissue specificity of gene expression

Related Special Issue

Published Papers (7 papers)

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Editorial

Jump to: Research, Review

6 pages, 233 KiB  
Editorial
Seed Dormancy: Molecular Control of Its Induction and Alleviation
by Angel J. Matilla
Plants 2020, 9(10), 1402; https://doi.org/10.3390/plants9101402 - 21 Oct 2020
Cited by 21 | Viewed by 3471
Abstract
A set of seed dormancy traits is included in this Special Issue. Thus, DELAY OF GERMINATION1 (DOG1) is reviewed in depth. Binding of DOG1 to Protein Phosphatase 2C ABSCISIC ACID (PP2C ABA) Hypersensitive Germination (AHG1) and heme are independent processes, but both are [...] Read more.
A set of seed dormancy traits is included in this Special Issue. Thus, DELAY OF GERMINATION1 (DOG1) is reviewed in depth. Binding of DOG1 to Protein Phosphatase 2C ABSCISIC ACID (PP2C ABA) Hypersensitive Germination (AHG1) and heme are independent processes, but both are essential for DOG1’s function in vivo. AHG1 and DOG1 constitute a regulatory system for dormancy and germination. DOG1 affects the ABA INSENSITIVE5 (ABI5) expression level. Moreover, reactive oxygen species (ROS) homeostasis is linked with seed after-ripening (AR) process and the oxidation of a portion of seed long-lived (SLL) mRNAs seems to be related to dormancy release. The association of SLL mRNAs to monosomes is required for their transcriptional upregulation at the beginning of germination. Global DNA methylation levels remain stable during dormancy, decreasing when germination occurs. The remarkable intervention of auxin in the life of the seed is increasingly evident year after year. Here, its synergistic cooperation with ABA to promote the dormancy process is extensively reviewed. ABI3 participation in this process is critical. New data on the effect of alternating temperatures (ATs) on dormancy release are contained in this Special Issue. On the one hand, the transcriptome patterns stimulated at ATs comprised ethylene and ROS signaling and metabolism together with ABA degradation. On the other hand, a higher physical dormancy release was observed in Medicago truncatula under 35/15 °C than under 25/15 °C, and genome-wide association analysis identified 136 candidate genes related to secondary metabolite synthesis, hormone regulation, and modification of the cell wall. Finally, it is suggested that changes in endogenous γ-aminobutyric acid (GABA) may prevent chestnut germination, and a possible relation with H2O2 production is considered. Full article
(This article belongs to the Special Issue Seed Dormancy: Molecular Control of Its Induction and Alleviation)

Research

Jump to: Editorial, Review

19 pages, 2739 KiB  
Article
Seed Transcriptome Annotation Reveals Enhanced Expression of Genes Related to ROS Homeostasis and Ethylene Metabolism at Alternating Temperatures in Wild Cardoon
by Hector R. Huarte, Giuseppe. D. Puglia, Andrey D. Prjibelski and Salvatore A. Raccuia
Plants 2020, 9(9), 1225; https://doi.org/10.3390/plants9091225 - 18 Sep 2020
Cited by 11 | Viewed by 2918
Abstract
The association among environmental cues, ethylene response, ABA signaling, and reactive oxygen species (ROS) homeostasis in the process of seed dormancy release is nowadays well-established in many species. Alternating temperatures are recognized as one of the main environmental signals determining dormancy release, but [...] Read more.
The association among environmental cues, ethylene response, ABA signaling, and reactive oxygen species (ROS) homeostasis in the process of seed dormancy release is nowadays well-established in many species. Alternating temperatures are recognized as one of the main environmental signals determining dormancy release, but their underlying mechanisms are scarcely known. Dry after-ripened wild cardoon achenes germinated poorly at a constant temperature of 20, 15, or 10 °C, whereas germination was stimulated by 80% at alternating temperatures of 20/10 °C. Using an RNA-Seq approach, we identified 23,640 and annotated 14,078 gene transcripts expressed in dry achenes and achenes exposed to constant or alternating temperatures. Transcriptional patterns identified in dry condition included seed reserve and response to dehydration stress genes (i.e., HSPs, peroxidases, and LEAs). At a constant temperature, we observed an upregulation of ABA biosynthesis genes (i.e., NCED9), ABA-responsive genes (i.e., ABI5 and TAP), as well as other genes previously related to physiological dormancy and inhibition of germination. However, the alternating temperatures were associated with the upregulation of ethylene metabolism (i.e., ACO1, 4, and ACS10) and signaling (i.e., EXPs) genes and ROS homeostasis regulators genes (i.e., RBOH and CAT). Accordingly, the ethylene production was twice as high at alternating than at constant temperatures. The presence in the germination medium of ethylene or ROS synthesis and signaling inhibitors reduced significantly, but not completely, germination at 20/10 °C. Conversely, the presence of methyl viologen and salicylhydroxamic acid (SHAM), a peroxidase inhibitor, partially increased germination at constant temperature. Taken together, the present study provides the first insights into the gene expression patterns and physiological response associated with dormancy release at alternating temperatures in wild cardoon (Cynara cardunculus var. sylvestris). Full article
(This article belongs to the Special Issue Seed Dormancy: Molecular Control of Its Induction and Alleviation)
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20 pages, 3137 KiB  
Article
Physical Dormancy Release in Medicago truncatula Seeds Is Related to Environmental Variations
by Juan Pablo Renzi, Martin Duchoslav, Jan Brus, Iveta Hradilová, Vilém Pechanec, Tadeáš Václavek, Jitka Machalová, Karel Hron, Jerome Verdier and Petr Smýkal
Plants 2020, 9(4), 503; https://doi.org/10.3390/plants9040503 - 14 Apr 2020
Cited by 16 | Viewed by 4330
Abstract
Seed dormancy and timing of its release is an important developmental transition determining the survival of individuals, populations, and species in variable environments. Medicago truncatula was used as a model to study physical seed dormancy at the ecological and genetics level. The effect [...] Read more.
Seed dormancy and timing of its release is an important developmental transition determining the survival of individuals, populations, and species in variable environments. Medicago truncatula was used as a model to study physical seed dormancy at the ecological and genetics level. The effect of alternating temperatures, as one of the causes releasing physical seed dormancy, was tested in 178 M. truncatula accessions over three years. Several coefficients of dormancy release were related to environmental variables. Dormancy varied greatly (4–100%) across accessions as well as year of experiment. We observed overall higher physical dormancy release under more alternating temperatures (35/15 °C) in comparison with less alternating ones (25/15 °C). Accessions from more arid climates released dormancy under higher experimental temperature alternations more than accessions originating from less arid environments. The plasticity of physical dormancy can probably distribute the germination through the year and act as a bet-hedging strategy in arid environments. On the other hand, a slight increase in physical dormancy was observed in accessions from environments with higher among-season temperature variation. Genome-wide association analysis identified 136 candidate genes related to secondary metabolite synthesis, hormone regulation, and modification of the cell wall. The activity of these genes might mediate seed coat permeability and, ultimately, imbibition and germination. Full article
(This article belongs to the Special Issue Seed Dormancy: Molecular Control of Its Induction and Alleviation)
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15 pages, 3689 KiB  
Article
Effects of GABA and Vigabatrin on the Germination of Chinese Chestnut Recalcitrant Seeds and Its Implications for Seed Dormancy and Storage
by Changjian Du, Wei Chen, Yanyan Wu, Guangpeng Wang, Jiabing Zhao, Jiacheng Sun, Jing Ji, Donghui Yan, Zeping Jiang and Shengqing Shi
Plants 2020, 9(4), 449; https://doi.org/10.3390/plants9040449 - 03 Apr 2020
Cited by 16 | Viewed by 3987
Abstract
Recalcitrant chestnut seeds are rich in γ-aminobutyric acid (GABA), which negatively regulates adventitious root development by altering carbon/nitrogen metabolism. However, little is known regarding the role of this metabolite in chestnut seeds. In this study, we investigated the effects of GABA changes on [...] Read more.
Recalcitrant chestnut seeds are rich in γ-aminobutyric acid (GABA), which negatively regulates adventitious root development by altering carbon/nitrogen metabolism. However, little is known regarding the role of this metabolite in chestnut seeds. In this study, we investigated the effects of GABA changes on the germination of chestnut seeds treated with exogenous GABA and vigabatrin (VGB, which inhibits GABA degradation). Both treatments significantly inhibited seed germination and primary root growth and resulted in the considerable accumulation of H2O2, but the endogenous GABA content decreased before germination at 48 h. Soluble sugar levels increased before germination, but subsequently decreased, whereas starch contents were relatively unchanged. Changes to organic acids were observed at 120 h after sowing, including a decrease and increase in citrate and malate levels, respectively. Similarly, soluble protein contents increased at 120 h, but the abundance of most free amino acids decreased at 48 h. Moreover, the total amino acid levels increased only in response to VGB at 0 h. Accordingly, GABA and VGB altered the balance of carbon and nitrogen metabolism, thereby inhibiting chestnut seed germination. These results suggested that changes to GABA levels in chestnut seeds might prevent seed germination. The study data may also help clarify the dormancy and storage of chestnut seeds, as well as other recalcitrant seeds. Full article
(This article belongs to the Special Issue Seed Dormancy: Molecular Control of Its Induction and Alleviation)
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Review

Jump to: Editorial, Research

17 pages, 747 KiB  
Review
Auxin: Hormonal Signal Required for Seed Development and Dormancy
by Angel J. Matilla
Plants 2020, 9(6), 705; https://doi.org/10.3390/plants9060705 - 01 Jun 2020
Cited by 43 | Viewed by 6025
Abstract
The production of viable seeds is a key event in the life cycle of higher plants. Historically, abscisic acid (ABA) and gibberellin (GAs) were considered the main hormones that regulate seed formation. However, auxin has recently emerged as an essential player that modulates, [...] Read more.
The production of viable seeds is a key event in the life cycle of higher plants. Historically, abscisic acid (ABA) and gibberellin (GAs) were considered the main hormones that regulate seed formation. However, auxin has recently emerged as an essential player that modulates, in conjunction with ABA, different cellular processes involved in seed development as well as the induction, regulation and maintenance of primary dormancy (PD). This review examines and discusses the key role of auxin as a signaling molecule that coordinates seed life. The cellular machinery involved in the synthesis and transport of auxin, as well as their cellular and tissue compartmentalization, is crucial for the development of the endosperm and seed-coat. Thus, auxin is an essential compound involved in integuments development, and its transport from endosperm is regulated by AGAMOUS-LIKE62 (AGL62) whose transcript is specifically expressed in the endosperm. In addition, recent biochemical and genetic evidence supports the involvement of auxins in PD. In this process, the participation of the transcriptional regulator ABA INSENSITIVE3 (ABI3) is critical, revealing a cross-talk between auxin and ABA signaling. Future experimental aimed at advancing knowledge of the role of auxins in seed development and PD are also discussed. Full article
(This article belongs to the Special Issue Seed Dormancy: Molecular Control of Its Induction and Alleviation)
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14 pages, 1273 KiB  
Review
Reactive Oxygen Species (ROS) and Nucleic Acid Modifications during Seed Dormancy
by Kai Katsuya-Gaviria, Elena Caro, Néstor Carrillo-Barral and Raquel Iglesias-Fernández
Plants 2020, 9(6), 679; https://doi.org/10.3390/plants9060679 - 27 May 2020
Cited by 32 | Viewed by 5917
Abstract
The seed is the propagule of higher plants and allows its dissemination and the survival of the species. Seed dormancy prevents premature germination under favourable conditions. Dormant seeds are only able to germinate in a narrow range of conditions. During after-ripening (AR), a [...] Read more.
The seed is the propagule of higher plants and allows its dissemination and the survival of the species. Seed dormancy prevents premature germination under favourable conditions. Dormant seeds are only able to germinate in a narrow range of conditions. During after-ripening (AR), a mechanism of dormancy release, seeds gradually lose dormancy through a period of dry storage. This review is mainly focused on how chemical modifications of mRNA and genomic DNA, such as oxidation and methylation, affect gene expression during late stages of seed development, especially during dormancy. The oxidation of specific nucleotides produced by reactive oxygen species (ROS) alters the stability of the seed stored mRNAs, being finally degraded or translated into non-functional proteins. DNA methylation is a well-known epigenetic mechanism of controlling gene expression. In Arabidopsis thaliana, while there is a global increase in CHH-context methylation through embryogenesis, global DNA methylation levels remain stable during seed dormancy, decreasing when germination occurs. The biological significance of nucleic acid oxidation and methylation upon seed development is discussed. Full article
(This article belongs to the Special Issue Seed Dormancy: Molecular Control of Its Induction and Alleviation)
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20 pages, 2074 KiB  
Review
Delay of Germination-1 (DOG1): A Key to Understanding Seed Dormancy
by Néstor Carrillo-Barral, María del Carmen Rodríguez-Gacio and Angel Jesús Matilla
Plants 2020, 9(4), 480; https://doi.org/10.3390/plants9040480 - 09 Apr 2020
Cited by 50 | Viewed by 7129
Abstract
DELAY OF GERMINATION-1 (DOG1), is a master regulator of primary dormancy (PD) that acts in concert with ABA to delay germination. The ABA and DOG1 signaling pathways converge since DOG1 requires protein phosphatase 2C (PP2C) to control PD. DOG1 enhances ABA signaling through [...] Read more.
DELAY OF GERMINATION-1 (DOG1), is a master regulator of primary dormancy (PD) that acts in concert with ABA to delay germination. The ABA and DOG1 signaling pathways converge since DOG1 requires protein phosphatase 2C (PP2C) to control PD. DOG1 enhances ABA signaling through its binding to PP2C ABA HYPERSENSITIVE GERMINATION (AHG1/AHG3). DOG1 suppresses the AHG1 action to enhance ABA sensitivity and impose PD. To carry out this suppression, the formation of DOG1-heme complex is essential. The binding of DOG1-AHG1 to DOG1-Heme is an independent processes but essential for DOG1 function. The quantity of active DOG1 in mature and viable seeds is correlated with the extent of PD. Thus, dog1 mutant seeds, which have scarce endogenous ABA and high gibberellin (GAs) content, exhibit a non-dormancy phenotype. Despite being studied extensively in recent years, little is known about the molecular mechanism underlying the transcriptional regulation of DOG1. However, it is well-known that the physiological function of DOG1 is tightly regulated by a complex array of transformations that include alternative splicing, alternative polyadenylation, histone modifications, and a cis-acting antisense non-coding transcript (asDOG1). The DOG1 becomes modified (i.e., inactivated) during seed after-ripening (AR), and its levels in viable seeds do not correlate with germination potential. Interestingly, it was recently found that the transcription factor (TF) bZIP67 binds to the DOG1 promoter. This is required to activate DOG1 expression leading to enhanced seed dormancy. On the other hand, seed development under low-temperature conditions triggers DOG1 expression by increasing the expression and abundance of bZIP67. Together, current data indicate that DOG1 function is not strictly limited to PD process, but that it is also required for other facets of seed maturation, in part by also interfering with the ethylene signaling components. Otherwise, since DOG1 also affects other processes such us flowering and drought tolerance, the approaches to understanding its mechanism of action and control are, at this time, still inconclusive. Full article
(This article belongs to the Special Issue Seed Dormancy: Molecular Control of Its Induction and Alleviation)
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