Ingo Ensminger

Increased Air Temperature during Simulated Autumn Conditions Does Not Increase Photosynthetic Carbon Gain But Affects the Dissipation of Excess Energy in Seedlings of the Evergreen Conifer Jack Pine

Temperature and daylength act as environmental signals that determine the length of the growing season in boreal evergreen conifers. Climate change might affect the seasonal development of these trees, as they will experience naturally decreasing daylength during autumn, while at the same time warmer air temperature will maintain photosynthesis and respiration. We characterized the down-regulation of photosynthetic gas exchange and the mechanisms involved in the dissipation of energy in Jack pine (Pinus banksiana) in controlled environments during a simulated summer-autumn transition under natural conditions and conditions with altered air temperature and photoperiod. Using a factorial design, we dissected the effects of daylength and temperature. Control plants were grown at either warm summer conditions with 16-h photoperiod and 22°C or conditions representing a cool autumn with 8 h/7°C. To assess the impact of photoperiod and temperature on photosynthesis and energy dissipation, plants were also grown under either cold summer (16-h photoperiod/7°C) or warm autumn conditions (8-h photoperiod/22°C). Photosynthetic gas exchange was affected by both daylength and temperature. Assimilation and respiration rates under warm autumn conditions were only about one-half of the summer values but were similar to values obtained for cold summer and natural autumn treatments. In contrast, photosynthetic efficiency was largely determined by temperature but not by daylength. Plants of different treatments followed different strategies for dissipating excess energy. Whereas in the warm summer treatment safe dissipation of excess energy was facilitated via zeaxanthin, in all other treatments dissipation of excess energy was facilitated predominantly via increased aggregation of the light-harvesting complex of photosystem II. These differences were accompanied by a lower deepoxidation state and larger amounts of β-carotene in the warm autumn treatment as well as by changes in the abundance of thylakoid membrane proteins compared to the summer condition. We conclude that photoperiod control of dormancy in Jack pine appears to negate any potential for an increased carbon gain associated with higher temperatures during the autumn season.

Soil temperature and intermittent frost modulate the rate of recovery of photosynthesis in Scots pine under simulated spring conditions

An earlier onset of photosynthesis in spring for boreal forest trees is predicted as the climate warms, yet the importance of soil vs air temperatures for spring recovery remains to be determined. Effects of various soil- and air-temperature conditions on spring recovery of photosynthesis in Scots pine (Pinus sylvestris) seedlings were assessed under controlled environmental conditions. Using winter-acclimated seedlings, photosynthetic responses were followed after transfer to different simulated spring conditions. Recovery rates for photosynthetic electron transport and net CO(2) uptake were slower in plants from cold or frozen soil compared with controls. In addition, a greater fraction of light absorbed was not used photochemically, but was dissipated thermally via xanthophyll cycle pigments. Intermittent frost events decreased photosynthetic capacity and increased thermal energy dissipation. Within a few days after frost events, photosynthetic capacity recovered to prefrost levels. After 18 d under spring conditions, no difference in the optimum quantum yield of photosynthesis was observed between seedlings that had been exposed to intermittent frost and control plants. These results show that, if air temperatures remain favourable and spells of subfreezing air temperatures are only of short duration, intermittent frost events delay but do not severely inhibit photosynthetic recovery in evergreen conifers during spring. Cold and/or frozen soils exert much stronger inhibitory effects on the recovery process, but they do not totally inhibit it.

A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers

Significance Evergreen photosynthetic activity has been difficult to determine from remote sensing, causing errors in terrestrial photosynthetic carbon uptake models. Using a reflectance chlorophyll/carotenoid index (CCI) sensitive to seasonally changing chlorophyll/carotenoid pigment ratios, we demonstrate a method of tracking photosynthetic phenology in evergreen conifers. The CCI reveals seasonally changing photosynthetic rates and detects the onset of the growing season in evergreen foliage. This method could improve our understanding of changing photosynthetic activity in a warming climate, and could improve assessment of the evergreen component of the terrestrial carbon budget, which has been elusive. In evergreen conifers, where the foliage amount changes little with season, accurate detection of the underlying “photosynthetic phenology” from satellite remote sensing has been difficult, presenting challenges for global models of ecosystem carbon uptake. Here, we report a close correspondence between seasonally changing foliar pigment levels, expressed as chlorophyll/carotenoid ratios, and evergreen photosynthetic activity, leading to a “chlorophyll/carotenoid index” (CCI) that tracks evergreen photosynthesis at multiple spatial scales. When calculated from NASA’s Moderate Resolution Imaging Spectroradiometer satellite sensor, the CCI closely follows the seasonal patterns of daily gross primary productivity of evergreen conifer stands measured by eddy covariance. This discovery provides a way of monitoring evergreen photosynthetic activity from optical remote sensing, and indicates an important regulatory role for carotenoid pigments in evergreen photosynthesis. Improved methods of monitoring photosynthesis from space can improve our understanding of the global carbon budget in a warming world of changing vegetation phenology.

Increased Air Temperature during Simulated Autumn Conditions Impairs Photosynthetic Electron Transport between Photosystem II and Photosystem I

Changes in temperature and daylength trigger physiological and seasonal developmental processes that enable evergreen trees of the boreal forest to withstand severe winter conditions. Climate change is expected to increase the autumn air temperature in the northern latitudes, while the natural decreasing photoperiod remains unaffected. As shown previously, an increase in autumn air temperature inhibits CO2 assimilation, with a concomitant increased capacity for zeaxanthin-independent dissipation of energy exceeding the photochemical capacity in Pinus banksiana. In this study, we tested our previous model of antenna quenching and tested a limitation in intersystem electron transport in plants exposed to elevated autumn air temperatures. Using a factorial design, we dissected the effects of temperature and photoperiod on the function as well as the stoichiometry of the major components of the photosynthetic electron transport chain in P. banksiana. Natural summer conditions (16-h photoperiod/22°C) and late autumn conditions (8-h photoperiod/7°C) were compared with a treatment of autumn photoperiod with increased air temperature (SD/HT: 8-h photoperiod/22°C) and a treatment with summer photoperiod and autumn temperature (16-h photoperiod/7°C). Exposure to SD/HT resulted in an inhibition of the effective quantum yield associated with a decreased photosystem II/photosystem I stoichiometry coupled with decreased levels of Rubisco. Our data indicate that a greater capacity to keep the primary electron donor of photosystem I (P700) oxidized in plants exposed to SD/HT compared with the summer control may be attributed to a reduced rate of electron transport from the cytochrome b6f complex to photosystem I. Photoprotection under increased autumn air temperature conditions appears to be consistent with zeaxanthin-independent antenna quenching through light-harvesting complex II aggregation and a decreased efficiency in energy transfer from the antenna to the photosystem II core. We suggest that models that predict the effect of climate change on the productivity of boreal forests must take into account the interactive effects of photoperiod and elevated temperatures.

Biochemical constrains limit the potential of the photochemical reflectance index as a predictor of effective quantum efficiency of photosynthesis during the winter spring transition in Jack pine seedlings

Leaf reflectance spectral measurements are an emerging non-invasive technique that can be used to derive the photochemical reflectance index (PRI) to assess the physiological state of plants from leaf to ecosystem level. Changes in PRI are associated with changes in the xanthophyll cycle activity and provide an estimate of changes in the effective photochemical quantum efficiency (ΦII) during the growing season. However, we hypothesised that the correlation between PRI and ΦII might be poor when the xanthophyll cycle is primed for sustained thermal dissipation of the light energy absorbed. To test our hypothesis, we studied the recovery of winter acclimated Jack pine (Pinus banksiana Lamb.) seedlings that were exposed to different simulated spring recovery treatments in controlled environments. Different growth temperatures and light intensities were used to dissect the effect of these two factors on chlorophyll fluorescence, pigment composition and leaf reflectance. ΦII showed a clear response to temperature whereas PRI was mostly affected by light intensity. In contrast, the de-epoxidation state of the xanthophyll cycle pigments was both temperature and light dependent. Our data suggest that zeaxanthin-independent non-photochemical quenching is employed to various degrees in the different treatments. As a result, within the limits of our experimental setup, PRI could not explain the variation in ΦII. This indicates that an improved understanding of the different energy quenching mechanisms is critical to accurately interpret the PRI signal under environmental conditions where the predominant mode of excess energy dissipation does not involve a dynamic operation of the xanthophyll cycle, but a sustained mechanism of energy dissipation.

A catalogue of putative unique transcripts from Douglas-fir (Pseudotsuga menziesii) based on 454 transcriptome sequencing of genetically diverse, drought stressed seedlings

BackgroundDouglas-fir (Pseudotsuga menziesii) extends over a wide range of contrasting environmental conditions, reflecting substantial local adaptation. For this reason, it is an interesting model species to study plant adaptation and the effects of global climate change such as increased temperatures and significant periods of drought on individual trees and the forest landscape in general. However, genomic data and tools for studying genetic variation in natural populations to understand the genetic and physiological mechanisms of adaptation are currently missing for Douglas-fir. This study represents a first step towards characterizing the Douglas-fir transcriptome based on 454 sequencing of twelve cDNA libraries. The libraries were constructed from needle and wood tissue of coastal and interior provenances subjected to drought stress experiments.ResultsThe 454 sequencing of twelve normalized cDNA libraries resulted in 3.6 million reads from which a set of 170,859 putative unique transcripts (PUTs) was assembled. Functional annotation by BLAST searches and Gene Ontology mapping showed that the composition of functional classes is very similar to other plant transcriptomes and demonstrated that a large fraction of the Douglas-fir transcriptome is tagged by the PUTs. Based on evolutionary conservation, we identified about 1,000 candidate genes related to drought stress. A total number of 187,653 single nucleotide polymorphisms (SNPs) were detected by three SNP detection tools. However, only 27,688 SNPs were identified by all three methods, indicating that SNP detection depends on the particular method used. The two alleles of about 60% of the 27,688 SNPs are segregating simultaneously in both coastal and interior provenances, which indicates a high proportion of ancestral shared polymorphisms or a high level of gene flow between these two ecologically and phenotypically different varieties.ConclusionsWe established a catalogue of PUTs and large SNP database for Douglas-fir. Both will serve as a useful resource for the further characterization of the genome and transcriptome of Douglas-fir and for the analysis of genetic variation using genotyping or resequencing methods.

Zeaxanthin-independent energy quenching and alternative electron sinks cause a decoupling of the relationship between the photochemical reflectance index (PRI) and photosynthesis in an evergreen conifer during spring

Highlight Decoupling of the photochemical reflectance index and photosynthesis in evergreen conifers during spring is caused by energy-quenching mechanisms that remain undetected by leaf reflectance measurements and remote sensing.

Relationship between leaf optical properties, chlorophyll fluorescence and pigment changes in senescing Acer saccharum leaves

The ability of plants to sequester carbon is highly variable over the course of the year and reflects seasonal variation in photosynthetic efficiency. This seasonal variation is most prominent during autumn, when leaves of deciduous tree species such as sugar maple (Acer saccharum Marsh.) undergo senescence, which is associated with downregulation of photosynthesis and a change of leaf color. The remote sensing of leaf color by spectral reflectance measurements and digital repeat images is increasingly used to improve models of growing season length and seasonal variation in carbon sequestration. Vegetation indices derived from spectral reflectance measurements and digital repeat images might not adequately reflect photosynthetic efficiency of red-senescing tree species during autumn due to the changes in foliar pigment content associated with autumn phenology. In this study, we aimed to assess how effectively several widely used vegetation indices capture autumn phenology and reflect the changes in physiology and photosynthetic pigments during autumn. Chlorophyll fluorescence and pigment content of green, yellow, orange and red leaves were measured to represent leaf senescence during autumn and used as a reference to validate and compare vegetation indices derived from leaf-level spectral reflectance measurements and color analysis of digital images. Vegetation indices varied in their suitability to track the decrease of photosynthetic efficiency and chlorophyll content despite increasing anthocyanin content. Commonly used spectral reflectance indices such as the normalized difference vegetation index and photochemical reflectance index showed major constraints arising from a limited representation of gradual decreases in chlorophyll content and an influence of high foliar anthocyanin levels. The excess green index and green-red vegetation index were more suitable to assess the process of senescence. Similarly, digital image analysis revealed that vegetation indices such as Hue and normalized difference index are superior compared with the often-used green chromatic coordinate. We conclude that indices based on red and green color information generally represent autumn phenology most efficiently.

A coastal and an interior Douglas fir provenance exhibit different metabolic strategies to deal with drought stress

Drought is a major environmental stress affecting growth and vitality of forest ecosystems. In the present study, foliar nitrogen (N) and carbon (C) metabolism of two Douglas fir (Pseudotsuga menziesii) provenances with assumed different drought tolerance were investigated. We worked with 1-year-old seedlings of the interior provenance Fehr Lake (FEHR) originating from a dry environment and the coastal provenance Snoqualmie (SNO) from a more humid origin. Total C and N, structural N and the concentrations of soluble protein, total amino acids (TAAs) and individual amino acids as well as the relative abundance of polar, low-molecular-weight metabolites including antioxidants were determined in current-year needles exposed either to 42 days of drought or to 42 days drought plus 14 days of rewatering. The seedlings reacted in a provenance-specific manner to drought stress. Coastal provenance SNO showed considerably increased contents of TAAs, which were caused by increased abundance of the quantitatively most important amino acids arginine, ornithine and lysine. Additionally, the polyamine putrescine accumulated exclusively in drought-stressed trees of this provenance. In contrast, the interior provenance FEHR showed the opposite response, i.e., drastically reduced concentrations of these amino acids. However, FEHR showed considerably increased contents of pyruvate-derived and aromatic amino acids, and also higher drought-induced levels of the antioxidants ascorbate and α-tocopherol. In response to drought, both provenances produced large amounts of carbohydrates, such as glucose and fructose, most likely as osmolytes that can readily be metabolized for protection against osmotic stress. We conclude that FEHR and SNO cope with drought stress in a provenance-specific manner: the coastal provenance SNO was mainly synthesizing N-based osmolytes, a reaction not observed in the interior provenance FEHR; instead, the latter increased the levels of scavengers of reactive oxygen species. Our results underline the importance of provenance-specific reactions to abiotic stress.

Will changes in root-zone temperature in boreal spring affect recovery of photosynthesis in Picea mariana and Populus tremuloides in a future climate?

Future climate will alter the soil cover of mosses and snow depths in the boreal forests of eastern Canada. In field manipulation experiments, we assessed the effects of varying moss and snow depths on the physiology of black spruce (Picea -mariana (Mill.) B.S.P.) and trembling aspen (Populus tremuloides Michx.) in the boreal black spruce forest of western Québec. For 1 year, naturally regenerated 10-year-old spruce and aspen were grown with one of the following treatments: additional N fertilization, addition of sphagnum moss cover, removal of mosses, delayed soil thawing through snow and hay addition, or accelerated soil thawing through springtime snow removal. Treatments that involved the addition of insulating moss or snow in the spring caused lower soil temperature, while removing moss and snow in the spring caused elevated soil temperature and thus had a warming effect. Soil warming treatments were associated with greater temperature variability. Additional soil cover, whether moss or snow, increased the rate of photosynthetic recovery in the spring. Moss and snow removal, on the other hand, had the opposite effect and lowered photosynthetic activity, especially in spruce. Maximal electron transport rate (ETR(max)) was, for spruce, 39.5% lower after moss removal than with moss addition, and 16.3% lower with accelerated thawing than with delayed thawing. Impaired photosynthetic recovery in the absence of insulating moss or snow covers was associated with lower foliar N concentrations. Both species were affected in that way, but trembling aspen generally reacted less strongly to all treatments. Our results indicate that a clear negative response of black spruce to changes in root-zone temperature should be anticipated in a future climate. Reduced moss cover and snow depth could adversely affect the photosynthetic capacities of black spruce, while having only minor effects on trembling aspen.