Most cited article - PubMed ID 25114251
DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature- and gibberellin-dependent control of seed germination
Seed dormancy is an adaptation that delays germination to prevent the start of this process during unsuitable conditions. It is crucial in wild species but its loss was selected during crop domestication to ensure a fast and uniform germination. Water uptake, or imbibition, is the first step of germination. In the Fabaceae family, seeds have physical dormancy, in which seed coats are impermeable to water. We used an interspecific cross between an elite lentil line (Lens culinaris) and a wild lentil (L. orientalis) to investigate the genetic basis of imbibition capacity through quantitative trait locus (QTL) mapping and by using RNA from embryos and seed coats at different development stages, and phenotypic data of seed coat thickness (SCT) and proportion of imbibed seeds (PIS). Both characteristics were consistent throughout different years and locations, suggesting a hereditary component. QTL results suggest that they are each controlled by relatively few loci. Differentially expressed genes (DEGs) within the QTL were considered candidate genes. Two glycosyl-hydrolase genes (a β-glucosidase and a β-galactosidase), which degrade complex polysaccharides in the cell wall, were found among the candidate genes, and one of them had a positive correlation (β-glucosidase) between gene expression and imbibition capacity, and the other gene (β-galactosidase) presented a negative correlation between gene expression and SCT.
- MeSH
- Lens Plant * genetics physiology MeSH
- Domestication * MeSH
- Phenotype MeSH
- Germination genetics MeSH
- Quantitative Trait Loci MeSH
- Chromosome Mapping MeSH
- Gene Expression Regulation, Plant MeSH
- Seeds * genetics growth & development physiology MeSH
- Gene Expression Profiling MeSH
- Transcriptome * MeSH
- Plant Dormancy * genetics MeSH
- Publication type
- Journal Article MeSH
Plants in habitats with unpredictable conditions often have diversified bet-hedging strategies that ensure fitness over a wider range of variable environmental factors. A striking example is the diaspore (seed and fruit) heteromorphism that evolved to maximize species survival in Aethionema arabicum (Brassicaceae) in which external and endogenous triggers allow the production of two distinct diaspores on the same plant. Using this dimorphic diaspore model, we identified contrasting molecular, biophysical, and ecophysiological mechanisms in the germination responses to different temperatures of the mucilaginous seeds (M+ seed morphs), the dispersed indehiscent fruits (IND fruit morphs), and the bare non-mucilaginous M- seeds obtained by pericarp (fruit coat) removal from IND fruits. Large-scale comparative transcriptome and hormone analyses of M+ seeds, IND fruits, and M- seeds provided comprehensive datasets for their distinct thermal responses. Morph-specific differences in co-expressed gene modules in seeds, as well as in seed and pericarp hormone contents, identified a role of the IND pericarp in imposing coat dormancy by generating hypoxia affecting abscisic acid (ABA) sensitivity. This involved expression of morph-specific transcription factors, hypoxia response, and cell wall remodeling genes, as well as altered ABA metabolism, transport, and signaling. Parental temperature affected ABA contents and ABA-related gene expression and altered IND pericarp biomechanical properties. Elucidating the molecular framework underlying the diaspore heteromorphism can provide insight into developmental responses to globally changing temperatures.
- MeSH
- Brassicaceae * genetics physiology metabolism MeSH
- Germination * genetics physiology MeSH
- Abscisic Acid metabolism MeSH
- Fruit * genetics physiology growth & development metabolism MeSH
- Gene Expression Regulation, Plant * MeSH
- Plant Growth Regulators metabolism MeSH
- Seeds * genetics physiology growth & development metabolism MeSH
- Temperature * MeSH
- Transcriptome genetics MeSH
- Plant Dormancy genetics physiology MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Abscisic Acid MeSH
- Plant Growth Regulators MeSH
The transition from germinating seeds to emerging seedlings is one of the most vulnerable plant life cycle stages. Heteromorphic diaspores (seed and fruit dispersal units) are an adaptive bet-hedging strategy to cope with spatiotemporally variable environments. While the roles and mechanisms of seedling traits have been studied in monomorphic species, which produce one type of diaspore, very little is known about seedlings in heteromorphic species. Using the dimorphic diaspore model Aethionema arabicum (Brassicaceae), we identified contrasting mechanisms in the germination responses to different temperatures of the mucilaginous seeds (M+ seed morphs), the dispersed indehiscent fruits (IND fruit morphs), and the bare non-mucilaginous M- seeds obtained from IND fruits by pericarp (fruit coat) removal. What follows the completion of germination is the pre-emergence seedling growth phase, which we investigated by comparative growth assays of early seedlings derived from the M+ seeds, bare M- seeds, and IND fruits. The dimorphic seedlings derived from M+ and M- seeds did not differ in their responses to ambient temperature and water potential. The phenotype of seedlings derived from IND fruits differed in that they had bent hypocotyls and their shoot and root growth was slower, but the biomechanical hypocotyl properties of 15-day-old seedlings did not differ between seedlings derived from germinated M+ seeds, M- seeds, or IND fruits. Comparison of the transcriptomes of the natural dimorphic diaspores, M+ seeds and IND fruits, identified 2,682 differentially expressed genes (DEGs) during late germination. During the subsequent 3 days of seedling pre-emergence growth, the number of DEGs was reduced 10-fold to 277 root DEGs and 16-fold to 164 shoot DEGs. Among the DEGs in early seedlings were hormonal regulators, in particular for auxin, ethylene, and gibberellins. Furthermore, DEGs were identified for water and ion transporters, nitrate transporter and assimilation enzymes, and cell wall remodeling protein genes encoding enzymes targeting xyloglucan and pectin. We conclude that the transcriptomes of seedlings derived from the dimorphic diaspores, M+ seeds and IND fruits, undergo transcriptional resetting during the post-germination pre-emergence growth transition phase from germinated diaspores to growing seedlings.
Production of morphologically and physiologically variable seeds is an important strategy that helps plants to survive in unpredictable natural conditions. However, the model plant Arabidopsis thaliana and most agronomically essential crops produce visually homogenous seeds. Using automated phenotype analysis, we observed that small seeds in Arabidopsis tend to have higher primary and secondary dormancy levels than large seeds. Transcriptomic analysis revealed distinct gene expression profiles between large and small seeds. Large seeds have higher expression of translation-related genes implicated in germination competence. By contrast, small seeds have elevated expression of many positive regulators of dormancy, including a key regulator of this process, the DOG1 gene. Differences in DOG1 expression are associated with differential production of its alternative cleavage and polyadenylation isoforms; in small seeds, the proximal poly(A) site is selected, resulting in a short mRNA isoform. Furthermore, single-seed RNA sequencing analysis demonstrated that large seeds resemble DOG1 knockout mutant seeds. Finally, on the single-seed level, expression of genes affected by seed size is correlated with expression of genes that position seeds on the path toward germination. Our results demonstrate an unexpected link between seed size and dormancy phenotypes in a species that produces highly homogenous seed pools, suggesting that the correlation between seed morphology and physiology is more widespread than initially assumed.
- Keywords
- Arabidopsis, DOG1, dormancy, seed size,
- MeSH
- Arabidopsis * metabolism MeSH
- Germination genetics MeSH
- Arabidopsis Proteins * genetics metabolism MeSH
- Seeds genetics MeSH
- Plant Dormancy genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DOG1 protein, Arabidopsis MeSH Browser
- Arabidopsis Proteins * MeSH
Developing innovative agri-technologies is essential for the sustainable intensification of global food production. Seed dormancy is an adaptive trait which defines the environmental conditions in which the seed is able to germinate. Dormancy release requires sensing and integration of multiple environmental signals, a complex process which may be mimicked by seed treatment technologies. Here, we reveal molecular mechanisms by which non-thermal (cold) atmospheric gas plasma-activated water (GPAW) releases the physiological seed dormancy of Arabidopsis thaliana. GPAW triggered dormancy release by synergistic interaction between plasma-generated reactive chemical species (NO3-, H2O2, ·NO, and ·OH) and multiple signalling pathways targeting gibberellin and abscisic acid (ABA) metabolism and the expression of downstream cell wall-remodelling genes. Direct chemical action of GPAW on cell walls resulted in premature biomechanical endosperm weakening. The germination responses of dormancy signalling (nlp8, prt6, and dog1) and ABA metabolism (cyp707a2) mutants varied with GPAW composition. GPAW removes seed dormancy blocks by triggering multiple molecular signalling pathways combined with direct chemical tissue weakening to permit seed germination. Gas plasma technologies therefore improve seed quality by mimicking permissive environments in which sensing and integration of multiple signals lead to dormancy release and germination.
- Keywords
- Arabidopsis thaliana, Abscisic acid metabolism, endosperm weakening, gas plasma-activated water, nitrogen signalling, non-thermal atmospheric gas plasma technology, plant hormone signalling, reactive oxygen species, seed dormancy,
- MeSH
- Arabidopsis * metabolism MeSH
- Germination physiology MeSH
- Abscisic Acid metabolism MeSH
- Hydrogen Peroxide metabolism MeSH
- Arabidopsis Proteins * metabolism MeSH
- Gene Expression Regulation, Plant MeSH
- Seeds metabolism MeSH
- Technology MeSH
- Plant Dormancy physiology MeSH
- Water metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DOG1 protein, Arabidopsis MeSH Browser
- Abscisic Acid MeSH
- Hydrogen Peroxide MeSH
- Arabidopsis Proteins * MeSH
- Water MeSH
Molecular responses of plants to natural phytotoxins comprise more general and compound-specific mechanisms. How phytotoxic chalcones and other flavonoids inhibit seedling growth was widely studied, but how they interfere with seed germination is largely unknown. The dihydrochalcone and putative allelochemical myrigalone A (MyA) inhibits seed germination and seedling growth. Transcriptome (RNAseq) and hormone analyses of Lepidium sativum seed responses to MyA were compared to other bioactive and inactive compounds. MyA treatment of imbibed seeds triggered the phased induction of a detoxification programme, altered gibberellin, cis-(+)-12-oxophytodienoic acid and jasmonate metabolism, and affected the expression of hormone transporter genes. The MyA-mediated inhibition involved interference with the antioxidant system, oxidative signalling, aquaporins and water uptake, but not uncoupling of oxidative phosphorylation or p-hydroxyphenylpyruvate dioxygenase expression/activity. MyA specifically affected the expression of auxin-related signalling genes, and various transporter genes, including for auxin transport (PIN7, ABCG37, ABCG4, WAT1). Responses to auxin-specific inhibitors further supported the conclusion that MyA interferes with auxin homeostasis during seed germination. Comparative analysis of MyA and other phytotoxins revealed differences in the specific regulatory mechanisms and auxin transporter genes targeted to interfere with auxin homestasis. We conclude that MyA exerts its phytotoxic activity by multiple auxin-dependent and independent molecular mechanisms.
- Keywords
- ATP-binding cassette (ABC) transporter, PIN auxin efflux carrier, WRKY transcription factors, allelochemical and allelopathy, aquaporin-mediated water transport, auxin transport and homeostasis, cis-(+)-12-oxophytodienoic acid (OPDA) reductase, gibberellin metabolism, phytotoxin detoxification programme, seed germination,
- MeSH
- Chalcones MeSH
- Homeostasis MeSH
- Hormones metabolism MeSH
- Germination * genetics MeSH
- Indoleacetic Acids metabolism MeSH
- Lepidium sativum * metabolism MeSH
- Gene Expression Regulation, Plant MeSH
- Plant Growth Regulators metabolism pharmacology MeSH
- Seeds genetics MeSH
- Seedlings metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Chalcones MeSH
- Hormones MeSH
- Indoleacetic Acids MeSH
- myrigalone A MeSH Browser
- Plant Growth Regulators MeSH
The dynamic behaviour of seeds in soil seed banks depends on their ability to act as sophisticated environmental sensors to adjust their sensitivity thresholds for germination by dormancy mechanisms. Here we show that prolonged incubation of sugar beet fruits at low temperature (chilling at 5°C, generally known to release seed dormancy of many species) can induce secondary nondeep physiological dormancy of an apparently nondormant crop species. The physiological and biophysical mechanisms underpinning this cold-induced secondary dormancy include the chilling-induced accumulation of abscisic acid in the seeds, a reduction in the embryo growth potential and a block in weakening of the endosperm covering the embryonic root. Transcriptome analysis revealed distinct gene expression patterns in the different temperature regimes and upon secondary dormancy induction and maintenance. The chilling caused reduced expression of cell wall remodelling protein genes required for embryo cell elongation growth and endosperm weakening, as well as increased expression of seed maturation genes, such as for late embryogenesis abundant proteins. A model integrating the hormonal signalling and master regulator expression with the temperature-control of seed dormancy and maturation programmes is proposed. The revealed mechanisms of the cold-induced secondary dormancy are important for climate-smart agriculture and food security.
- Keywords
- coat dormancy, cold-induced dormancy, embryo growth potential, endosperm weakening, germination temperature, secondary dormancy, seed transcriptomes, sugar beet,
- MeSH
- Beta vulgaris * genetics MeSH
- Germination physiology MeSH
- Abscisic Acid metabolism MeSH
- Seeds physiology MeSH
- Plant Dormancy genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Abscisic Acid MeSH
The timing of seed germination is crucial for seed plants and is coordinated by internal and external cues, reflecting adaptations to different habitats. Physiological and molecular studies with lettuce and Arabidopsis thaliana have documented a strict requirement for light to initiate germination and identified many receptors, signaling cascades, and hormonal control elements. In contrast, seed germination in several other plants is inhibited by light, but the molecular basis of this alternative response is unknown. We describe Aethionema arabicum (Brassicaceae) as a suitable model plant to investigate the mechanism of germination inhibition by light, as this species has accessions with natural variation between light-sensitive and light-neutral responses. Inhibition of germination occurs in red, blue, or far-red light and increases with light intensity and duration. Gibberellins and abscisic acid are involved in the control of germination, as in Arabidopsis, but transcriptome comparisons of light- and dark-exposed A. arabicum seeds revealed that, upon light exposure, the expression of genes for key regulators undergo converse changes, resulting in antipodal hormone regulation. These findings illustrate that similar modular components of a pathway in light-inhibited, light-neutral, and light-requiring germination among the Brassicaceae have been assembled in the course of evolution to produce divergent pathways, likely as adaptive traits.
- Keywords
- Aethionema arabicum, light inhibition, model plant, natural variation, seed germination, transcriptional regulation,
- MeSH
- Brassicaceae physiology radiation effects MeSH
- Gene Expression radiation effects MeSH
- Gibberellins metabolism MeSH
- Germination radiation effects MeSH
- Abscisic Acid metabolism MeSH
- Genes, Plant * MeSH
- Sunlight * MeSH
- Transcriptome drug effects MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Gibberellins MeSH
- Abscisic Acid MeSH
Pectin methylesterase (PME) controls the methylesterification status of pectins and thereby determines the biophysical properties of plant cell walls, which are important for tissue growth and weakening processes. We demonstrate here that tissue-specific and spatiotemporal alterations in cell wall pectin methylesterification occur during the germination of garden cress (Lepidium sativum). These cell wall changes are associated with characteristic expression patterns of PME genes and resultant enzyme activities in the key seed compartments CAP (micropylar endosperm) and RAD (radicle plus lower hypocotyl). Transcriptome and quantitative real-time reverse transcription-polymerase chain reaction analysis as well as PME enzyme activity measurements of separated seed compartments, including CAP and RAD, revealed distinct phases during germination. These were associated with hormonal and compartment-specific regulation of PME group 1, PME group 2, and PME inhibitor transcript expression and total PME activity. The regulatory patterns indicated a role for PME activity in testa rupture (TR). Consistent with a role for cell wall pectin methylesterification in TR, treatment of seeds with PME resulted in enhanced testa permeability and promoted TR. Mathematical modeling of transcript expression changes in germinating garden cress and Arabidopsis (Arabidopsis thaliana) seeds suggested that group 2 PMEs make a major contribution to the overall PME activity rather than acting as PME inhibitors. It is concluded that regulated changes in the degree of pectin methylesterification through CAP- and RAD-specific PME and PME inhibitor expression play a crucial role during Brassicaceae seed germination.
- MeSH
- Endosperm enzymology physiology MeSH
- Hypocotyl enzymology physiology MeSH
- Carboxylic Ester Hydrolases biosynthesis genetics physiology MeSH
- Germination genetics physiology MeSH
- Real-Time Polymerase Chain Reaction MeSH
- Lepidium sativum enzymology genetics physiology MeSH
- Gene Expression Regulation, Plant genetics physiology MeSH
- Plant Proteins genetics physiology MeSH
- Seeds enzymology physiology MeSH
- Gene Expression Profiling MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Carboxylic Ester Hydrolases MeSH
- pectinesterase MeSH Browser
- Plant Proteins MeSH