Natural variation in tolerance to sub-zero temperatures among populations of Arabidopsis lyrata ssp. petraea.

BACKGROUND: Temperature is one of the most important abiotic factors limiting plant growth and productivity. Many plants exhibit cold acclimation to prepare for the likelihood of freezing as temperatures decrease towards 0 °C. The physiological mechanisms associated with enabling increased tolerance to sub-zero temperatures vary between species and genotypes. Geographically and climatically diverse populations of Arabidopsis lyrata ssp. petraea were examined for their ability to survive, maintain functional photosynthetic parameters and cellular electrolyte leakage integrity after being exposed to sub-zero temperatures. The duration of cold acclimation prior to sub-zero temperatures was also manipulated (2 and 14 days). RESULTS: We found that there was significant natural variation in tolerances to sub-zero temperatures among populations of A. petraea. The origin of the population affected the acclimation response and survival after exposure to sub-zero temperatures. Cold acclimation of plants prior to sub-zero temperatures affected the maximum quantum efficiency of photosystem II (PSII) (Fv/Fm) in that plants that were cold acclimated for longer periods had higher values of Fv/Fm as a result of sub-zero temperatures. The inner immature leaves were better able to recover Fv/Fm from sub-zero temperatures than mature outer leaves. The Irish population (Leitrim) acclimated faster, in terms of survival and electrolyte leakage than the Norwegian population (Helin). CONCLUSION: The ability to survive, recover photosynthetic processes and cellular electrolyte leakage after exposure to sub-zero temperatures is highly dependent on the duration of cold acclimation.

The impact of alternative trait-scaling hypotheses for the maximum photosynthetic carboxylation rate (Vcmax ) on global gross primary production.

The maximum photosynthetic carboxylation rate (Vcmax ) is an influential plant trait that has multiple scaling hypotheses, which is a source of uncertainty in predictive understanding of global gross primary production (GPP). Four trait-scaling hypotheses (plant functional type, nutrient limitation, environmental filtering, and plant plasticity) with nine specific implementations were used to predict global Vcmax distributions and their impact on global GPP in the Sheffield Dynamic Global Vegetation Model (SDGVM). Global GPP varied from 108.1 to 128.2 PgC yr-1 , 65% of the range of a recent model intercomparison of global GPP. The variation in GPP propagated through to a 27% coefficient of variation in net biome productivity (NBP). All hypotheses produced global GPP that was highly correlated (r = 0.85-0.91) with three proxies of global GPP. Plant functional type-based nutrient limitation, underpinned by a core SDGVM hypothesis that plant nitrogen (N) status is inversely related to increasing costs of N acquisition with increasing soil carbon, adequately reproduced global GPP distributions. Further improvement could be achieved with accurate representation of water sensitivity and agriculture in SDGVM. Mismatch between environmental filtering (the most data-driven hypothesis) and GPP suggested that greater effort is needed understand Vcmax variation in the field, particularly in northern latitudes.

Effects of elevated carbon dioxide on stomatal characteristics and carbon isotope ratio of Arabidopsis thaliana ecotypes originating from an altitudinal gradient.

Stomatal functioning regulates the fluxes of CO2 and water vapor between vegetation and atmosphere and thereby influences plant adaptation to their habitats. Stomatal traits are controlled by external environmental and internal cellular signaling. The objective of this study was to quantify the effects of CO2 enrichment (CE) on stomatal density (SD)-related properties, guard cell length (GCL) and carbon isotope ratio (δ13 C) of a range of Arabidopsis thaliana ecotypes originating from a wide altitudinal range [50-1260 m above sea level (asl)], and grown at 400 and 800 ppm [CO2 ], and thereby elucidate the possible adaptation and acclimation responses controlling stomatal traits and water use efficiency (WUE). There was a highly significant variation among ecotypes in the magnitude and direction of response of stomatal traits namely, SD and stomatal index (SI) and GCL, and δ13 C to CE, which represented a short-term acclimation response. A majority of ecotypes showed increased SD and SI with CE with the response not depending on the altitude of origin. Significant ecotypic variation was shown in all stomatal traits and δ13 C at each [CO2 ]. At 400 ppm, means of SD, SI and GCL for broad altitudinal ranges, i.e. low (<100 m), mid (100-400 m) and high (>400 m), increased with increasing altitude, which represented an adaptation response to decreased availability of CO2 with altitude. δ13 C was negatively correlated to SD and SI at 800 ppm but not at 400 ppm. Our results highlight the diversity in the response of key stomatal characters to CE and altitude within the germplasm of A. thaliana and the need to consider this diversity when using A. thaliana as a model plant.

Carbon residence time dominates uncertainty in terrestrial vegetation responses to future climate and atmospheric CO2.

Future climate change and increasing atmospheric CO2 are expected to cause major changes in vegetation structure and function over large fractions of the global land surface. Seven global vegetation models are used to analyze possible responses to future climate simulated by a range of general circulation models run under all four representative concentration pathway scenarios of changing concentrations of greenhouse gases. All 110 simulations predict an increase in global vegetation carbon to 2100, but with substantial variation between vegetation models. For example, at 4 °C of global land surface warming (510-758 ppm of CO2), vegetation carbon increases by 52-477 Pg C (224 Pg C mean), mainly due to CO2 fertilization of photosynthesis. Simulations agree on large regional increases across much of the boreal forest, western Amazonia, central Africa, western China, and southeast Asia, with reductions across southwestern North America, central South America, southern Mediterranean areas, southwestern Africa, and southwestern Australia. Four vegetation models display discontinuities across 4 °C of warming, indicating global thresholds in the balance of positive and negative influences on productivity and biomass. In contrast to previous global vegetation model studies, we emphasize the importance of uncertainties in projected changes in carbon residence times. We find, when all seven models are considered for one representative concentration pathway × general circulation model combination, such uncertainties explain 30% more variation in modeled vegetation carbon change than responses of net primary productivity alone, increasing to 151% for non-HYBRID4 models. A change in research priorities away from production and toward structural dynamics and demographic processes is recommended.

Physiological advantages of C4 grasses in the field: a comparative experiment demonstrating the importance of drought.

Global climate change is expected to shift regional rainfall patterns, influencing species distributions where they depend on water availability. Comparative studies have demonstrated that C4 grasses inhabit drier habitats than C3 relatives, but that both C3 and C4 photosynthesis are susceptible to drought. However, C4 plants may show advantages in hydraulic performance in dry environments. We investigated the effects of seasonal variation in water availability on leaf physiology, using a common garden experiment in the Eastern Cape of South Africa to compare 12 locally occurring grass species from C4 and C3 sister lineages. Photosynthesis was always higher in the C4 than C3 grasses across every month, but the difference was not statistically significant during the wettest months. Surprisingly, stomatal conductance was typically lower in the C3 than C4 grasses, with the peak monthly average for C3 species being similar to that of C4 leaves. In water-limited, rain-fed plots, the photosynthesis of C4 leaves was between 2.0 and 7.4 µmol m(-2) s(-1) higher, stomatal conductance almost double, and transpiration 60% higher than for C3 plants. Although C4 average instantaneous water-use efficiencies were higher (2.4-8.1 mmol mol(-1)) than C3 averages (0.7-6.8 mmol mol(-1)), differences were not as great as we expected and were statistically significant only as drought became established. Photosynthesis declined earlier during drought among C3 than C4 species, coincident with decreases in stomatal conductance and transpiration. Eventual decreases in photosynthesis among C4 plants were linked with declining midday leaf water potentials. However, during the same phase of drought, C3 species showed significant decreases in hydrodynamic gradients that suggested hydraulic failure. Thus, our results indicate that stomatal and hydraulic behaviour during drought enhances the differences in photosynthesis between C4 and C3 species. We suggest that these drought responses are important for understanding the advantages of C4 photosynthesis under field conditions.

Plant growth rates and seed size: a re-evaluation.

Small-seeded plant species are often reported to have high relative growth rate or RGR. However, because RGR declines as plants grow larger, small-seeded species could achieve higher RGR simply by virtue of their small size. In contrast, size-standardized growth rate or SGR factors out these size effects. Differences in SGR can thus only be due to differences in morphology, allocation, or physiology. We used nonlinear regression to calculate SGR for comparison with RGR for 10 groups of species spanning a wide range of life forms. We found that RGR was negatively correlated with seed mass in nearly all groups, but the relationship between SGR and seed mass was highly variable. We conclude that small-seeded species only sometimes possess additional adaptations for rapid growth over and above their general size advantage.

Partitioning the components of relative growth rate: how important is plant size variation?

Plant growth plays a key role in the functioning of the terrestrial biosphere, and there have been substantial efforts to understand why growth varies among species. To this end, a large number of experimental analyses have been undertaken; however, the emergent patterns between growth rate and its components are often contradictory. We believe that these conflicting results are a consequence of the way growth is measured. Growth is typically characterized by relative growth rate (RGR); however, RGR often declines as organisms get larger, making it difficult to compare species of different sizes. To overcome this problem, we advocate using nonlinear mixed-effects models so that RGR can be calculated at a standard size, and we present easily implemented methods for doing this. We then present new methods for analyzing the traditional components of RGR that explicitly allow for the fact that (log)(RGR) is the sum of its components. These methods provide an exact decomposition of the variance in (log)(RGR). Finally, we use simple analytical and simulation approaches to explore the effect of size variation on growth and its components and show that the relative importance of the components of RGR is influenced by the extent to which analyses standardize for plant size.

Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations.

*Second-generation Dynamic Global Vegetation Models (DGVMs) have recently been developed that explicitly represent the ecological dynamics of disturbance, vertical competition for light, and succession. Here, we introduce a modified second-generation DGVM and examine how the representation of demographic processes operating at two-dimensional spatial scales not represented by these models can influence predicted community structure, and responses of ecosystems to climate change. *The key demographic processes we investigated were seed advection, seed mixing, sapling survival, competitive exclusion and plant mortality. We varied these parameters in the context of a simulated Amazon rainforest ecosystem containing seven plant functional types (PFTs) that varied along a trade-off surface between growth and the risk of starvation induced mortality. *Varying the five unconstrained parameters generated community structures ranging from monocultures to equal co-dominance of the seven PFTs. When exposed to a climate change scenario, the competing impacts of CO(2) fertilization and increasing plant mortality caused ecosystem biomass to diverge substantially between simulations, with mid-21st century biomass predictions ranging from 1.5 to 27.0 kg C m(-2). *Filtering the results using contemporary observation ranges of biomass, leaf area index (LAI), gross primary productivity (GPP) and net primary productivity (NPP) did not substantially constrain the potential outcomes. We conclude that demographic processes represent a large source of uncertainty in DGVM predictions.

Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment.

Experimental evidence demonstrates a higher efficiency of water and nitrogen use in C(4) compared with C(3) plants, which is hypothesized to drive differences in biomass allocation between C(3) and C(4) species. However, recent work shows that contrasts between C(3) and C(4) grasses may be misinterpreted without phylogenetic control. Here, we compared leaf physiology and growth in multiple lineages of C(3) and C(4) grasses sampled from a monophyletic clade, and asked the following question: which ecophysiological traits differ consistently between photosynthetic types, and which vary among lineages? C(4) species had lower stomatal conductance and water potential deficits, and higher water-use efficiency than C(3) species. Photosynthesis and nitrogen-use efficiency were also greater in C(4) species, varying markedly between clades. Contrary to previous studies, leaf nitrogen concentration was similar in C(4) and C(3) types. Canopy mass and area were greater, and root mass smaller, in the tribe Paniceae than in most other lineages. The size of this phylogenetic effect on biomass partitioning was greater in the C(4) NADP-me species than in species of other types. Our results show that the phylogenetic diversity underlying C(4) photosynthesis is critical to understanding its functional consequences. Phylogenetic bias is therefore a crucial factor to be considered when comparing the ecophysiology of C(3) and C(4) species.

The role of stomata in sensing and driving environmental change.

Stomata, the small pores on the surfaces of leaves and stalks, regulate the flow of gases in and out of leaves and thus plants as a whole. They adapt to local and global changes on all timescales from minutes to millennia. Recent data from diverse fields are establishing their central importance to plant physiology, evolution and global ecology. Stomatal morphology, distribution and behaviour respond to a spectrum of signals, from intracellular signalling to global climatic change. Such concerted adaptation results from a web of control systems, reminiscent of a 'scale-free' network, whose untangling requires integrated approaches beyond those currently used.

Variation at range margins across multiple spatial scales: environmental temperature, population genetics and metabolomic phenotype.

Range margins are spatially complex, with environmental, genetic and phenotypic variations occurring across a range of spatial scales. We examine variation in temperature, genes and metabolomic profiles within and between populations of the subalpine perennial plant Arabidopsis lyrata ssp. petraea from across its northwest European range. Our surveys cover a gradient of fragmentation from largely continuous populations in Iceland, through more fragmented Scandinavian populations, to increasingly widely scattered populations at the range margin in Scotland, Wales and Ireland. Temperature regimes vary substantially within some populations, but within-population variation represents a larger fraction of genetic and especially metabolomic variances. Both physical distance and temperature differences between sites are found to be associated with genetic profiles, but not metabolomic profiles, and no relationship was found between genetic and metabolomic population structures in any region. Genetic similarity between plants within populations is the highest in the fragmented populations at the range margin, but differentiation across space is the highest there as well, suggesting that regional patterns of genetic diversity may be scale dependent.

Genome size as a predictor of guard cell length in Arabidopsis thaliana is independent of environmental conditions.

The recent discovery of a strong positive relationship between angiosperm genome size and stomatal guard cell length (GCL) opens the possibility of using plant fossil guard cell size as a proxy for changes in angiosperm genome size over periods of environmental change. The responses of GCL to environmental stimuli are currently unknown and may obscure this predictive relationship. Here, we investigated the effects of environmental variables (atmospheric CO2, drought, relative humidity, irradiance, ultraviolet radiation and pathogen attack) on GCL in the model plant Arabidopsis thaliana to quantify environmentally induced variation. GCL responded to all variables tested, but the changes incurred did not significantly impinge on the predictive capability of the relationship.

Potential impacts of global elevated CO(2) concentrations on plants.

Early experiments investigating the effects of CO(2) enrichment on plants frequently showed photosynthetic stimulation and reduced stomatal aperture over short time periods. Work on the effects of elevated CO(2) has advanced in two major areas: by the extension of long-term and field experiments, and through investigations on the wide range of negative feedbacks affecting plant responses to CO(2). Downward photosynthetic acclimation in response to CO(2) enrichment is frequently observed over the short and long term, and indicates the activity of diverse feedback mechanisms. CO(2) is generally viewed as a limiting photosynthetic resource. However, recent work on stomatal development has shown that this view is simplistic: long- and short-distance signalling of CO(2) concentration are necessary components of normal plant development.