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Global change factors impact flowering time in natural and selected Arabidopsis genotypes
Henderson-Carter, Aleah L
Henderson-Carter, Aleah L
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Abstract
AbstractA critical aim in the ecology and evolutionary biology field is to better understand the mechanisms driving changes in plant phenology events. Plant phenology is the study of life cycle changes, such as leaf-out and flowering time, and their fundamental role in terrestrial ecosystems. Flowering time is an important phenology event because changes in the timing of the transition from the vegetative to reproductive phase can impact development, plant-pollinator interactions, fruiting, and seed-set. Over the last several decades, plant biologists have been investigating the effects of anthropogenic global change on flowering time. Classic hallmarks of anthropogenic global change have included rising global temperatures, loss in biodiversity, land-use change, and rising atmospheric CO2 concentrations, hereafter [CO2]. Ecological, physiological, and molecular flowering time dynamics are directly affected by rising [CO2]. The immediate effects of rising [CO2] on physiological and ecosystem functioning have been explored; however, the molecular mechanisms driving flowering time shifts in response to rising [CO2] remain unclear.Since the onset of the Industrial Revolution, current CO2 levels have risen from 280 ppm to just over 400 ppm. It’s important to note that over the last 400,000 years, atmospheric carbon dioxide concentrations averaged around 280 ppm; therefore, modern-day plants are already experiencing climate conditions and CO2 levels (~ 67% higher) much different than what they evolved under. Also, according to the 2013 Intergovernmental Panel on Climate Change (IPCC) report, concentrations are expected to reach between 700 ppm and 900 ppm by the year 2100. If these projections hold, under the assumption that international course-correction efforts fail, plant life, especially for C3 photosynthetic pathway species, may not maintain physiological and developmental processes in this high [CO2] world.Flowering time is affected by external cues like daylength, light quality, water availability, temperature as well as endogenous cues such as carbohydrate status. Plants integrate external and endogenous cues to determine the most favorable conditions to initiate flowering, usually coordinating with spring and summer conditions. Given that seasonal changes are primarily determined by the increase or decrease of daylength and temperature, these two external cues greatly influence plant phenology. Regarding the initiation of plant phenology shifts, more attention has been given to temperature effects. However, a landmark meta-analysis demonstrated that increased warming significantly under-predicts phenology shifts. A common garden of plant species collected from regions spanning Europe, Scandinavia, and North America was exposed to short-term warming experiments using heat lamps lasting one growth season. The short-term warming experiment was compared to long-term observational studies lasting several years. For this work, researchers took phenology measurements (leafing and flowering time) to analyze sensitivity to increased warming assessed via shifts in the aforementioned phenology events. Although both studies experienced that same increase in temperature, sensitivity to increased warming in the long-term observational studies exhibited accelerations in leafing and flowering, whereas the short-term heat lamp studies exhibited delays. It’s noteworthy that meta-analysis did not consider rising [CO2] which can directly alter flowering time at a similar, and sometimes larger magnitude than warmer temperatures.Although plants integrate external and endogenous cues to determine the most favorable conditions to initiate flowering, these cues can be perturbed by rising [CO2], causing flowering time shifts. For example, a review comprised of over 60 studies on the effects of elevated CO2 on flowering time revealed that over half of wild and cultivated species exhibited accelerations and delays. Flowering time shifts in response to rising [CO2] can have negative impacts across a macro to micro scale. From an ecological perspective, changes in flowering time can create plant-pollinator mismatches, increase competition among plant and animal species on a community ecosystem level, and lead to unpredictable crop yields. Previous studies on rising [CO2] effects on plant physiology in soybean and other C3 species have shown increases in photosynthesis, foliar sugar concentrations, biomass, and seed yield. Given that previous work has also highlighted how sugars behave as signaling molecules, essentially acting as plant hormones, that can affect plant developmental programming and floral transition, there appears to be at least an indirect link between rising [CO2] and flowering time signaling pathways. However, rising [CO2] does not uniformly affect flowering time in a linear way. Local adaptations to climate, seasonal cues, latitude, and altitude have all been reported to influence flowering, and over time favor specific life history habits such as winter or summer-annual life histories with variation in underlying genetic functioning. Using model plant Arabidopsis thaliana genotypes, which has nearly global coverage as well as documented flowering time variation in elevated [CO2] environments, we can provide more insight into how global change factors like elevated [CO2] may influence flowering times and overall fitness in future climate change scenarios.Previously, a pre-adapted Arabidopsis genotype (referred to as SG) selected for high fitness at elevated [CO2] showed delayed flowering and larger size at flowering when grown at 700 ppm versus 380 ppm [CO2]. This response correlated with prolonged expression of FLOWERING LOCUS C (FLC), a vernalization-responsive floral repressor gene. To determine the molecular mechanism(s) underlying this response, our first aim was to determine if variation in MADS-box transcription factor and major floral repressor FLOWERING LOCUS C (FLC) was directly driving changes in flowering time at elevated [CO2]. To confirm if FLC directly delays flowering at elevated [CO2] in SG, we used a vernalization treatment (a prolonged period of chilling at non-freezing temperatures) to naturally downregulate FLC expression. We hypothesized that vernalization would eliminate delayed flowering at elevated [CO2] through the direct reduction of FLC expression, eliminating differences in flowering time between current and elevated [CO2]. We found that with downregulation of FLC expression via vernalization, SG plants grown at elevated [CO2] no longer delayed flowering compared to current [CO2] based on leaf number and size at flowering. Thus, vernalization returned the earlier flowering phenotype, counteracting effects of elevated [CO2] on flowering. This study indicates that elevated [CO2] can delay flowering directly through FLC, and downregulation of FLC under elevated [CO2] reverses this effect. Moreover, this study demonstrates that increasing [CO2] may potentially drive major changes in development through FLC.In our first aim, we observed how FLC is required for elevated [CO2] to drive changes in flowering time in the pre-adapted selected genotype (SG). To further examine the relationship between FLC and elevated [CO2] our second aim was to determine whether variation in FLC expression levels was a critical component for elevated [CO2] to alter flowering time using natural Arabidopsis genotypes collected from the field. In related research, elevated [CO2]-induced changes in flowering time have been observed in vernalization-responsive wild grasses and crops. Summer-annual or winter-annual Arabidopsis genotypes spend different amounts of time in their vegetative phase, due to their differences in FLC levels (Shindo et al., 2005). Pursuant to our second aim, we also wanted to determine whether there is a threshold response of time (days) spent in an elevated [CO2] environment necessary to influence upregulation in FLC transcriptional activity and subsequent flowering time shifts through altered endogenous cues possibly linked to changes in sugar status. In this study, we tested the response in flowering time across natural Arabidopsis genotypes varying in FLC expression levels as a first assessment of whether high FLC expression is critical for elevated [CO2]-induced effects on flowering time as previously observed in SG. In addition, we also examined whether an elevated [CO2] threshold response of exposure time (0 days, 4 days, 8 days, 12 days, and 16 days) in natural Arabidopsis genotypes can be determined to identify the mechanism driving changes in flowering. We found that, overall, late flowering at elevated [CO2] was associated with higher FLC expression. In addition, a threshold response was revealed in some late-flowering ecotypes. The data provided by this study gives a more informed assessment of the extent by which differences in FLC expression and elevated [CO2] exposure time may influence variation in flowering.In addition to elevated [CO2], flowering time variation and differences in flowering life history habits have been associated with local adaptation to regional climate variables such as latitudinal and altitudinal clines. Regional altitude can affect multiple climate variables such as minimum and maximum seasonal temperatures, precipitation, and vernalization sensitivity that may be acting on flowering time responses. For example, previous work has shown that higher altitude (>800 meters above sea level) Arabidopsis genotypes are typically vernalization obligate and genotypes locally adapted to lower altitudes (800 meters above sea level) Arabidopsis genotypes are typically vernalization obligate and genotypes locally adapted to lower altitudes (< 800 meters above sea level) tend to be vernalization facultative. Obligate genotypes, referred to as winter annuals, are typically more sensitive to vernalization as they require this period of over-wintering in order to reach competence to flower. Facultative genotypes, or summer-annuals, may be responsive to vernalization, however over-wintering is not necessary to complete their life cycle. For winter-annuals, vernalization accelerates flowering by epigenetically silencing the floral repressor transcription factor FLOWERING LOCUS C through a series of histone modifications; repression is stabilized through additional vernalization pathway genes. Previously, we found that elevated [CO2] altered FLC expression and correlated with delayed flowering in SG only when grown in a high CO2 environment. Inadvertently, facultative vernalization responsiveness was observed in SG only when grown at elevated [CO2]. Therefore, for our third aim, we used low and high-altitude Arabidopsis genotypes with known differences in vernalization sensitivity to determine the interaction between vernalization responsiveness and elevated [CO2] on variation in flowering time. In general, we found that elevated [CO2] altered vernalization responsiveness across low and high-altitude genotypes. We also found that, high-altitude genotypes grown at elevated CO2 exhibited more variation in vernalization responsiveness and flowering time, compared to low-altitude genotypes. Vernalization responsiveness is an important agronomic trait, and multiple crops contain genes with analogous FLC functioning. The results here should encourage more work to investigate how vernalization sensitivity can shift under future climate change scenarios in general and at elevated CO2, in particular. 
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Date
2022-08-31
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University of Kansas
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Keywords
Plant sciences, Climate change, elevated carbon dioxide, FLOWERING LOCUS C (FLC), flowering time