Akiko Satake

Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment.

Plants flower in particular seasons even in natural, fluctuating environments. The molecular basis of temperature-dependent flowering-time regulation has been extensively studied, but little is known about how gene expression is controlled in natural environments. Without a memory of past temperatures, it would be difficult for plants to detect seasons in natural, noisy environments because temperature changes occurring within a few weeks are often inconsistent with seasonal trends. Our 2-y census of the expression of a temperature-dependent flowering-time gene, AhgFLC, in a natural population of perennial Arabidopsis halleri revealed that the regulatory system of this flowering-time gene extracts seasonal cues as if it memorizes temperatures over the past 6 wk. Time-series analysis revealed that as much as 83% of the variation in the AhgFLC expression is explained solely by the temperature for the previous 6 wk, but not by the temperatures over shorter or longer periods. The accuracy of our model in predicting the gene expression pattern under contrasting temperature regimes in the transplant experiments indicates that such modeling incorporating the molecular bases of flowering-time regulation will contribute to predicting plant responses to future climate changes.

Spatially limited pollen exchange and a long-range synchronization of trees

Many trees in mature forests show intermittent reproduction. Intensive flowering and seed production occur only once in several years, often synchronized over a long distance. In a previous paper, we showed that the limitation of fruit production by the outcross pollen availability can bring about synchronized reproduction of trees in a constant environment, assuming that pollen availability depends on the mean flowering intensity of the trees. However, pollen exchange normally occurs within a distance much shorter than the extent of the whole forest. We studied a coupled map lattice, in which each tree engages in the chaotic dynamics of energy reserve level, but different trees are coupled by pollen exchange with neighbors. We first derived a relation between two statistics of spatial covariance (dynamic spatial covariance and snapshot spatial covariance). A strong synchronization of tree reproduction can develop over the whole forest that may be orders of magnitude larger than the distance of direct pollen exchange between trees. The fluctuation is close to a cycle with a period of two years. The model of local coupling always generates non-uniform spatial patterns, but the enhanced spatial covariance caused by the spatial heterogeneity is restricted to a short range, only a few times larger than the spatial range of direct interaction. When pollen exchange occurs beyond the nearest neighbors, the local spatial pattern becomes proportionally larger, but the condition for synchronization of the whole forest and its magnitude are the same as for the case with the nearest neighbor pollen exchange. When a fraction of the seeds are sired by globally dispersed pollen and the rest are sired by local pollen, long-range synchronization can occur for a wide-parameter region, and trees may engage in a fluctuation with a masting interval longer than two years. We discuss alternative explanations for the long-range synchronization of beech forests.

Forecasting flowering phenology under climate warming by modelling the regulatory dynamics of flowering-time genes

Understanding how climate warming has an impact on the life cycle schedule of terrestrial organisms is critical to evaluate ecosystem vulnerability to environmental change. Despite recent advances identifying the molecular basis of temperature responses, few studies have incorporated this knowledge into predictive models. Here we develop a method to forecast flowering phenology by modelling regulatory dynamics of key flowering-time genes in perennial life cycles. The model, parameterized by controlled laboratory experiments, accurately reproduces the seasonal changes in gene expression, the corresponding timing of floral initiation and return to vegetative growth after a period of flowering in complex natural environments. A striking scenario forecast by the model under climate warming is that the shift in the return time to vegetative growth is greater than that in floral initiation, which results in a significant reduction of the flowering period. Our study demonstrates the usefulness of gene expression assessment to predict unexplored risks of climate change.

Nonviable seed set enhances plant fitness: the sacrificial sibling hypothesis

Many tree species produce far more fruits than eventually mature, with a large proportion of developing fruits being aborted midway through the development process. Whether this is a maternally controlled late-acting self-incompatibility mechanism, or an expression of inbreeding depression, is difficult to determine. In either case, however, selection is expected to favor early abortion of inbred or incompatible zygotes to minimize loss of resources. In many species, this does not occur, suggesting the possibility of adaptive reasons for retaining selfed or inbred seeds that are aborted at relatively late developmental stages. We propose that such seeds serve an important function in diluting the impact of pre-dispersal seed predators by acting as seed predator sinks and thereby increasing the survival probabilities of outcrossed and fully viable seeds. We suggest that selfed seeds retained and developed through the periods of seed predator attack are effectively offered and sacrificed for the benefit of outcrossed seeds.

Mechanisms inducing spatially extended synchrony in mast seeding: The role of pollen coupling and environmental fluctuation

Trees in mature forests often show intermittent reproduction. Intensive flowering and seed production occur only once in several years (mast seeding), often synchronized over a long distance. Recently, coupled map models for the dynamics of individual energy reserves have been adopted to explain the phenomena. Even in a constant environment, the trees show a large between-year fluctuation in seed crops and the reproduction can be synchronized over the whole forest if the fruit production is limited by the availability of outcross pollen (pollen coupling). The model with local coupling in which trees are coupled by pollen exchange only with the neighbors shows that a strong synchronization of tree reproduction can develop over the whole forest that may be orders of magnitude larger than the distance of direct pollen exchange between trees. However, their fluctuation is close to the period-two oscillation, and is unable to explain observed intermittent reproduction of a longer interval between mast years. Finally the effect of common environmental fluctuation experienced by different individuals is studied, when the annual productivity and the reproductive threshold of trees fluctuate between years. In the absence of pollen limitation, environmental fluctuation correlated strongly between individuals (Moran effect) failed to produce a high positive correlation in seed production between individuals. If both pollen limitation and correlated environmental fluctuation are at work, a significantly large correlation was maintained. Hence, both pollen coupling and common environmental fluctuation are needed to explain synchronized reproduction with intervals longer than 2 years.

Nitrogen as a key regulator of flowering in Fagus crenata: Understanding the physiological mechanism of masting by gene expression analysis

The role of resource availability in determining the incidence of masting has been widely studied, but how floral transition and initiation are regulated by the resource level is unclear. We tested the hypothesis that floral transition is stimulated by high resource availabiltiy in Fagus crenata based on a new technique, the expression analyses of flowering genes. We isolated F. crenata orthologues of FLOWERING LOCUS T, LEAFY and APETALA1, and confirmed their functions using transgenic Arabidopsis thaliana. We monitored the gene expression levels for 5 years and detected a cycle of on and off years, which was correlated with fluctuations of the shoot-nitrogen concentration. Nitrogen fertilisation resulted in the significantly higher expression of flowering genes than the control, where all of the fertilised trees flowered, whereas the control did not. Our findings identified nitrogen as a key regulator of mast flowering, thereby providing new empirical evidence to support the resource budget model.

Spatial Dynamics of Specialist Seed Predators on Synchronized and Intermittent Seed Production of Host Plants

Masting, the synchronized and intermittent seed production by plant populations, provides highly variable food resources for specialist seed predators. Such a reproductive mode helps minimize seed losses through predator satiation and extinction of seed predator populations. The seed predators can buffer the resource variation through dispersal or extended diapause. We developed a spatially explicit resource‐consumer model to understand the effect of masting on specialist seed predators. The masting dynamics were assumed to follow a resource‐based model for plant reproduction, and the population dynamics of the predator were represented by a spatially extended Nicholson‐Bailey model. The resultant model demonstrated that when host plants reproduce intermittently, seed predator populations go locally extinct, but global persistence of the predator is facilitated by dispersal or extended diapause. Global extinction of the predator resulted when the intermittent reproduction is highly synchronized among plants. An approximate invasion criterion for the predators showed that negative lag‐1 autocorrelation in seeding reduces invasibility, and positive lag‐1 cross‐correlation enhances invasibility. Spatial synchronization in seeding at local scale caused by pollen coupling (or climate forcing) further prevented invasion of the predators. If the predators employed extended diapause, extremely high temporal variability in reproduction was required for plants to evade the predators.

Dynamical feedback between circadian clock and sucrose availability explains adaptive response of starch metabolism to various photoperiods

Plants deal with resource management during all their life. During the day they feed on photosynthetic carbon, sucrose, while storing a part into starch for night use. Careful control of carbon partitioning, starch degradation, and sucrose export rates is crucial to avoid carbon starvation, insuring optimal growth whatever the photoperiod. Efficient regulation of these key metabolic rates can give an evolutionary advantage to plants. Here we propose a model of adaptive starch metabolism in response to various photoperiods. We assume the three key metabolic rates to be circadian regulated in leaves and that their phases of oscillations are shifted in response to sucrose starvation. We performed gradient descents for various photoperiod conditions to find the corresponding optimal sets of phase shifts that minimize starvation. Results at convergence were all consistent with experimental data: (1) diurnal starch profile showed linear increase during the day and linear decrease at night; (2) shorter photoperiod tended to increase starch synthesis speed while decreasing its degradation speed during the longer night; (3) sudden early dusk showed slower starch degradation during the longer night. Profiles that best explained observations corresponded to circadian regulation of all rates. This theoretical study would establish a framework for future research on feedback between starch metabolism and circadian clock as well as plant productivity.

Indian Ocean Dipole and Rainfall drive a Moran Effect in East Africa Malaria transmission

BACKGROUND Patterns of concerted fluctuation in populations-synchrony-can reveal impacts of climatic variability on disease dynamics. We examined whether malaria transmission has been synchronous in an area with a common rainfall regime and sensitive to the Indian Ocean Dipole (IOD), a global climatic phenomenon affecting weather patterns in East Africa. METHODS We studied malaria synchrony in 5 15-year long (1984-1999) monthly time series that encompass an altitudinal gradient, approximately 1000 m to 2000 m, along Lake Victoria basin. We quantified the association patterns between rainfall and malaria time series at different altitudes and across the altitudinal gradient encompassed by the study locations. RESULTS We found a positive seasonal association of rainfall with malaria, which decreased with altitude. By contrast, IOD and interannual rainfall impacts on interannual disease cycles increased with altitude. Our analysis revealed a nondecaying synchrony of similar magnitude in both malaria and rainfall, as expected under a Moran effect, supporting a role for climatic variability on malaria epidemic frequency, which might reflect rainfall-mediated changes in mosquito abundance. CONCLUSIONS Synchronous malaria epidemics call for the integration of knowledge on the forcing of malaria transmission by environmental variability to develop robust malaria control and elimination programs.

Coupled ecological and social dynamics in a forested landscape : the deviation of individual decisions from the social optimum

We present a Markov chain model for land-use dynamics in a forested landscape. This model emphasizes the importance of coupling socioeconomic and ecological processes underlying landscape change. We assume that a forest is composed of many land parcels, each of which is in one of a finite list of land-use states. The land-use state of each land parcel changes stochastically. The transition probability is determined by two processes: the forest succession and the decision of landowners. The landowner tends to choose the land-use state which has a high expected discounted utility, i.e., the sum of the current and the future utilities of the land parcel. Landowners take the likelihood of future landscape changes into account when making decisions. We focus on a three-state model in which forested, agricultural, and abandoned states are considered. The land-use composition at equilibrium was analyzed and compared with the social optimum that maximizes the net benefit of all landowners in a society. We show that when landowners make a myopic choice focused on short-term benefits, their individual decisions tend to push the entire landscape toward an agricultural state even if the forested state represents the highest utility. This land-use composition at equilibrium is very different from the social optimum. A long-term management perspective and an enhanced rate of forest recovery can eliminate the discrepancy.