To germinate or not to germinate : a question of dormancy relief not germination stimulation

A common understanding of the control of germination through dormancy is essential for effective communication between seed scientists whether they are ecologists, physiologists or molecular biologists. Vleeshouwers et al. (1995) realized that barriers between disciplines limited progress and through insightful conclusions in their paper ‘Redefining seed dormancy: an attempt to integrate physiology and ecology’, they did much to overcome these barriers at that time. However, times move on, understanding develops, and now there is a case for ‘Redefining seed dormancy as an integration of physiology, ecology and molecular biology’. Finch-Savage and Leubner-Metzger (2006) had this in mind when they extended and re-interpreted the definition of dormancy proposed by Vleeshouwers et al. (1995), by considering dormancy as a having a number of layers that must be removed, with the final layer of dormancy being synonymous with the stimulation/induction of germination

A laboratory simulation of Arabidopsis seed dormancy cycling provides new insight into its regulation by clock genes and the dormancy-related genes DOG1 , MFT , CIPK23 and PHYA

Environmental signals drive seed dormancy cycling in the soil to synchronise germination with the optimal time of year; a process essential for species fitness and survival. Previous correlation of transcription profiles in exhumed seeds with annual environmental signals revealed the coordination of dormancy regulating mechanisms with the soil environment. Here, we developed a rapid and robust laboratory dormancy cycling simulation. The utility of this simulation was tested in two ways. Firstly using mutants in known dormancy-related genes (DELAY OF GERMINATION 1 (DOG1), MOTHER OF FLOWERING TIME (MFT), CBL-INTERACTING PROTEIN KINASE 23 (CIPK23) and PHYTOCHROME A (PHYA)). Secondly, using further mutants we test the hypothesis that components of the circadian clock are involved in coordination of the annual seed dormancy cycle. The rate of dormancy induction and relief differed in all lines tested. In the mutants, dog1-2 and mft2, dormancy induction was reduced but not absent. DOG1 is not absolutely required for dormancy. In cipk23 and phyA dormancy induction was accelerated. Involvement of the clock in dormancy cycling was clear when mutants in the morning and evening loops of the clock were compared. Dormancy induction was faster when the morning loop was compromised and delayed when the evening loop was compromised

Environment sensing in spring-dispersed seeds of a winter annual Arabidopsis influences the regulation of dormancy to align germination potential with seasonal changes

Seed dormancy cycling plays a crucial role in the lifecycle timing of many plants. Little is known of how the seeds respond to the soil seed bank environment following dispersal in spring into the short-term seed bank before seedling emergence in autumn. Seeds of the winter annual Arabidopsis ecotype Cvi were buried in field soils in spring and recovered monthly until autumn and their molecular eco-physiological responses were recorded. DOG1 expression is initially low and then increases as dormancy increases. MFT expression is negatively correlated with germination potential. Abscisic acid (ABA) and gibberellin (GA) signalling responds rapidly following burial and adjusts to the seasonal change in soil temperature. Collectively these changes align germination potential with the optimum climate space for seedling emergence. Seeds naturally dispersed to the soil in spring enter a shallow dormancy cycle dominated by spatial sensing that adjusts germination potential to the maximum when soil environment is most favourable for germination and seedling emergence upon soil disturbance. This behaviour differs subtly from that of seeds overwintered in the soil seed bank to spread the period of potential germination in the seed population (existing seed bank and newly dispersed). As soil temperature declines in autumn, deep dormancy is re-imposed as seeds become part of the persistent seed bank

Seed dormancy cycling and the regulation of dormancy mechanisms to time germination in variable field environments

Many molecular mechanisms that regulate dormancy have been identified individually in controlled laboratory studies. However, little is known about how the seed employs this complex suite of mechanisms during dormancy cycling in the variable environment of the soil seed bank. Nevertheless, this behavior is essential to ensure germination takes place in a favourable habitat and climate space, and in the correct season for the resulting plant to complete its life cycle. During their time in the soil seed bank seeds continually adjust their dormancy status by sensing a range of environmental signals. Those related to slow seasonal change (e.g. temperature) are used for temporal sensing to determine the time of year and depth of dormancy. This alters their sensitivity to signals related to their spatial environment (e.g. light, nitrate, water potential) that indicate conditions are suitable for germination, and so trigger the termination of dormancy. We review work on the physiological, molecular and ecological aspects of seed dormancy in Arabidopsis and interpret it in the context of dormancy cycling in the soil seed bank. This approach has provided new insight into the coordination of mechanisms and signaling networks and the multidimensional sensing that regulates dormancy cycling in a variable environment

Seed Dormancy in Red Rice (Oryza Sativa): Changes in Embryo pH and Metabolism During the Dormancy-Breaking Process.

Hydrated, dehulled, dormant seeds of red rice (Oryza sativa L.) were exposed to chemical treatments (nitrite, propionic acid, methyl propionate, propionaldehyde, and n-propanol) that saturate the dormancy-breaking response. Dormancy-breaking chemicals were (a) metabolized (n-propanol and propionate) by embryos in dormant seeds to weak acids; (b) decreased embryo pH; and (c) increased embryo (Fru 2,6-P\sb2) prior to dormancy-breaking. Embryo acidification, but not increased embryo (Fru 2,6-P\sb2), was associated with the chemical contact interval required for the onset of dormancy-breaking. During chemical contact, embryo (Fru 2,6-P\sb2) increased independent of dormancy-breaking and was inversely correlated with the elapsed time to 30% germination. On subsequent transfer to H\sb2O, further embryo acidification and increased embryo (Fru 2,6-P\sb2) were significantly correlated with visible germination irrespective of the dormancy-breaking chemical employed. These data suggest that dormancy-breaking chemicals lacking a dissociable proton are metabolized to weak acids, leading to embryo acidification that results in dormancy-breaking; increased embryo (Fru 2,6-P\sb2) is related to the subsequent germination rate. Embryo acidification may be analogous to that associated with the termination of developmental arrest in other multicellular systems (Brine shrimp and nematodes). In hydrating dormant and nondormant seeds, seed respiration, embryo pH and (Fru 2,6-P\sb2) were similar. In phase 2, these parameters diverge as nondormant seeds enter the germination phase. In dormant seeds, embryo (Fru 2,6-P\sb2) was transient in phase 2 suggesting the imposition of a block on the germination phase

Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling resulting in winter and summer annual phenotypes

Seeds use environmental cues to sense the seasons and their surroundings to initiate the plants life cycle. Dormancy cycling underlying this process is extensively described, but the molecular mechanism is largely unknown. To address this we selected a range of representative genes from published array experiments in the laboratory and investigated their expression patterns in seeds of Arabidopsis ecotypes, having contrasting life cycles, over an annual dormancy cycle in the field. We show how mechanisms identified in the laboratory are coordinated in response to the soil environment to determine dormancy cycles that result in winter and summer annual phenotypes. Our results are consistent with a seed specific response to seasonal temperature patterns (temporal sensing) involving the gene DELAY OF GERMINATION1 (DOG1) that indicates the correct season; and concurrent temporally driven co-opted mechanisms that sense spatial signals i.e. nitrate via CBL-INTERACTING PROTEIN KINASE 23 (CIPK23) phosphorylation of the NITRATE TRANSPORTER 1 (NRT1.1) and light via PHYTOCHROME A (PHYA). In both ecotypes studied, when all three genes have low expression there is enhanced GIBBERELLIN 3 BETA-HYDROXYLASE 1 (GA3ox1) expression, exhumed seeds have the potential to germinate in the laboratory, and the initiation of seedling emergence occurs following soil disturbance (exposure to light) in the field. Unlike DOG1, expression of MOTHER of FLOWERING TIME (MFT) has an opposite thermal response in seeds of the two ecotypes indicating a role in determining their different dormancy cycling phenotypes

Changes in phenological events in response to a global warming scenario reveal greater adaptability of winter annual compared to summer annual Arabidopsis ecotypes

Background and Aims The impact of global warming on life cycle timing is uncertain. We investigated changes in life cycle timing in a global warming scenario. We compared Arabidopsis thaliana ecotypes adapted to the warm/dry Cape Verdi Islands (Cvi), Macaronesia, and the cool/wet climate of the Burren (Bur), Ireland, Northern Europe. These are obligate winter and summer annuals respectively. Methods Using a global warming scenario predicting a 4°C temperature rise from 2011 to circa 2080 we produced F1 seeds at each end of a thermogradient tunnel. Each F1 cohort (cool and warm) then produced F2 seeds at both ends of the thermal gradient in winter and summer annual life cycles. F2 seeds from the winter life cycle were buried at three positions along the gradient to determine the impact of temperature on seedling emergence in a simulated winter life cycle. Key Results In a winter life cycle, increasing temperatures advanced flowering time by 10.1 days °C-1 in the winter annual and 4.9 days °C-1 in the summer annual. Plant size and seed yield responded positively to global warming in both ecotypes. In a winter life cycle, the impact of increasing temperature on seedling emergence timing was positive in the winter annual, but negative in the summer annual. Global warming reduced summer annual plant size and seed yield in a summer life cycle. Conclusions Seedling emergence timing observed in the north European summer annual ecotype may exacerbate the negative impact of predicted increased spring and summer temperatures on their establishment and reproductive performance. In contrast, seedling establishment of the Macaronesian winter annual may benefit from higher soil temperatures that will delay emergence until autumn, but which also facilitates earlier spring flowering and consequent avoidance of high summer temperatures. Such plasticity gives winter annual Arabidopsis ecotypes a distinct advantage over summer annuals in expected global warming scenarios. This highlights the importance of variation in the timing of seedling establishment in understanding plant species responses to Anthropogenic Climate Change

Predicted global warming scenarios impact on the mother plant to alter seed dormancy and germination behaviour in Arabidopsis

Seed characteristics are key components of plant fitness that are influenced by temperature in their maternal environment, and temperature will change with global warming. To study the effect of such temperature changes, Arabidopsis thaliana plants were grown to produce seeds along a uniquely designed polyethylene tunnel having a thermal gradient reflecting local global warming predictions. Plants therefore experienced the same variations in temperature and light conditions but different mean temperatures. A range of seed-related plant fitness estimates were measured. There were dramatic non-linear temperature effects on the germination behaviour in two contrasting ecotypes. Maternal temperatures lower than 15–16 °C resulted in significantly greater primary dormancy. In addition, the impact of nitrate in the growing media on dormancy was shown only by seeds produced below 15–16 °C. However, there were no consistent effects on seed yield, number, or size. Effects on germination behaviour were shown to be a species characteristic responding to temperature and not time of year. Elevating temperature above this critical value during seed development has the potential to dramatically alter the timing of subsequent seed germination and the proportion entering the soil seed bank. This has potential consequences for the whole plant life cycle and species fitness

Seed dormancy cycling in Arabidopsis : chromatin remodelling and regulation of DOG1 in response to seasonal environmental signals

The involvement of chromatin remodelling in dormancy cycling in the soil seed bank (SSB) is poorly understood. Natural variation between the winter and summer annual Arabidopsis ecotypes Cvi and Bur was exploited to investigate the expression of genes involved in chromatin remodelling via histone 2B (H2B) ubiquitination/de-ubiquitination and histone acetylation/deacetylation, the repressive histone methyl transferases CURLY LEAF (CLF) and SWINGER (SWN), and the gene silencing repressor ROS1 (REPRESSOR OF SILENCING1) and promoter of silencing KYP/SUVH4 (KRYPTONITE), during dormancy cycling in the SSB. ROS1 expression was positively correlated with dormancy while the reverse was observed for CLF and KYP/SUVH4. We propose ROS1 dependent repression of silencing and a sequential requirement of CLF and KYP/SUVH4 dependent gene repression and silencing for the maintenance and suppression of dormancy during dormancy cycling. Seasonal expression of H2B modifying genes was correlated negatively with temperature and positively with DOG1 expression, as were histone acetyltransferase genes, with histone deacetylases positively correlated with temperature. Changes in the histone marks H3K4me3 and H3K27me3 were seen on DOG1 (DELAY OF GERMINATION1) in Cvi during dormancy cycling. H3K4me3 activating marks remained stable along DOG1. During relief of dormancy, H3K27me3 repressive marks slowly accumulated and accelerated on exposure to light completing dormancy loss. We propose that these marks on DOG1 serve as a thermal sensing mechanism during dormancy cycling in preparation for light repression of dormancy. Overall, chromatin remodelling plays a vital role in temporal sensing through regulation of gene expression

Aquaporins influence seed dormancy and germination in response to stress

Aquaporins influence water flow in plants, yet little is known of their involvement in the water‐driven process of seed germination. We therefore investigated their role in seeds in the laboratory and under field and global warming conditions. We mapped the expression of tonoplast intrinsic proteins (TIPs) during dormancy cycling and during germination under normal and water stress conditions. We found that the two key tonoplast aquaporins, TIP3;1 and TIP3;2, which have previously been implicated in water or solute transport, respectively, act antagonistically to modulate the response to abscisic acid, with TIP3;1 being a positive and TIP3;2 a negative regulator. A third isoform, TIP4;1, which is normally expressed upon completion of germination, was found to play an earlier role during water stress. Seed TIPs also contribute to the regulation of depth of primary dormancy and differences in the induction of secondary dormancy during dormancy cycling. Protein and gene expression during annual cycling under field conditions and a global warming scenario further illustrate this role. We propose that the different responses of the seed TIP contribute to mechanisms that influence dormancy status and the timing of germination under variable soil conditions