Joy K. Ward

Plant responses to low [CO2] of the past

During the Last Glacial Maximum (LGM; 18,000-20,000 yr ago) and previous glacial periods, atmospheric [CO(2)] dropped to 180-190 ppm, which is among the lowest concentrations that occurred during the evolution of land plants. Modern atmospheric CO(2) concentrations ([CO(2)]) are more than twice those of the LGM and 45% higher than pre-industrial concentrations. Since CO(2) is the carbon source for photosynthesis, lower carbon availability during glacial periods likely had a major impact on plant productivity and evolution. From the studies highlighted here, it is clear that the influence of low [CO(2)] transcends several scales, ranging from physiological effects on individual plants to changes in ecosystem functioning, and may have even influenced the development of early human cultures (via the timing of agriculture). Through low-[CO(2)] studies, we have determined a baseline for plant response to minimal [CO(2)] that occurred during the evolution of land plants. Moreover, an increased understanding of plant responses to low [CO(2)] contributes to our knowledge of how natural global change factors in the past may continue to influence plant responses to future anthropogenic changes. Future work, however, should focus more on the evolutionary responses of plants to changing [CO(2)] in order to account for the potentially large effects of genetic change.

Patterns of Tamarix water use during a record drought

During a record drought (2006) in southwest Kansas, USA, we assessed groundwater dynamics in a shallow, unconfined aquifer, along with plant water sources and physiological responses of the invasive riparian shrub Tamarix ramosissima. In early May, diel water table fluctuations indicated evapotranspirative consumption of groundwater by vegetation. During the summer drought, the water table elevation dropped past the lowest position previously recorded. Concurrent with this drop, water table fluctuations abruptly diminished at all wells at which they had previously been observed despite increasing evapotranspirative demand. Following reductions in groundwater fluctuations, volumetric water content declined corresponding to the well-specific depths of the capillary fringe in early May, suggesting a switch from primary dependence on groundwater to vadose-zone water. In at least one well, the fluctuations appear to re-intensify in August, suggesting increased groundwater uptake by Tamarix or other non-senesced species from a deeper water table later in the growing season. Our data suggest that Tamarix can rapidly shift water sources in response to declines in the water table. The use of multiple water sources by Tamarix minimized leaf-level water stress during drought periods. This study illustrates the importance of the previous hydrologic conditions experienced by site vegetation for controlling root establishment at depth and demonstrates the utility of data from high-frequency hydrologic monitoring in the interpretation of plant water sources using isotopic methods.

Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to increases in CO2 concentration from glacial to future concentrations

SUMMARY *Despite the importance of nutrient availability in determining plant responses to climate change, few studies have addressed the interactive effects of phosphorus (P) supply and rising atmospheric CO(2) concentration ([CO(2)]) from glacial to modern and future concentrations on tree seedling growth. *The objective of our study was to examine interactive effects across a range of P supply (six concentrations from 0.004 to 0.5 mM) and [CO(2)] (200 (glacial), 350 (modern) and 700 (future) ppm) on growth, dry mass allocation, and light-saturated photosynthesis (A(sat)) in Populus deltoides (cottonwood) seedlings grown in well-watered conditions. *Increasing [CO(2)] from glacial to modern concentrations increased growth by 25% across P treatments, reflecting reduced [CO(2)] limitations to photosynthesis and increased A(sat). Conversely, the growth response to future [CO(2)] was very sensitive to P supply. Future [CO(2)] increased growth by 80% in the highest P supply but only by 7% in the lowest P supply, reflecting P limitations to A(sat), leaf area and leaf area ratio (LAR), compared with modern [CO(2)]. *Our results suggest that future [CO(2)] will minimally increase cottonwood growth in low-P soils, but in high-P soils may stimulate production to a greater extent than predicted based on responses to past increases in [CO(2)]. Our results indicate that the capacity for [CO(2)] stimulation of cottonwood growth does not decline as [CO(2)] rises from glacial to future concentrations.

Plastic and adaptive responses of plant respiration to changes in atmospheric CO2 concentration.

The concentration of atmospheric CO2 has increased from below 200 microl l(-1) during last glacial maximum in the late Pleistocene to near 280 microl l(-1) at the beginning of the Holocene and has continuously increased since the onset of the industrial revolution. Most responses of plants to increasing atmospheric CO2 levels result in increases in photosynthesis, water use efficiency and biomass. Less known is the role that respiration may play during adaptive responses of plants to changes in atmospheric CO2. Although plant respiration does not increase proportionally with CO2-enhanced photosynthesis or growth rates, a reduction in respiratory costs in plants grown at subambient CO2 can aid in maintaining a positive plant C-balance (i.e. enhancing the photosynthesis-to-respiration ratio). The understanding of plant respiration is further complicated by the presence of the alternative pathway that consumes photosynthate without producing chemical energy [adenosine triphosphate (ATP)] as effectively as respiration through the normal cytochrome pathway. Here, we present the respiratory responses of Arabidopsis thaliana plants selected at Pleistocene (200 microl l(-1)), current Holocene (370 microl l(-1)), and elevated (700 microl l(-1)) concentrations of CO2 and grown at current CO2 levels. We found that respiration rates were lower in Pleistocene-adapted plants when compared with Holocene ones, and that a substantial reduction in respiration was because of reduced activity of the alternative pathway. In a survey of the literature, we found that changes in respiration across plant growth forms and CO2 levels can be explained in part by differences in the respiratory energy demand for maintenance of biomass. This trend was substantiated in the Arabidopsis experiment in which Pleistocene-adapted plants exhibited decreases in respiration without concurrent reductions in tissue N content. Interestingly, N-based respiration rates of plants adapted to elevated CO2 also decreased. As a result, ATP yields per unit of N increased in Pleistocene-adapted plants compared with current CO2 adapted ones. Our results suggest that mitochondrial energy coupling and alternative pathway-mediated responses of respiration to changes in atmospheric CO2 may enhance survival of plants at low CO2 levels to help overcome a low carbon balance. Therefore, increases in the basal activity of the alternative pathway are not necessarily associated to metabolic plant stress in all cases.

Elevated CO2 influences the expression of floral‐initiation genes in Arabidopsis thaliana

Atmospheric CO(2) concentration ([CO(2)]) is rising on a global scale and is known to affect flowering time. Elevated [CO(2)] may be as influential as temperature in determining future changes in plant developmental timing, but little is known about the molecular mechanisms that control altered flowering times at elevated [CO(2)]. Using Arabidopsis thaliana, the expression patterns were compared of floral-initiation genes between a genotype that was selected for high fitness at elevated [CO(2)] and a nonselected control genotype. The selected genotype exhibits pronounced delays in flowering time when grown at elevated [CO(2)], whereas the control genotype is unaffected by elevated [CO(2)]. Thus, this comparison provides an evolutionarily relevant system for gaining insight into the responses of plants to future increases in [CO(2)]. Evidence is provided that elevated [CO(2)] influences the expression of floral-initiation genes. In addition, it is shown that delayed flowering at elevated [CO(2)] is associated with sustained expression of the floral repressor gene, FLOWERING LOCUS C (FLC), in an elevated CO(2)-adapted genotype. Understanding the mechanisms that account for changes in plant developmental timing at elevated [CO(2)] is critical for predicting the responses of plants to a high-CO(2) world of the near future.

Glacial trees from the La Brea tar pits show physiological constraints of low CO2

• While studies of modern plants indicate negative responses to low [CO₂] that occurred during the last glacial period, studies with glacial plant material that incorporate evolutionary responses are rare. In this study, physiological responses to changing [CO₂] were compared between glacial (La Brea tar pits) and modern Juniperus trees from southern California. • Carbon isotopes were measured on annual rings of glacial and modern Juniperus. The intercellular:atmospheric [CO₂] ratio (c(i) /c(a) ) and intercellular [CO₂] (c(i) ) were then calculated on an annual basis and compared through geologic time. • Juniperus showed constant mean c(i) /c(a) between the last glacial period and modern times, spanning 50,000 yr. Interannual variation in physiology was greatly dampened during the last glacial period relative to the present, indicating constraints of low [CO₂] that reduced responses to other climatic factors. Furthermore, glacial Juniperus exhibited low c(i) that rarely occurs in modern trees, further suggesting limiting [CO₂] in glacial plants. • This study provides some of the first direct evidence that glacial plants remained near their lower carbon limit until the beginning of the glacial-interglacial transition. Our results also suggest that environmental factors that dominate carbon-uptake physiology vary across geologic time, resulting in major alterations in physiological response patterns through time.

Physiological and Growth Responses of C3 and C4 Plants to Reduced Temperature When Grown at Low CO2 of the Last Ice Age

During the last ice age, CO2 concentration ([CO2]) was 180-200 micromol/mol compared with the modern value of 380 micromol/mol, and global temperatures were approximately 8 degrees C cooler. Relatively little is known about the responses of C3 and C4 species to long-term exposure to glacial conditions. Here Abutilon theophrasti Medik. (C3) and Amaranthus retroflexus L. (C4) were grown at 200 micromol/mol CO2 with current (30/24 degrees C) and glacial (22/16 degrees C) temperatures for 22 d. Overall, the C4 species exhibited a large growth advantage over the C3 species at low [CO2]. However, this advantage was reduced at low temperature, where the C4 species produced 5 x the total mass of the C3 species versus 14 x at the high temperature. This difference was due to a reduction in C4 growth at low temperature, since the C3 species exhibited similar growth between temperatures. Physiological differences between temperatures were not detected for either species, although photorespiration/net photosynthesis was reduced in the C3 species grown at low temperature, suggesting evidence of improved carbon balance at this treatment. This system suggests that C4 species had a growth advantage over C3 species during low [CO2] of the last ice age, although concurrent reductions in temperatures may have reduced this advantage.

Evolutionary history underlies plant physiological responses to global change since the last glacial maximum

Assessing family- and species-level variation in physiological responses to global change across geologic time is critical for understanding factors that underlie changes in species distributions and community composition. Here, we used stable carbon isotopes, leaf nitrogen content and stomatal measurements to assess changes in leaf-level physiology in a mixed conifer community that underwent significant changes in composition since the last glacial maximum (LGM) (21 kyr BP). Our results indicate that most plant taxa decreased stomatal conductance and/or maximum photosynthetic capacity in response to changing conditions since the LGM. However, plant families and species differed in the timing and magnitude of these physiological responses, and responses were more similar within families than within co-occurring species assemblages. This suggests that adaptation at the level of leaf physiology may not be the main determinant of shifts in community composition, and that plant evolutionary history may drive physiological adaptation to global change over recent geologic time.

Identification of a Major QTL That Alters Flowering Time at Elevated [CO2] in Arabidopsis thaliana

Background The transition from vegetative to reproductive stages marks a major milestone in plant development. It is clear that global change factors (e.g., increasing [CO2] and temperature) have already had and will continue to have a large impact on plant flowering times in the future. Increasing atmospheric [CO2] has recently been shown to affect flowering time, and may produce even greater responses than increasing temperature. Much is known about the genes influencing flowering time, although their relevance to changing [CO2] is not well understood. Thus, we present the first study to identify QTL (Quantitative Trait Loci) that affect flowering time at elevated [CO2] in Arabidopsis thaliana. Methodology/Principal Findings We developed our mapping population by crossing a genotype previously selected for high fitness at elevated [CO2] (SG, Selection Genotype) to a Cape Verde genotype (Cvi-0). SG exhibits delayed flowering at elevated [CO2], whereas Cvi-0 is non-responsive to elevated [CO2] for flowering time. We mapped one major QTL to the upper portion of chromosome 1 that explains 1/3 of the difference in flowering time between current and elevated [CO2] between the SG and Cvi-0 parents. This QTL also alters the stage at which flowering occurs, as determined from higher rosette leaf number at flowering in RILs (Recombinant Inbred Lines) harboring the SG allele. A follow-up study using Arabidopsis mutants for flowering time genes within the significant QTL suggests MOTHER OF FT AND TFL1 (MFT) as a potential candidate gene for altered flowering time at elevated [CO2]. Conclusion/Significance This work sheds light on the underlying genetic architecture that controls flowering time at elevated [CO2]. Prior to this work, very little to nothing was known about these mechanisms at the genomic level. Such a broader understanding will be key for better predicting shifts in plant phenology and for developing successful crops for future environments.

Examining Plant Physiological Responses to Climate Change through an Evolutionary Lens

Integrating knowledge from physiological ecology, evolutionary biology, phylogenetics, and paleobiology provides novel insights into factors driving plant physiological responses to both past and future climate change.