The timing of germination has profound impacts on fitness, population dynamics, and species ranges. Many plants have evolved responses to seasonal environmental cues to time germination with favorable conditions; these responses interact with temporal variation in local climate to drive the seasonal climate niche and may reflect local adaptation. Here, we examined germination responses to temperature cues in Streptanthus tortuosus populations across an elevational gradient.
Methods
Using common garden experiments, we evaluated differences among populations in response to cold stratification (chilling) and germination temperature and related them to observed germination phenology in the field. We then explored how these responses relate to past climate at each site and the implications of those patterns under future climate change.
Results
Populations from high elevations had stronger stratification requirements for germination and narrower temperature ranges for germination without stratification. Differences in germination responses corresponded with elevation and variability in seasonal temperature and precipitation across populations. Further, they corresponded with germination phenology in the field; low‐elevation populations germinated in the fall without chilling, whereas high‐elevation populations germinated after winter chilling and snowmelt in spring and summer. Climate‐change forecasts indicate increasing temperatures and decreasing snowpack, which will likely alter germination cues and timing, particularly for high‐elevation populations.
Conclusions
The seasonal germination niche for S. tortuosus is highly influenced by temperature and varies across the elevational gradient. Climate change will likely affect germination timing, which may cascade to influence trait expression, fitness, and population persistence.
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Functional variants of DOG1 control seed chilling responses and variation in seasonal life-history strategies in Arabidopsis thaliana
The seasonal timing of seed germination determines a plant’s realized environmental niche, and is important for adaptation to climate. The timing of seasonal germination depends on patterns of seed dormancy release or induction by cold and interacts with flowering-time variation to construct different seasonal life histories. To characterize the genetic basis and climatic associations of natural variation in seed chilling responses and associated life-history syndromes, we selected 559 fully sequenced accessions of the model annual species Arabidopsis thaliana from across a wide climate range and scored each for seed germination across a range of 13 cold stratification treatments, as well as the timing of flowering and senescence. Germination strategies varied continuously along 2 major axes: 1) Overall germination fraction and 2) induction vs. release of dormancy by cold. Natural variation in seed responses to chilling was correlated with flowering time and senescence to create a range of seasonal life-history syndromes. Genome-wide association identified several loci associated with natural variation in seed chilling responses, including a known functional polymorphism in the self-binding domain of the candidate gene DOG1. A phylogeny of DOG1 haplotypes revealed ancient divergence of these functional variants associated with periods of Pleistocene climate change, and Gradient Forest analysis showed that allele turnover of candidate SNPs was significantly associated with climate gradients. These results provide evidence that A. thaliana ’s germination niche and correlated life-history syndromes are shaped by past climate cycles, as well as local adaptation to contemporary climate.
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- PAR ID:
- 10134000
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 117
- Issue:
- 5
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- 2526 to 2534
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Premise The timing of germination has profound impacts on fitness, population dynamics, and species ranges. Many plants have evolved responses to seasonal environmental cues to time germination with favorable conditions; these responses interact with temporal variation in local climate to drive the seasonal climate niche and may reflect local adaptation. Here, we examined germination responses to temperature cues in
Streptanthus tortuosus populations across an elevational gradient.Methods Using common garden experiments, we evaluated differences among populations in response to cold stratification (chilling) and germination temperature and related them to observed germination phenology in the field. We then explored how these responses relate to past climate at each site and the implications of those patterns under future climate change.
Results Populations from high elevations had stronger stratification requirements for germination and narrower temperature ranges for germination without stratification. Differences in germination responses corresponded with elevation and variability in seasonal temperature and precipitation across populations. Further, they corresponded with germination phenology in the field; low‐elevation populations germinated in the fall without chilling, whereas high‐elevation populations germinated after winter chilling and snowmelt in spring and summer. Climate‐change forecasts indicate increasing temperatures and decreasing snowpack, which will likely alter germination cues and timing, particularly for high‐elevation populations.
Conclusions The seasonal germination niche for
S. tortuosus is highly influenced by temperature and varies across the elevational gradient. Climate change will likely affect germination timing, which may cascade to influence trait expression, fitness, and population persistence. -
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Abstract In Mediterranean climates, the timing of seasonal rains determines germination, flowering phenology and fitness. As climate change alters seasonal precipitation patterns, it is important to ask how these changes will affect the phenology and fitness of plant populations. We addressed this question experimentally with the annual plant species
Arabidopsis thaliana .In a first experiment, we manipulated the date of rainfall onset and recorded germination phenology on sand and soil substrates. In a second experiment, we manipulated germination date, growing season length and mid‐season drought to measure their effects on flowering time and fitness. Within each experiment, we manipulated seed dormancy and flowering time using multilocus near‐isogenic lines segregating strong and weak alleles of the seed dormancy gene
DOG1 and the flowering time geneFRI . We synthesized germination phenology data from the first experiment with fitness functions from the second experiment to project population fitness under different seasonal rainfall scenarios.Germination phenology tracked rainfall onset but was slower and more variable on sand than on soil. Many seeds dispersed on sand in spring and summer delayed germination until the cooler temperatures of autumn. The high‐dormancy
DOG1 allele also prevented immediate germination in spring and summer. Germination timing strongly affected plant fitness. Fecundity was highest in the October germination cohort and declined in spring germinants. The late floweringFRI allele had lower fecundity, especially in early fall and spring cohorts. Projections of population fitness revealed that: (1) Later onset of autumn rains will negatively affect population fitness. (2) Slow, variable germination on sand buffers populations against fitness impacts of variable spring and summer rainfall. (3) Seasonal selection favours high dormancy and early flowering genotypes in a Mediterranean climate with hot dry summers. The high‐dormancyDOG1 allele delayed germination of spring‐dispersed fresh seeds until more favourable early fall conditions, resulting in higher projected population fitness.These findings suggest that Mediterranean annual plant populations are vulnerable to changes in seasonal precipitation, especially in California where rainfall onset is already occurring later. The fitness advantage of highly dormant, early flowering genotypes helps explain the prevalence of this strategy in Mediterranean populations.
Read the free
Plain Language Summary for this article on the Journal blog. -
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Abstract 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 HTT assumptions 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. θHTis 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 θHTand 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.
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Abstract The seasonal timing of life history transitions is often critical to fitness, and many organisms rely upon environmental cues to match life cycle events with favorable conditions. In plants, the timing of seed germination is mediated by seasonal cues such as rainfall and temperature. Variation in cue responses among species can reflect evolutionary processes and adaptation to local climate and can affect vulnerability to changing conditions. Indeed, climate change is altering the timing of precipitation, and germination responses to such change can have consequences for individual fitness, population dynamics, and species distributions. Here, we assessed responses to the seasonal timing of germination‐triggering rains for eleven species spanning the
Streptanthus /Caulanthus clade (Brassicaceae). To do so, we experimentally manipulated the onset date of rainfall events, measured effects on germination fraction, and evaluated whether responses were constrained by evolutionary relationships across the phylogeny. We then explored the possible consequences of these responses to contemporary shifts in precipitation timing. Germination fractions decreased with later onset of rains and cooler temperatures for all but threeCaulanthus species. Species' germination responses to the timing of rainfall and seasonal temperatures were phylogenetically constrained, withCaulanthus species appearing less responsive. Further, four species are likely already experiencing significant decreases in germination fractions with observed climate change, which has shifted the timing of rainfall towards the cooler, winter months in California. Overall, our findings emphasize the sensitivity of germination to seasonal conditions, underscore the importance of interacting environmental cues, and highlight vulnerability to shifting precipitation patterns with climate change, particularly in more northern, mesic species.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.1912451117
