Genotype-dependent contribution of CBF transcription factors to long-term acclimation to high light and cool temperature.

When grown under cool temperature, winter annuals upregulate photosynthetic capacity as well as freezing tolerance. Here, the role of three cold-induced C-repeat-binding factor (CBF1-3) transcription factors in photosynthetic upregulation and freezing tolerance was examined in two Arabidopsis thaliana ecotypes originating from Italy (IT) or Sweden (SW), and their corresponding CBF1-3-deficient mutant lines it:cbf123 and sw:cbf123. Photosynthetic, morphological and freezing-tolerance phenotypes, as well as gene expression profiles, were characterized in plants grown from the seedling stage under different combinations of light level and temperature. Under high light and cool (HLC) growth temperature, a greater role of CBF1-3 in IT versus SW was evident from both phenotypic and transcriptomic data, especially with respect to photosynthetic upregulation and freezing tolerance of whole plants. Overall, features of SW were consistent with a different approach to HLC acclimation than seen in IT, and an ability of SW to reach the new homeostasis through the involvement of transcriptional controls other than CBF1-3. These results provide tools and direction for further mechanistic analysis of the transcriptional control of approaches to cold acclimation suitable for either persistence through brief cold spells or for maximisation of productivity in environments with continuous low temperatures.

Less photoprotection can be good in some genetic and environmental contexts.

Antioxidant systems modulate oxidant-based signaling networks and excessive removal of oxidants can prevent beneficial acclimation responses. Evidence from mutant, transgenic, and locally adapted natural plant systems is used to interpret differences in the capacity for antioxidation and formulate hypotheses for future inquiry. We focus on the first line of chloroplast antioxidant defense, pre-emptive thermal dissipation of excess absorbed light (monitored as nonphotochemical fluorescence quenching, NPQ) as well as on tocopherol-based antioxidation. Findings from NPQ-deficient and tocopherol-deficient mutants that exhibited enhanced biomass production and/or enhanced foliar water-transport capacity are reviewed and discussed in the context of the impact of lower levels of antioxidation on plant performance in hot/dry conditions, under cool temperature, and in the presence of biotic stress. The complexity of cellular redox-signaling networks is related to the complexity of environmental and endogenous inputs as well as to the need for intensified training and collaboration in the study of plant-environment interactions across biological sub-disciplines.

Zeaxanthin and Lutein: Photoprotectors, Anti-Inflammatories, and Brain Food.

This review compares and contrasts the role of carotenoids across the taxa of life-with a focus on the xanthophyll zeaxanthin (and its structural isomer lutein) in plants and humans. Xanthophylls' multiple protective roles are summarized, with attention to the similarities and differences in the roles of zeaxanthin and lutein in plants versus animals, as well as the role of meso-zeaxanthin in humans. Detail is provided on the unique control of zeaxanthin function in photosynthesis, that results in its limited availability in leafy vegetables and the human diet. The question of an optimal dietary antioxidant supply is evaluated in the context of the dual roles of both oxidants and antioxidants, in all vital functions of living organisms, and the profound impact of individual and environmental context.

Zeaxanthin, a Molecule for Photoprotection in Many Different Environments.

Conversion of sunlight into photochemistry depends on photoprotective processes that allow safe use of sunlight over a broad range of environmental conditions. This review focuses on the ubiquity of photoprotection associated with a group of interconvertible leaf carotenoids, the xanthophyll cycle. We survey the striking plasticity of this process observed in nature with respect to (1) xanthophyll cycle pool size, (2) degree and speed of interconversion of its components, and (3) flexibility in the association between xanthophyll cycle conversion state and photoprotective dissipation of excess excitation energy. It is concluded that the components of this system can be independently tuned with a high degree of flexibility to produce a fit for different environments with various combinations of light, temperature, and other factors. In addition, the role of genetic variation is apparent from variation in the response of different species growing side-by-side in the same environment. These findings illustrate how field studies can generate insight into the adjustable levers that allow xanthophyll cycle-associated photoprotection to support plant photosynthetic productivity and survival in environments with unique combinations of environmental factors.

Optimization of Photosynthetic Productivity in Contrasting Environments by Regulons Controlling Plant Form and Function.

We review the role of a family of transcription factors and their regulons in maintaining high photosynthetic performance across a range of challenging environments with a focus on extreme temperatures and water availability. Specifically, these transcription factors include CBFs (C-repeat binding factors) and DREBs (dehydration-responsive element-binding), with CBF/DREB1 primarily orchestrating cold adaptation and other DREBs serving in heat, drought, and salinity adaptation. The central role of these modulators in plant performance under challenging environments is based on (i) interweaving of these regulators with other key signaling networks (plant hormones and redox signals) as well as (ii) their function in integrating responses across the whole plant, from light-harvesting and sugar-production in the leaf to foliar sugar export and water import and on to the plant's sugar-consuming sinks (growth, storage, and reproduction). The example of Arabidopsisthaliana ecotypes from geographic origins with contrasting climates is used to describe the links between natural genetic variation in CBF transcription factors and the differential acclimation of plant anatomical and functional features needed to support superior photosynthetic performance in contrasting environments. Emphasis is placed on considering different temperature environments (hot versus cold) and light environments (limiting versus high light), on trade-offs between adaptations to contrasting environments, and on plant lines minimizing such trade-offs.

Effects of Foliar Redox Status on Leaf Vascular Organization Suggest Avenues for Cooptimization of Photosynthesis and Heat Tolerance.

The interaction of heat stress with internal signaling networks was investigated through Arabidopsisthaliana mutants that were deficient in either tocopherols (vte1 mutant) or non-photochemical fluorescence quenching (NPQ; npq1, npq4, and npq1 npq4 mutants). Leaves of both vte1 and npq1 npq4 mutants that developed at a high temperature exhibited a significantly different leaf vascular organization compared to wild-type Col-0. Both mutants had significantly smaller water conduits (tracheary elements) of the xylem, but the total apparent foliar water-transport capacity and intrinsic photosynthetic capacity were similarly high in mutants and wild-type Col-0. This was accomplished through a combination of more numerous (albeit narrower) water conduits per vein, and a significantly greater vein density in both mutants relative to wild-type Col-0. The similarity of the phenotypes of tocopherol-deficient and NPQ-deficient mutants suggests that leaf vasculature organization is modulated by the foliar redox state. These results are evaluated in the context of interactions between redox-signaling pathways and other key regulators of plant acclimation to growth temperature, such as the C-repeat binding factor (CBF) transcription factors, several of which were upregulated in the antioxidant-deficient mutants. Possibilities for the future manipulation of the interaction between CBF and redox-signaling networks for the purpose of cooptimizing plant productivity and plant tolerance to extreme temperatures are discussed.

Acclimation of Swedish and Italian ecotypes of Arabidopsis thaliana to light intensity.

This study addressed whether ecotypes of Arabidopsis thaliana from Sweden and Italy exhibited differences in foliar acclimation to high versus low growth light intensity, and compared CO2 uptake under growth conditions with light- and CO2-saturated intrinsic photosynthetic capacity and leaf morphological and vascular features. Differential responses between ecotypes occurred mainly at the scale of leaf architecture, with thicker leaves with higher intrinsic photosynthetic capacities and chlorophyll contents per leaf area, but no difference in photosynthetic capacity on a chlorophyll basis, in high light-grown leaves of the Swedish versus the Italian ecotype. Greater intrinsic photosynthetic capacity per leaf area in the Swedish ecotype was accompanied by a greater capacity of vascular infrastructure for sugar and water transport, but this was not associated with greater CO2 uptake rates under growth conditions. The Swedish ecotype with its thick leaves is thus constructed for high intrinsic photosynthetic and vascular flux capacity even under growth chamber conditions that may not permit full utilization of this potential. Conversely, the Swedish ecotype was less tolerant of low growth light intensity than the Italian ecotype, with smaller rosette areas and lesser aboveground biomass accumulation in low light-grown plants. Foliar vein density and stomatal density were both enhanced by high growth light intensity with no significant difference between ecotypes, and the ratio of water to sugar conduits was also similar between the two ecotypes during light acclimation. These findings add to the understanding of the foliar vasculature's role in plant photosynthetic acclimation and adaptation.

Light, temperature and tocopherol status influence foliar vascular anatomy and leaf function in Arabidopsis thaliana.

This study addressed whether the winter annual Arabidopsis thaliana can adjust foliar phloem and xylem anatomy both differentially and in parallel. In plants acclimated to hot vs cool temperature, foliar minor vein xylem-to-phloem ratio was greater, whereas xylem and phloem responded concomitantly to growth light intensity. Across all growth conditions, xylem anatomy correlated with transpiration rate, while phloem anatomy correlated with photosynthetic capacity for two plant lines (wild-type Col-0 and tocopherol-deficient vte1 mutant) irrespective of tocopherol status. A high foliar vein density (VD) was associated with greater numbers and cross-sectional areas of both xylem and phloem cells per vein as well as higher rates of both photosynthesis and transpiration under high vs low light intensities. Under hot vs cool temperature, high foliar VD was associated with a higher xylem-to-phloem ratio and greater relative rates of transpiration to photosynthesis. Tocopherol status affected development of foliar vasculature as dependent on growth environment. The most notable impact of tocopherol deficiency was seen under hot growth temperature, where the vte1 mutant exhibited greater numbers of tracheary elements (TEs) per vein, a greater ratio of TEs to sieve elements, with smaller individual sizes of TEs, and resulting similar total areas of TEs per vein and transpiration rates compared with Col-0 wild-type. These findings illustrate the plasticity of foliar vascular anatomy acclimation to growth environment resulting from independent adjustments of the vasculature's components.

Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe.

The plasticity of leaf form and function in European lines of Arabidopsis thaliana was evaluated in ecotypes from Sweden and Italy grown under contrasting (cool versus hot) temperature regimes. Although both ecotypes exhibited acclimatory adjustments, the Swedish ecotype exhibited more pronounced responses to the two contrasting temperature regimes in several characterized features. These responses included thicker leaves with higher capacities for photosynthesis, likely facilitated by a greater number of phloem cells per minor vein for the active loading and export of sugars, when grown under cool temperature as opposed to leaves with a higher vein density and a greater number of tracheary elements per minor vein, likely facilitating higher rates of transpirational water loss (and thus evaporative cooling), when grown under hot temperature with high water availability. In addition, only the Swedish ecotype exhibited reduced rosette growth and greater levels of foliar tocopherols under the hot growth temperature. These responses, and the greater responsiveness of the Swedish ecotype compared with the Italian ecotype, are discussed in the context of redox signalling networks and transcription factors, and the greater range of environmental conditions experienced by the Swedish versus the Italian ecotype during the growing season in their native habitats.

Differences in light-harvesting, acclimation to growth-light environment, and leaf structural development between Swedish and Italian ecotypes of Arabidopsis thaliana.

MAIN CONCLUSION: Leaf morphological differences have an impact on light distribution within the leaf, photosynthesis, and photoprotection in Arabidopsis thaliana ecotypes from near the limits of this species' latitudinal distribution in Europe. Leaf morphology, photosynthesis, and photoprotection were characterized in two Arabidopsis ecotypes from near the limits of this species' latitudinal distribution in Europe (63°N and 42°N). The Swedish ecotype formed thicker leaves and upregulated photosynthesis more substantially than the Italian ecotype in high-light environments. Conversely, the smaller rosette formed, and lesser aboveground biomass accumulated, by the Swedish versus the Italian ecotype in low growth-light environments is consistent with a lesser shade tolerance of the Swedish ecotype. The response of the thinner leaves of the Italian ecotype to evenly spaced daily periods of higher light against a background of otherwise non-fluctuating low light was to perform the same rate of photosynthesis with less chlorophyll, rather than exhibiting greater rates of photosynthesis. In contrast, the thicker leaves of the Swedish ecotype showed elevated photosynthetic performance in response to daily supplemental higher light periods in a low-light growth environment. These findings suggest significant self-shading in the lower depths of leaves of the Swedish ecotype by the chloroplasts residing in the upper portions of the leaf, resulting in a requirement for higher incident light to trigger photosynthetic upregulation in the lower portions of its thicker leaves. Conversely, photoprotective responses in the Italian ecotype suggest that more excess light penetrated into the lower depths of this ecotype's leaves. It is speculated that light absorption and the degree of utilization of this absorbed light inform cellular signaling networks that orchestrate leaf structural development, which, in turn, affects light distribution and the level of absorbed versus photosynthetically utilized light in a leaf.

Leaf anatomical and photosynthetic acclimation to cool temperature and high light in two winter versus two summer annuals.

Acclimation of foliar features to cool temperature and high light was characterized in winter (Spinacia oleracea L. cv. Giant Nobel; Arabidopsis thaliana (L.) Heynhold Col-0 and ecotypes from Sweden and Italy) versus summer (Helianthus annuus L. cv. Soraya; Cucurbita pepo L. cv. Italian Zucchini Romanesco) annuals. Significant relationships existed among leaf dry mass per area, photosynthesis, leaf thickness and palisade mesophyll thickness. While the acclimatory response of the summer annuals to cool temperature and/or high light levels was limited, the winter annuals increased the number of palisade cell layers, ranging from two layers under moderate light and warm temperature to between four and five layers under cool temperature and high light. A significant relationship was also found between palisade tissue thickness and either cross-sectional area or number of phloem cells (each normalized by vein density) in minor veins among all four species and growth regimes. The two winter annuals, but not the summer annuals, thus exhibited acclimatory adjustments of minor vein phloem to cool temperature and/or high light, with more numerous and larger phloem cells and a higher maximal photosynthesis rate. The upregulation of photosynthesis in winter annuals in response to low growth temperature may thus depend on not only (1) a greater volume of photosynthesizing palisade tissue but also (2) leaf veins containing additional phloem cells and presumably capable of exporting a greater volume of sugars from the leaves to the rest of the plant.

Leaf architectural, vascular and photosynthetic acclimation to temperature in two biennials.

Acclimation of leaf features to growth temperature was investigated in two biennials (whose life cycle spans summer and winter seasons) using different mechanisms of sugar loading into exporting conduits, Verbascum phoeniceum (employs sugar-synthesizing enzymes driving symplastic loading through plasmodesmatal wall pores of phloem cells) and Malva neglecta (likely apoplastic loader transporting sugar via membrane transport proteins of phloem cells). In both species, acclimation to lower temperature involved greater maximal photosynthesis rates and vein density per leaf area in close correlation with modification of minor vein cellular features. While the symplastically loading biennial exhibited adjustments in the size of minor leaf vein cells (consistent with adjustment of the level of sugar-synthesizing enzymes), the putative apoplastic biennial exhibited adjustments in the number of cells (consistent with adjustment of cell membrane area for transporter placement). This upregulation of morphological and anatomical features at lower growth temperature likely contributes to the success of both the species during the winter. Furthermore, while acclimation to low temperature involved greater leaf mass per area in both species, this resulted from greater leaf thickness in V. phoeniceum vs a greater number of mesophyll cells per leaf area in M. neglecta. Both types of adjustments presumably accommodate more chloroplasts per leaf area contributing to photosynthesis. Both biennials exhibited high foliar vein densities (particularly the solar-tracking M. neglecta), which should aid both sugar export from and delivery of water to the leaves.

Association between photosynthesis and contrasting features of minor veins in leaves of summer annuals loading phloem via symplastic versus apoplastic routes.

Foliar vascular anatomy and photosynthesis were evaluated for a number of summer annual species that either load sugars into the phloem via a symplastic route (Cucumis sativus L. cv. Straight Eight; Cucurbita pepo L. cv. Italian Zucchini Romanesco; Citrullus lanatus L. cv. Faerie Hybrid; Cucurbita pepo L. cv. Autumn Gold) or an apoplastic route (Nicotiana tabacum L.; Solanum lycopersicum L. cv. Brandywine; Gossypium hirsutum L.; Helianthus annuus L. cv. Soraya), as well as winter annual apoplastic loaders (Spinacia oleracea L. cv. Giant Nobel; Arabidopsis thaliana (L.) Heynhold Col-0, Swedish and Italian ecotypes). For all summer annuals, minor vein cross-sectional xylem area and tracheid number as well as the ratio of phloem loading cells to phloem sieve elements, each when normalized for foliar vein density (VD), was correlated with photosynthesis. These links presumably reflect (1) the xylem's role in providing water to meet foliar transpirational demand supporting photosynthesis and (2) the importance of the driving force of phloem loading as well as the cross-sectional area for phloem sap flux to match foliar photosynthate production. While photosynthesis correlated with the product of VD and cross-sectional phloem cell area among symplastic loaders, photosynthesis correlated with the product of VD and phloem cell number per vein among summer annual apoplastic loaders. Phloem cell size has thus apparently been a target of selection among symplastic loaders (where loading depends on enzyme concentration within loading cells) versus phloem cell number among apoplastic loaders (where loading depends on membrane transporter numbers).

Emerging trade-offs - impact of photoprotectants (PsbS, xanthophylls, and vitamin E) on oxylipins as regulators of development and defense.

This review summarizes evidence for a mechanistic link between plant photoprotection and the synthesis of oxylipin hormones as regulators of development and defense. Knockout mutants of Arabidopsis, deficient in various key components of the chloroplast photoprotection system, consistently produced greater concentrations of the hormone jasmonic acid or its precursor 12- oxo-phytodienoic acid (OPDA), both members of the oxylipin messenger family. Characterized plants include several mutants deficient in PsbS (an intrinsic chlorophyll-binding protein of photosystem II) or pigments (zeaxanthin and/or lutein) required for photoprotective thermal dissipation of excess excitation energy in the chloroplast and a mutant deficient in reactive oxygen detoxification via the antioxidant vitamin E (tocopherol). Evidence is also presented that certain plant defenses against herbivores or pathogens are elevated for these mutants. This evidence furthermore indicates that wild-type Arabidopsis plants possess less than maximal defenses against herbivores or pathogens, and suggest that plant lines with superior defenses against abiotic stress may have lower biotic defenses. The implications of this apparent trade-off between abiotic and biotic plant defenses for plant ecology as well as for plant breeding/engineering are explored, and the need for research further addressing this important issue is highlighted.

May photoinhibition be a consequence, rather than a cause, of limited plant productivity?

Photoinhibition in leaves in response to high and/or excess light, consisting of a decrease in photosynthesis and/or photosynthetic efficiency, is frequently equated to photodamage and often invoked as being responsible for decreased plant growth and productivity. However, a review of the literature reveals that photoinhibited leaves characterized for foliar carbohydrate levels were invariably found to possess high levels of sugars and starch. We propose that photoinhibition should be placed in the context of whole-plant source-sink regulation of photosynthesis. Photoinhibition may represent downregulation of the photosynthetic apparatus in response to excess light when (1) more sugar is produced in leaves than can be utilized by the rest of the plant and/or (2) more light energy is harvested than can be utilized by the chloroplast for the fixation of carbon dioxide into sugars.

Lemnaceae as Novel Crop Candidates for CO2 Sequestration and Additional Applications.

Atmospheric carbon dioxide (CO2) is projected to be twice as high as the pre-industrial level by 2050. This review briefly highlights key responses of terrestrial plants to elevated CO2 and compares these with the responses of aquatic floating plants of the family Lemnaceae (duckweeds). Duckweeds are efficient at removing CO2 from the atmosphere, which we discuss in the context of their exceptionally high growth rates and capacity for starch storage in green tissue. In contrast to cultivation of terrestrial crops, duckweeds do not contribute to CO2 release from soils. We briefly review how this potential for contributions to stabilizing atmospheric CO2 levels is paired with multiple additional applications and services of duckweeds. These additional roles include wastewater phytoremediation, feedstock for biofuel production, and superior nutritional quality (for humans and livestock), while requiring minimal space and input of light and fertilizer. We, furthermore, elaborate on other environmental factors, such as nutrient availability, light supply, and the presence of a microbiome, that impact the response of duckweed to elevated CO2. Under a combination of elevated CO2 with low nutrient availability and moderate light supply, duckweeds' microbiome helps maintain CO2 sequestration and relative growth rate. When incident light intensity increases (in the presence of elevated CO2), the microbiome minimizes negative feedback on photosynthesis from increased sugar accumulation. In addition, duckweed shows a clear propensity for absorption of ammonium over nitrate, accepting ammonium from their endogenous N2-fixing Rhizobium symbionts, and production of large amounts of vegetative storage protein. Finally, cultivation of duckweed could be further optimized using hydroponic vertical farms where nutrients and water are recirculated, saving both resources, space, and energy to produce high-value products.

Terrestrial and Floating Aquatic Plants Differ in Acclimation to Light Environment.

The ability of plants to respond to environmental fluctuations is supported by acclimatory adjustments in plant form and function that may require several days and development of a new leaf. We review adjustments in photosynthetic, photoprotective, and foliar vascular capacity in response to variation in light and temperature in terrestrial plants. The requirement for extensive acclimation to these environmental conditions in terrestrial plants is contrasted with an apparent lesser need for acclimation to different light environments, including rapid light fluctuations, in floating aquatic plants for the duckweed Lemna minor. Relevant features of L. minor include unusually high growth rates and photosynthetic capacities coupled with the ability to produce high levels of photoprotective xanthophylls across a wide range of growth light environments without compromising photosynthetic efficiency. These features also allow L. minor to maximize productivity and avoid problems during an abrupt experimental transfer of low-light-grown plants to high light. The contrasting responses of land plants and floating aquatic plants to the light environment further emphasize the need of land plants to, e.g., experience light fluctuations in their growth environment before they induce acclimatory adjustments that allow them to take full advantage of natural settings with such fluctuations.

Foliar Phenotypic Plasticity Reflects Adaptation to Environmental Variability.

Arabidopsis thaliana ecotypes adapted to native habitats with different daylengths, temperatures, and precipitation were grown experimentally under seven combinations of light intensity and leaf temperature to assess their acclimatory phenotypic plasticity in foliar structure and function. There were no differences among ecotypes when plants developed under moderate conditions of 400 µmol photons m-2 s-1 and 25 °C. However, in response to more extreme light or temperature regimes, ecotypes that evolved in habitats with pronounced differences in either the magnitude of changes in daylength or temperature or in precipitation level exhibited pronounced adjustments in photosynthesis and transpiration, as well as anatomical traits supporting these functions. Specifically, when grown under extremes of light intensity (100 versus 1000 µmol photons m-2 s-1) or temperature (8 °C versus 35 °C), ecotypes from sites with the greatest range of daylengths and temperature over the growing season exhibited the greatest differences in functional and structural features related to photosynthesis (light- and CO2-saturated capacity of oxygen evolution, leaf dry mass per area or thickness, phloem cells per minor vein, and water-use efficiency of CO2 uptake). On the other hand, the ecotype from the habitat with the lowest precipitation showed the greatest plasticity in features related to water transport and loss (vein density, ratio of water to sugar conduits in foliar minor veins, and transpiration rate). Despite these differences, common structure-function relationships existed across all ecotypes and growth conditions, with significant positive, linear correlations (i) between photosynthetic capacity (ranging from 10 to 110 µmol O2 m-2 s-1) and leaf dry mass per area (from 10 to 75 g m-2), leaf thickness (from 170 to 500 µm), and carbohydrate-export infrastructure (from 6 to 14 sieve elements per minor vein, from 2.5 to 8 µm2 cross-sectional area per sieve element, and from 16 to 82 µm2 cross-sectional area of sieve elements per minor vein); (ii) between transpiration rate (from 1 to 17 mmol H2O m-2 s-1) and water-transport infrastructure (from 3.5 to 8 tracheary elements per minor vein, from 13.5 to 28 µm2 cross-sectional area per tracheary element, and from 55 to 200 µm2 cross-sectional area of tracheary elements per minor vein); (iii) between the ratio of transpirational water loss to CO2 fixation (from 0.2 to 0.7 mol H2O to mmol-1 CO2) and the ratio of water to sugar conduits in minor veins (from 0.4 to 1.1 tracheary to sieve elements, from 4 to 6 µm2 cross-sectional area of tracheary to sieve elements, and from 2 to 6 µm2 cross-sectional area of tracheary elements to sieve elements per minor vein); (iv) between sugar conduits and sugar-loading cells; and (v) between water conducting and sugar conducting cells. Additionally, the proportion of water conduits to sugar conduits was greater for all ecotypes grown experimentally under warm-to-hot versus cold temperature. Thus, developmental acclimation to the growth environment included ecotype-dependent foliar structural and functional adjustments resulting in multiple common structural and functional relationships.

Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons.

Modulation of the efficiency with which leaves convert absorbed light to photochemical energy [intrinsic efficiency of open photosystem II (PSII) centers, as the ratio of variable to maximal chlorophyll fluorescence] as well as leaf xanthophyll composition (interconversions of the xanthophyll cycle pigments violaxanthin and zeaxanthin) were characterized throughout single days and nights to entire seasons in plants growing naturally in contrasting light and temperature environments. All pronounced decreases of intrinsic PSII efficiency took place in the presence of zeaxanthin. The reversibility of these PSII efficiency changes varied widely, ranging from reversible-within-seconds (in a vine experiencing multiple sunflecks under a eucalypt canopy) to apparently permanently locked-in for entire seasons (throughout the whole winter in a subalpine conifer forest at 3,000 m). While close association between low intrinsic PSII efficiency and zeaxanthin accumulation was ubiquitous, accompanying features (such as trans-thylakoid pH gradient, thylakoid protein composition, and phosphorylation) differed among contrasting conditions. The strongest and longest-lasting depressions in intrinsic PSII efficiency were seen in the most stress-tolerant species. Evergreens, in particular, showed the most pronounced modulation of PSII efficiency and thermal dissipation, and are therefore suggested as model species for the study of photoprotection. Implications of the responses of field-grown plants in nature for mechanistic models are discussed.

Low temperature acclimation of photosynthetic capacity and leaf morphology in the context of phloem loading type.

Carbon export from leaf mesophyll to sugar-transporting phloem occurs via either an apoplastic (across the cell membrane) or symplastic (through plasmodesmatal cell wall openings) pathway. Herbaceous apoplastic loaders generally exhibit an up-regulation of photosynthetic capacity in response to growth at lower temperature. However, acclimation of photosynthesis to temperature by symplastically loading species, whose geographic distribution is particularly strong in tropical and subtropical areas, has not been characterized. Photosynthetic and leaf anatomical acclimation to lower temperature was explored in two symplastic (Verbascum phoeniceum, Cucurbita pepo) and two apoplastic (Helianthus annuus, Spinacia oleracea) loaders, representing summer- and winter-active life histories for each loading type. Regardless of phloem loading type, the two summer-active species, C. pepo and H. annuus, exhibited neither foliar anatomical nor photosynthetic acclimation when grown under low temperature compared to moderate temperature. In contrast, and again irrespective of phloem loading type, the two winter-active mesophytes, V. phoeniceum and S. oleracea, exhibited both a greater number of palisade cell layers (and thus thicker leaves) and significantly higher maximal capacities of photosynthetic electron transport, as well as, in the case of V. phoeniceum, a greater foliar vein density in response to cool temperatures compared to growth at moderate temperature. It is therefore noteworthy that symplastic phloem loading per se does not prevent acclimation of intrinsic photosynthetic capacity to cooler growth temperatures. Given the vagaries of weather and climate, understanding the basis of plant acclimation to, and tolerance of, low temperature is critical to maintaining and increasing plant productivity for food, fuel, and fiber to meet the growing demands of a burgeoning human population.