Seed germination and flowering, two critical developmental transitions in plant life cycles, are coordinately regulated by genetic and environmental factors to match plant establishment and ...reproduction to seasonal cues. The DELAY OF GERMINATION1 (DOG1) gene is involved in regulating seed dormancy in response to temperature and has also been associated genetically with pleiotropic flowering phenotypes across diverse Arabidopsis thaliana accessions and locations. Here we show that DOG1 can regulate seed dormancy and flowering times in lettuce (Lactuca sativa, Ls) and Arabidopsis through an influence on levels of microRNAs (miRNAs) miR156 and miR172. In lettuce, suppression of LsDOG1 expression enabled seed germination at high temperature and promoted early flowering in association with reduced miR156 and increased miR172 levels. In Arabidopsis, higher miR156 levels resulting from overexpression of the MIR156 gene enhanced seed dormancy and delayed flowering. These phenotypic effects, as well as conversion of MIR156 transcripts to miR156, were compromised in DOG1 loss-of-function mutant plants, especially in seeds. Overexpression of MIR172 reduced seed dormancy and promoted early flowering in Arabidopsis, and the effect on flowering required functional DOG1. Transcript levels of several genes associated with miRNA processing were consistently lower in dry seeds of Arabidopsis and lettuce when DOG1 was mutated or its expression was reduced; in contrast, transcript levels of these geneswere elevated in a DOG1 gain-of-function mutant. Our results reveal a previously unknown linkage between two critical developmental phase transitions in the plant life cycle through a DOG1–miR156–miR172 interaction.
In the coming decades, maintaining a steady food supply for the increasing world population will require high-yielding crop plants which can be productive under increasingly variable conditions. ...Maintaining high yields will require the successful and uniform establishment of plants in the field under altered environmental conditions. Seed vigor, a complex agronomic trait that includes seed longevity, germination speed, seedling growth, and early stress tolerance, determines the duration and success of this establishment period. Elevated temperature during early seed development can decrease seed size, number, and fertility, delay germination and reduce seed vigor in crops such as cereals, legumes, and vegetable crops. Heat stress in mature seeds can reduce seed vigor in crops such as lettuce, oat, and chickpea. Warming trends and increasing temperature variability can increase seed dormancy and reduce germination rates, especially in crops that require lower temperatures for germination and seedling establishment. To improve seed germination speed and success, much research has focused on selecting quality seeds for replanting, priming seeds before sowing, and breeding varieties with improved seed performance. Recent strides in understanding the genetic basis of variation in seed vigor have used genomics and transcriptomics to identify candidate genes for improving germination, and several studies have explored the potential impact of climate change on the percentage and timing of germination. In this review, we discuss these recent advances in the genetic underpinnings of seed performance as well as how climate change is expected to affect vigor in current varieties of staple, vegetable, and other crops.
Even as increasing populations put pressure on food supplies, about one-third of the total food produced for human consumption is wasted, with the majority of loss in developing countries occurring ...between harvest and the consumer. Controlling product dryness is the most critical factor for maintaining quality in stored non-perishable foods. The high relative humidity prevalent in humid climates elevates the moisture content of dried commodities stored in porous woven bags, enabling fungal and insect infestations. Mycotoxins (e.g., aflatoxin) produced by fungi in insufficiently dried food commodities affect 4.5 billion people worldwide.
We introduce the term “dry chain” to describe initial dehydration of durable commodities to levels preventing fungal growth followed by storage in moisture-proof containers. This is analogous to the “cold chain” in which continuous refrigeration is used to preserve quality in the fresh produce industry. However, in the case of the dry chain, no further equipment or energy input is required to maintain product quality after initial drying as long as the integrity of the storage container is preserved. In some locations/seasons, only packaging is required to implement a “climate smart” dry chain, while in humid conditions, additional drying is required and desiccant-based drying methods have unique advantages.
We propose both climate-based and drying-based approaches to implement the dry chain to minimize mycotoxin accumulation and insect infestations in dry products, reduce food loss, improve food quality, safety and security, and protect public health.
•One-third of food produced in developing countries is lost before consumption.•High moisture contents in storage promote spoilage and production of mycotoxins.•We propose the “dry chain”: initial drying with storage in water-proof containers.•New drying and storage technologies make implementation of the dry chain feasible.•The dry chain would empower farmers, reduce food loss and improve public health.
Seeds offer a unique perspective from which to view biology. An individual seed is an autonomous biological entity that must rely on its own resources (and resourcefulness) to persist after dispersal ...and to time its transition to germination and seedling growth to coincide with environmental opportunities for survival. At the same time, seed biology in agriculture and ecology is determined largely by the behaviours of populations of individual seeds. The percentage of seeds in a population that is in a particular state (e.g. dormant, germinated, dead) at a given time is a fundamental metric of seed biology. This duality of individual diversity underlying consistent population-wide behaviour patterns can be described quantitatively using population-based threshold (PBT) models. While conceptually simple, these models are highly flexible and can describe the wide diversity of responses of seed populations to temperature, water potential, hormones, oxygen, light, ageing and combinations of these factors. This seed behaviour is linked to respiratory rates of individual seeds, indicating that basic metabolic processes within seeds vary among individuals in accordance with PBT principles. Looking more broadly across microbial, plant and animal biology, examples of cellular diversity in hormonal sensitivity, gene expression, developmental responses and signalling abound. This variation often is termed ‘noise’, and analysis efforts are focused on extracting mean signals from this variation to understand regulatory pathways. However, extension of the PBT approach to the cellular and molecular levels suggests that population sensitivity distributions and recruitment phenomena may underlie many fundamental biological processes. Thus, concepts and quantitative approaches developed for the analysis of seed populations can be applied across biological scales from molecules to ecosystems to interpret inherent biological variation and provide mechanistic insights into the nature of biological regulatory systems.
Plant germination ecology involves continuous interactions between changing environmental conditions and the sensitivity of seed populations to respond to those conditions at a given time. ...Ecologically meaningful parameters characterizing germination capacity (or dormancy) are needed to advance our understanding of the evolution of germination strategies within plant communities. The germination traits commonly examined (e.g., maximum germination percentage under optimal conditions) may not adequately reflect the critical ecological differences in germination behavior across species, communities, and seasons. In particular, most seeds exhibit primary dormancy at dispersal that is alleviated by exposure to dry after-ripening or to hydrated chilling to enable germination in a subsequent favorable season. Population-based threshold (PBT) models of seed germination enable quantification of patterns of germination timing using parameters based on mechanistic assumptions about the underlying germination physiology. We applied the hydrothermal time (HTT) model, a type of PBT model that integrates environmental temperature and water availability, to study germination physiology in a guild of coexisting desert annual species whose seeds were after-ripened by dry storage under different conditions. We show that HTTassumptions are valid for describing germination physiology in these species, including loss of dormancy during after-ripening. Key HTT parameters, the hydrothermal time constant (θHT) and base water potential distribution among seeds (Ψb(g)), were effective in describing changes in dormancy states and in clustering species exhibiting similar germination syndromes. θHT is an inherent species-specific trait relating to timing of germination that correlates well with long-term field germination fraction, while Ψb(g) shifts with depth of dormancy in response to after-ripening and seasonal environmental variation. Predictions based on variation among coexisting species in θHT and Ψb(g) in laboratory germination tests matched well with 25-yr observations of germination dates and fractions for the same species in natural field conditions. Seed dormancy and germination strategies, which are significant contributors to long-term species demographics under natural conditions, can be represented by readily measurable functional traits underlying variation in germination phenologies.
Early life‐cycle events play critical roles in determining the population and community dynamics of plants. The ecology of seeds and their germination patterns can determine range limits, adaptation ...to environmental variation, species diversity, and community responses to climate change. Understanding the adaptive consequences and environmental filtering of such functional traits will allow us to explain and predict ecological dynamics. Here we quantify key functional aspects of germination physiology and relate them to an existing functional ecology framework to explain long‐term population dynamics for 13 species of desert annuals near Tucson, Arizona, USA. Our goal was to assess the extent to which germination functional biology contributes to long‐term population processes in nature. Some of the species differences in base, optimum, and maximum temperatures for germination, thermal times to germination, and base water potentials for germination were strongly related to 20‐yr mean germination fractions, 25‐yr average germination dates, seed size, and long‐term demographic variation. Comparisons of germination fraction, survival, and fecundity vs. yearly changes in population size found significant roles for all three factors, although in varying proportions for different species. Relationships between species’ germination physiologies and relative germination fractions varied across years, with fast‐germinating species being favored in years with warm temperatures during rainfall events in the germination season. Species with low germination fractions and high demographic variance have low integrated water‐use efficiency, higher vegetative growth rates, and smaller, slower‐germinating seeds. We have identified and quantified a number of functional traits associated with germination biology that play critical roles in ecological population dynamics.
Seed germination is responsive to diverse environmental, hormonal and chemical signals. Germination rates (i.e. speed and distribution in time) reveal information about timing, uniformity and extent ...of germination in seed populations and are sensitive indicators of seed vigour and stress tolerance. Population-based threshold (PBT) models have been applied to describe germination responses to temperature, water potential, hormones, ageing and oxygen. However, obtaining detailed data on germination rates of seed populations requires repeated observations at frequent times to construct germination time courses, which is labour intensive and often impractical. Recently, instruments have been developed to measure repeatedly the respiration (oxygen consumption) of individual seeds following imbibition, providing complete respiratory time courses for populations of individual seeds in an automated manner. In this study, we demonstrate a new approach that enables the use of single-seed respiratory data, rather than germination data, to characterize the responses of seed populations to diverse conditions. We applied PBT models to single-seed respiratory data and compared the results to similar analyses of germination time courses. We found consistent and quantitatively comparable relationships between seed respiratory and germination patterns in response to temperature, water potential, abscisic acid, gibberellin, respiratory inhibitors, ageing and priming. This close correspondence between seed respiration and germination time courses enables the use of semi-automated respiratory measurements to assess seed vigour and quality parameters. It also raises intriguing questions about the fundamental relationship between the respiratory capacities of seeds and the rates at which they proceed toward completion of germination.
Key message
Bet-hedging is a complex evolutionary strategy involving morphological, eco-physiological, (epi)genetic and population dynamics aspects. We review these aspects in flowering plants and ...propose further research needed for this topic.
Bet-hedging is an evolutionary strategy that reduces the temporal variance in fitness at the expense of a lowered arithmetic mean fitness. It has evolved in organisms subjected to variable cues from the external environment, be they abiotic or biotic stresses such as irregular rainfall or predation. In flowering plants, bet-hedging is exhibited by hundreds of species and is mainly exerted by reproductive organs, in particular seeds but also embryos and fruits. The main example of bet-hedging in angiosperms is diaspore heteromorphism in which the same individual produces different seed/fruit morphs in terms of morphology, dormancy, eco-physiology and/or tolerance to biotic and abiotic stresses in order to ‘hedge its bets’ in unpredictable environments. The objective of this review is to provide a comprehensive overview of the ecological, genetic, epigenetic and physiological aspects involved in shaping bet-hedging strategies, and how these can affect population dynamics. We identify several open research questions about bet-hedging strategies in plants: 1) understanding ecological trade-offs among different traits; 2) producing more comprehensive phylogenetic analyses to understand the diffusion and evolutionary implications of this strategy; 3) clarifying epigenetic mechanisms related to bet-hedging and plant responses to environmental cues; and 4) applying multi-omics approaches to study bet-hedging at different levels of detail. Clarifying those aspects of bet-hedging will deepen our understanding of this fascinating evolutionary strategy.
CRISPR/Cas9 is a transformative tool for making targeted genetic alterations. In plants, high mutation efficiencies have been reported in primary transformants. However, many of the mutations ...analyzed were somatic and therefore not heritable. To provide more insights into the efficiency of creating stable homozygous mutants using CRISPR/Cas9, we targeted
(
, a gene conditioning thermoinhibition of seed germination in lettuce. Three constructs, each capable of expressing Cas9 and a single gRNA targeting different sites in
, were stably transformed into lettuce (Lactuca sativa) cvs. Salinas and Cobham Green. Analysis of 47 primary transformants (T
) and 368 T
plants by deep amplicon sequencing revealed that 57% of T
plants contained events at the target site: 28% of plants had germline mutations in one allele indicative of an early editing event (mono-allelic), 8% of plants had germline mutations in both alleles indicative of two early editing events (bi-allelic), and the remaining 21% of plants had multiple low frequency mutations indicative of late events (chimeric plants). Editing efficiency was similar in both genotypes, while the different gRNAs varied in efficiency. Amplicon sequencing of 20 T
and more than 100 T
plants for each of the three gRNAs showed that repair outcomes were not random, but reproducible and characteristic for each gRNA. Knockouts of
resulted in large increases in the maximum temperature for seed germination, with seeds of both cultivars capable of germinating >70% at 37°. Knockouts of
provide a whole-plant selectable phenotype that has minimal pleiotropic consequences. Targeting
in a co-editing strategy could therefore be used to enrich for germline-edited events simply by germinating seeds at high temperature.
Thermoinhibition, or failure of seeds to germinate at warm temperatures, is common in lettuce (Lactuca sativa) cultivars. Using a recombinant inbred line population developed from a lettuce cultivar ...(Salinas) and thermotolerant Lactuca serriola accession UC96US23 (UC), we previously mapped a quantitative trait locus associated with thermoinhibition of germination to a genomic region containing a gene encoding a key regulated enzyme in abscisic acid (ABA) biosynthesis, 9-cis-EPOXYCAROTENOID DIOXYGENASE4 (NCED4). NCED4 from either Salinas or UC complements seeds of the Arabidopsis thaliana nced6-1 nced9-1 double mutant by restoring germination thermosensitivity, indicating that both NCED4 genes encode functional proteins. Transgenic expression of Salinas NCED4 in UC seeds resulted in thermoinhibition, whereas silencing of NCED4 in Salinas seeds led to loss of thermoinhibition. Mutations in NCED4 also alleviated thermoinhibition. NCED4 expression was elevated during late seed development but was not required for seed maturation. Heat but not water stress elevated NCED4 expression in leaves, while NCED2 and NCED3 exhibited the opposite responses. Silencing of NCED4 altered the expression of genes involved in ABA, gibberellin, and ethylene biosynthesis and signaling pathways. Together, these data demonstrate that NCED4 expression is required for thermoinhibition of lettuce seeds and that it may play additional roles in plant responses to elevated temperature.
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