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

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 vigour and crop establishment : extending performance beyond adaptation

Seeds are central to crop production, human nutrition, and food security. A key component of the performance of crop seeds is the complex trait of seed vigour. Crop yield and resource use efficiency depend on successful plant establishment in the field, and it is the vigour of seeds that defines their ability to germinate and establish seedlings rapidly, uniformly, and robustly across diverse environmental conditions. Improving vigour to enhance the critical and yield-defining stage of crop establishment remains a primary objective of the agricultural industry and the seed/breeding companies that support it. Our knowledge of the regulation of seed germination has developed greatly in recent times, yet understanding of the basis of variation in vigour and therefore seed performance during the establishment of crops remains limited. Here we consider seed vigour at an ecophysiological, molecular, and biomechanical level. We discuss how some seed characteristics that serve as adaptive responses to the natural environment are not suitable for agriculture. Past domestication has provided incremental improvements, but further actively directed change is required to produce seeds with the characteristics required both now and in the future. We discuss ways in which basic plant science could be applied to enhance seed performance in crop production

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

Trait to gene analysis reveals that allelic variation in three genes determines seed vigour

Predictable seedling establishment is essential for resource-efficient and cost-effective crop production; it is widely accepted as a critically important trait determining yield and profitability. Seed vigour is essential to this, but its genetic basis is not understood. We used natural variation and fine mapping in the crop Brassica oleracea to show that allelic variation at three loci influence the key vigour trait of rapid germination. Functional analysis in both B. oleracea and the model Arabidopsis identified and demonstrated activity of genes at these loci. Two candidate genes were identified at the principal Speed of Germination QTL (SOG1) in B. oleracea. One gene BoLCVIG2 is a homologue of the alternative-splicing regulator (AtPTB1). The other gene BoLCVIG1 was unknown, but different alleles had different splice forms that were coincident with altered abscisic acid (ABA) sensitivity. We identified a further QTL, Reduced ABscisic Acid 1 (RABA1) that influenced ABA content and provide evidence that this results from the activity of a homologue of the ABA catabolic gene AtCYP707A2 at this locus. Lines containing beneficial alleles of these three genes had greater seed vigour. We propose a mechanism in which both seed ABA content and sensitivity to it determines speed of germination

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

Regulation of seed germination in the close Arabidopsis relative Lepidium sativum : a global tissue-specific transcript analysis

The completion of germination in Lepidium sativum and other endospermic seeds (e.g. Arabidopsis [Arabidopsis thaliana]) is regulated by two opposing forces, the growth potential of the radicle (RAD) and the resistance to this growth from the micropylar endosperm cap (CAP) surrounding it. We show by puncture force measurement that the CAP progressively weakens during germination, and we have conducted a time-course transcript analysis of RAD and CAP tissues throughout this process. We have also used specific inhibitors to investigate the importance of transcription, translation, and posttranslation levels of regulation of endosperm weakening in isolated CAPs. Although the impact of inhibiting translation is greater, both transcription and translation are required for the completion of endosperm weakening in the whole seed population. The majority of genes expressed during this process occur in both tissues, but where they are uniquely expressed, or significantly differentially expressed between tissues, this relates to the functions of the RAD as growing tissue and the CAP as a regulator of germination through weakening. More detailed analysis showed that putative orthologs of cell wall-remodeling genes are expressed in a complex manner during CAP weakening, suggesting distinct roles in the RAD and CAP. Expression patterns are also consistent with the CAP being a receptor for environmental signals influencing germination. Inhibitors of the aspartic, serine, and cysteine proteases reduced the number of isolated CAPs in which weakening developed, and inhibition of the 26S proteasome resulted in its complete cessation. This indicates that targeted protein degradation is a major control point for endosperm weakening

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