29 results on '"Jared J. Stewart"'
Search Results
2. Distinct Cold Acclimation of Productivity Traits in
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Barbara, Demmig-Adams, Stephanie K, Polutchko, Christopher R, Baker, Jared J, Stewart, and William W, Adams Iii
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Cold Temperature ,Ecotype ,Acclimatization ,Arabidopsis ,Photosynthesis - Abstract
Improvement of crop climate resilience will require an understanding of whole-plant adaptation to specific local environments. This review places features of plant form and function related to photosynthetic productivity, as well as associated gene-expression patterns, into the context of the adaptation of
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- 2022
3. Growth and Nutritional Quality of Lemnaceae Viewed Comparatively in an Ecological and Evolutionary Context
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Barbara Demmig-Adams, Marina López-Pozo, Stephanie K. Polutchko, Paul Fourounjian, Jared J. Stewart, Madeleine C. Zenir, and William W. Adams
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lutein ,Ecology ,chlorophyll fluorescence ,fungi ,Botany ,electron transport chain ,photosystem ,food and beverages ,Plant Science ,Review ,inflammation ,relative growth rate ,QK1-989 ,Ecology, Evolution, Behavior and Systematics ,photosynthetic capacity - Abstract
This review focuses on recently characterized traits of the aquatic floating plant Lemna with an emphasis on its capacity to combine rapid growth with the accumulation of high levels of the essential human micronutrient zeaxanthin due to an unusual pigment composition not seen in other fast-growing plants. In addition, Lemna’s response to elevated CO2 was evaluated in the context of the source–sink balance between plant sugar production and consumption. These and other traits of Lemnaceae are compared with those of other floating aquatic plants as well as terrestrial plants adapted to different environments. It was concluded that the unique features of aquatic plants reflect adaptations to the freshwater environment, including rapid growth, high productivity, and exceptionally strong accumulation of high-quality vegetative storage protein and human antioxidant micronutrients. It was further concluded that the insensitivity of growth rate to environmental conditions and plant source–sink imbalance may allow duckweeds to take advantage of elevated atmospheric CO2 levels via particularly strong stimulation of biomass production and only minor declines in the growth of new tissue. It is proposed that declines in nutritional quality under elevated CO2 (due to regulatory adjustments in photosynthetic metabolism) may be mitigated by plant–microbe interaction, for which duckweeds have a high propensity. This work was funded by the Translational Research Institute for Space Health through Cooperative Agreement NNX16AO69A, the National Science Foundation award number IOS-1907338, and the University of Colorado.
- Published
- 2021
4. Genotype-dependent contribution of CBF transcription factors to long-term acclimation to high light and cool temperature
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Krishna K. Niyogi, William W. Adams, Cynthia L. Amstutz, Jeffrey Johnson, Jared J. Stewart, Christopher R. Baker, Barbara Demmig-Adams, and Lindsey G. Ching
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Ecotype ,Genotype ,Light ,Physiology ,Arabidopsis Proteins ,Acclimatization ,Arabidopsis ,Plant Science ,Biology ,biology.organism_classification ,Photosynthesis ,Photosynthetic capacity ,Cold Temperature ,Seedling ,Photosynthetic acclimation ,Botany ,Cold acclimation ,Trans-Activators ,Arabidopsis thaliana ,Transcription Factors - Abstract
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 seedling stage under different combinations of light level and temperature. Under high light and cool growth temperature (HLC), 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 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 maximization of productivity in environments with continuous low temperatures. This article is protected by copyright. All rights reserved.
- Published
- 2021
5. Photosynthesis and foliar vascular adjustments to growth light intensity in summer annual species with symplastic and apoplastic phloem loading
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Barbara Demmig-Adams, Jared J. Stewart, Stephanie K. Polutchko, and William W. Adams
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Light ,Physiology ,fungi ,food and beverages ,Xylem ,Plant Science ,Biology ,Phloem ,Photosynthesis ,Photosynthetic capacity ,Sunflower ,Apoplast ,Plant Leaves ,Horticulture ,Light intensity ,Cucurbita ,Ocimum basilicum ,Composition (visual arts) ,Seasons ,Cucumis sativus ,Sugars ,Agronomy and Crop Science - Abstract
Concomitant adjustments in photosynthetic capacity and size, composition, and/or density of minor foliar veins in response to growth environment were previously described primarily for winter annuals that load sugars into foliar phloem apoplastically. Here, common trends, differences associated with phloem-loading mechanism, and species-dependent differences are identified for summer annuals (loading sugars either symplastically [cucumber, pumpkin, and basil] or apoplastically [tomato and sunflower]) that were grown in low and high light. Photosynthetic capacity per leaf area was significantly positively correlated with leaf-level volume of phloem-loading cells (LCs), sugar-export conduits (sieve elements), and water conduits (tracheary elements) irrespective of phloem-loading mechanism. The relative contribution to leaf-level volume of LC numbers versus individual LC size was greater in apoplastic loaders than in symplastic loaders. Species-dependent differences included different vein density within each loading group and either greater or lower numbers of cells per minor vein (especially of tracheary elements in the symplastic loaders basil versus cucumber, respectively), which may be due to genetic adaptation to different environmental conditions. These results indicate considerable plasticity in foliar vascular features in summer annuals as well as some loading-mechanism-dependent trends.
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- 2021
6. Distinct Cold Acclimation of Productivity Traits in Arabidopsis thaliana Ecotypes
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Barbara Demmig-Adams, Stephanie K. Polutchko, Christopher R. Baker, Jared J. Stewart, and William W. Adams III
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Inorganic Chemistry ,fungi ,Organic Chemistry ,food and beverages ,General Medicine ,Physical and Theoretical Chemistry ,Molecular Biology ,Spectroscopy ,Catalysis ,Computer Science Applications - Abstract
Improvement of crop climate resilience will require an understanding of whole-plant adaptation to specific local environments. This review places features of plant form and function related to photosynthetic productivity, as well as associated gene-expression patterns, into the context of the adaptation of Arabidopsis thaliana ecotypes to local environments with different climates in Sweden and Italy. The growth of plants under common cool conditions resulted in a proportionally greater emphasis on the maintenance of photosynthetic activity in the Swedish ecotype. This is compared to a greater emphasis on downregulation of light-harvesting antenna size and upregulation of a host of antioxidant enzymes in the Italian ecotype under these conditions. This differential response is discussed in the context of the climatic patterns of the ecotypes’ native habitats with substantial opportunity for photosynthetic productivity under mild temperatures in Italy but not in Sweden. The Swedish ecotype’s response is likened to pushing forward at full speed with productivity under low temperature versus the Italian ecotype’s response of staying safe from harm (maintaining redox homeostasis) while letting productivity decline when temperatures are transiently cold. It is concluded that either strategy can offer directions for the development of climate-resilient crops for specific locations of cultivation.
- Published
- 2022
7. Foliar sieve elements: Nexus of the leaf
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William W. Adams III, Jared J. Stewart, Stephanie K. Polutchko, and Barbara Demmig-Adams
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Plant Leaves ,Physiology ,Carbohydrates ,Carbohydrate Metabolism ,Plant Science ,Phloem ,Photosynthesis ,Plants ,Agronomy and Crop Science - Abstract
In this review, a central position of foliar sieve elements in linking leaf structure and function is explored. Results from studies involving plants grown under, and acclimated to, different growth regimes are used to identify significant, linear relationships between features of minor vein sieve elements and those of 1) leaf photosynthetic capacity that drives sugar synthesis, 2) overall leaf structure that serves as the platform for sugar production, 3) phloem components that facilitate the loading of sugars (companionphloem parenchyma cells), and 4) the tracheary elements that import water to support photosynthesis (and stomatal opening) as well as mass flow of sugars out of the leaf. Despite comprising only a small fraction of physical space within the leaf, sieve elements represent a hub through which multiple functions of the leaf intersect. As the conduits for export of energy-rich carbohydrates, essential mineral nutrients, and information carriers, sieve elements play a central role in fueling and orchestrating development and function of the plant as well as, by extension, of natural and human communities that depend on plants as producers and partners in the global carbon cycle.
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- 2022
8. Growth and Essential Carotenoid Micronutrients in Lemna gibba as a Function of Growth Light Intensity
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Jared J. Stewart, William W. Adams, Marina López-Pozo, Barbara Demmig-Adams, and Christine M. Escobar
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0106 biological sciences ,energy dissipation ,duckweed ,Lemna gibba ,Plant Science ,lcsh:Plant culture ,Photosynthesis ,01 natural sciences ,03 medical and health sciences ,chemistry.chemical_compound ,Nutrient ,lcsh:SB1-1110 ,human nutrition ,Carotenoid ,030304 developmental biology ,chemistry.chemical_classification ,0303 health sciences ,photosynthesis ,biology ,food and beverages ,biology.organism_classification ,co-optimization ,Zeaxanthin ,photoprotection ,Light intensity ,Horticulture ,chemistry ,Chlorophyll ,Photoprotection ,010606 plant biology & botany - Abstract
Duckweed is a promising food crop with multiple benefits for space applications. Fresh duckweed could deliver synergistically acting essential antioxidant nutrients to a crew – but only if growth conditions provide the plant with the right cues to trigger antioxidant formation. We grew Lemna gibba under continuous growth light ranging from low to very high intensities (photosynthetic photon flux densities = PPFDs) in order to investigate the effect on plant growth, photosynthesis, and level of carotenoid antioxidants that are essential human micronutrients. Lemna gibba achieved remarkably high growth rates under modest growth PPFD by virtue of superior light absorption resulting from minimal self-shading and high chlorophyll levels. Conversely, L. gibba’s growth rate remained high even under very high growth PPFDs. This notable ability of L. gibba to avoid inactivation of photosynthesis and diminished growth under very high growth PPFDs resulted from a combination of downregulation of chlorophyll synthesis and increased biochemical photoprotection that limited a build-up of excessive excitation energy. This biochemical photoprotection included accumulation of zeaxanthin (an essential human micronutrient) and high levels of zeaxanthin-catalyzed thermal energy dissipation of excess excitation. Compared to the light levels needed to saturate L. gibba photosynthesis and growth, higher light levels were thus required for strong induction of the essential antioxidant zeaxanthin. These results indicate a need for design of light protocols that achieve simultaneous optimization of plant yield, nutritional quality, and light-use efficiency to circumvent the fact that the light requirement to saturate plant growth is lower than that for production of high zeaxanthin levels. How this trade-off between light-use efficiency of growth and nutritional quality might be minimized or circumvented to co-optimize all desired features is discussed.
- Published
- 2020
9. Growth and Essential Carotenoid Micronutrients in
- Author
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Jared J, Stewart, William W, Adams, Christine M, Escobar, Marina, López-Pozo, and Barbara, Demmig-Adams
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co-optimization ,spaceflight ,energy dissipation ,photoprotection ,photosynthesis ,zeaxanthin ,duckweed ,food and beverages ,Plant Science ,human nutrition ,Original Research - Abstract
Duckweed is a promising food crop with multiple benefits for space applications. Fresh duckweed could deliver synergistically acting essential antioxidant nutrients to a crew – but only if growth conditions provide the plant with the right cues to trigger antioxidant formation. We grew Lemna gibba under continuous growth light ranging from low to very high intensities (photosynthetic photon flux densities = PPFDs) in order to investigate the effect on plant growth, photosynthesis, and level of carotenoid antioxidants that are essential human micronutrients. Lemna gibba achieved remarkably high growth rates under modest growth PPFD by virtue of superior light absorption resulting from minimal self-shading and high chlorophyll levels. Conversely, L. gibba’s growth rate remained high even under very high growth PPFDs. This notable ability of L. gibba to avoid inactivation of photosynthesis and diminished growth under very high growth PPFDs resulted from a combination of downregulation of chlorophyll synthesis and increased biochemical photoprotection that limited a build-up of excessive excitation energy. This biochemical photoprotection included accumulation of zeaxanthin (an essential human micronutrient) and high levels of zeaxanthin-catalyzed thermal energy dissipation of excess excitation. Compared to the light levels needed to saturate L. gibba photosynthesis and growth, higher light levels were thus required for strong induction of the essential antioxidant zeaxanthin. These results indicate a need for design of light protocols that achieve simultaneous optimization of plant yield, nutritional quality, and light-use efficiency to circumvent the fact that the light requirement to saturate plant growth is lower than that for production of high zeaxanthin levels. How this trade-off between light-use efficiency of growth and nutritional quality might be minimized or circumvented to co-optimize all desired features is discussed.
- Published
- 2020
10. Tocopherols modulate leaf vein arrangement and composition without impacting photosynthesis
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Barbara Demmig-Adams, William W. Adams, Jared J. Stewart, and Christopher M. Cohu
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0106 biological sciences ,0301 basic medicine ,biology ,Physiology ,fungi ,Wild type ,food and beverages ,Xylem ,Plant physiology ,Plant Science ,Photosynthesis ,biology.organism_classification ,01 natural sciences ,Photosynthetic capacity ,03 medical and health sciences ,030104 developmental biology ,Botany ,Parenchyma ,Arabidopsis thaliana ,Phloem ,010606 plant biology & botany - Abstract
Growth of the tocopherol-deficient vte1 mutant and Col-0 wild type of Arabidopsis thaliana in a sunlit glasshouse revealed both similarities and differences between genotypes. Photosynthetic capacity and leaf mesophyll features did not differ between mutant and wild type. Likewise, the total volume of water conduits (tracheary elements, TEs), sugar conduits (sieve elements, SEs), and sugar-loading cells (companion and phloem parenchyma cells) on a leaf area basis were unaffected by tocopherol deficiency. However, tocopherol deficiency yielded smaller and more numerous minor veins with fewer phloem cells and smaller TEs, resulting in greater ratios of TEs to SEs. The smaller TEs in the vte1 mutant may present a decreased risk for cavitation under high evaporative demand or in response to freezing. In turn, compensation for fewer phloem cells and smaller TEs by more numerous veins may bolster resistance to cavitation at no cost to photosynthetic capacity.
- Published
- 2018
11. Evaluating the link between photosynthetic capacity and leaf vascular organization with principal component analysis
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William W. Adams, Jared J. Stewart, Stephanie K. Polutchko, and Barbara Demmig-Adams
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0106 biological sciences ,0301 basic medicine ,Phloem loading ,Physiology ,Chemistry ,fungi ,food and beverages ,Plant physiology ,Xylem ,Membrane Transporters ,Plant Science ,01 natural sciences ,Photosynthetic capacity ,Apoplast ,03 medical and health sciences ,030104 developmental biology ,Botany ,Principal component analysis ,Phloem ,010606 plant biology & botany - Abstract
Significant linear relationships between photosynthetic capacity and principal components loaded by phloem cell numbers and tracheary elements per minor vein as well as the latter two normalized for vein density (proxy for apoplastic phloem loading capacity involving membrane transporters) were revealed for all apoplastic loaders (summer annuals and winter annual Arabidopsis thaliana). In addition, significant linear relationships between photosynthetic capacity and a principal component loaded by tracheary element cross-sectional areas and volumes per unit of leaf area (water flux capacity proxy) was present for symplastic and apoplastic loaders. Lastly, a significant linear relationship between photosynthetic capacity and a principal component loaded by phloem cell cross-sectional areas and volumes per unit of leaf area (proxy for symplastic loading capacity involving cytosolic enzymes for companion cells) was revealed for summer annual symplastic loaders as well as for A. thaliana (in the case of sieve elements, a proxy for sugar export capacity from the leaves).
- Published
- 2018
12. Features of the Duckweed Lemna That Support Rapid Growth under Extremes of Light Intensity
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Jared J. Stewart, Barbara Demmig-Adams, Marina López-Pozo, William W. Adams, Naiara Doherty Garcia, Christine M. Escobar, and Maureen McNamara
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0106 biological sciences ,0301 basic medicine ,Light ,Perennial plant ,QH301-705.5 ,Acclimatization ,Lemna gibba ,Population ,Biology ,01 natural sciences ,Article ,03 medical and health sciences ,Malva ,Botany ,Araceae ,Biology (General) ,education ,photochemical efficiency ,Shade tolerance ,education.field_of_study ,Lemna ,chlorophyll fluorescence ,carotenoids ,food and beverages ,xanthophyll cycle ,Pigments, Biological ,General Medicine ,tocopherol ,biology.organism_classification ,Plant Leaves ,Light intensity ,antioxidants ,zeaxanthin ,030104 developmental biology ,Malva neglecta ,protein ,010606 plant biology & botany - Abstract
This study addresses the unique functional features of duckweed via comparison of Lemna gibba grown under controlled conditions of 50 versus 1000 µmol photons m−2 s−1 and of a L. minor population in a local pond with a nearby population of the biennial weed Malva neglecta. Principal component analysis of foliar pigment composition revealed that Malva was similar to fast-growing annuals, while Lemna was similar to slow-growing evergreens. Overall, Lemna exhibited traits reminiscent of those of its close relatives in the family Araceae, with a remarkable ability to acclimate to both deep shade and full sunlight. Specific features contributing to duckweed’s shade tolerance included a foliar pigment composition indicative of large peripheral light-harvesting complexes. Conversely, features contributing to duckweed’s tolerance of high light included the ability to convert a large fraction of the xanthophyll cycle pool to zeaxanthin and dissipate a large fraction of absorbed light non-photochemically. Overall, duckweed exhibited a combination of traits of fast-growing annuals and slow-growing evergreens with foliar pigment features that represented an exaggerated version of that of terrestrial perennials combined with an unusually high growth rate. Duckweed’s ability to thrive under a wide range of light intensities can support success in a dynamic light environment with periodic cycles of rapid expansion.
- Published
- 2021
13. Environmental regulation of intrinsic photosynthetic capacity: an integrated view
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Jared J. Stewart, Barbara Demmig-Adams, and William W. Adams
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0106 biological sciences ,0301 basic medicine ,High rate ,Chloroplasts ,Ecotype ,Ecology ,fungi ,food and beverages ,Vascular transport ,Plant Science ,Carbon Dioxide ,Biology ,Photosynthesis ,01 natural sciences ,Photosynthetic capacity ,Plant Leaves ,Chloroplast ,03 medical and health sciences ,030104 developmental biology ,Environmental regulation ,010606 plant biology & botany - Abstract
Environmental modulation of photosynthetic capacity is reviewed in the context of its assessment and its regulation, genetic differences among species and ecotypes, and links to plant stress tolerance and productivity. Modulation of intrinsic photosynthetic capacity matches investment in photosynthetic components to opportunity for CO2 uptake and productivity in specific environments, with exceptionally high rates during particularly narrow windows of opportunity. Response varies among species and ecotypes and should be evaluated on multiple reference bases as well as chloroplast, leaf, and whole plant scales. Photosynthetic capacity, total foliar vascular transport capacity, and plant sink strength are modulated in concert. Switching among alternative target sinks and alternative foliar vascular architectures may provide avenues for co-optimization of productivity and stress tolerance.
- Published
- 2017
14. Algal glycerol accumulation and release as a sink for photosynthetic electron transport
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Jared J. Stewart, Barbara Demmig-Adams, Tyson A. Burch, Evan L. Savage, and William W. Adams
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0106 biological sciences ,0301 basic medicine ,biology ,Chlamydomonas ,biology.organism_classification ,Photosynthesis ,01 natural sciences ,Salinity ,03 medical and health sciences ,chemistry.chemical_compound ,Light intensity ,030104 developmental biology ,Algae ,chemistry ,Bioenergy ,Botany ,Osmoregulation ,Glycerol ,Agronomy and Crop Science ,010606 plant biology & botany - Abstract
Responses of freshwater and marine species of Chlamydomonas to salinity and light intensity were compared in the context of potential biomaterial and bioenergy production. While the freshwater species C. reinhardtii arrested growth at a salinity of 0.2 M NaCl, the marine species C. euryale showed vigorous growth and high levels of internal glycerol accumulation between 0.2 and 2 M NaCl. The freshwater species exhibited no downregulation of photosynthesis between 0 and 0.2 M NaCl; the marine species exhibited significant upregulation of photosynthesis between 0.2 and 2.0 M NaCl, indicating that internal glycerol, unlike sugars, does not induce photosynthetic downregulation. The freshwater species released considerably more glycerol than the marine species at the common salinity of 0.2 M NaCl, suggesting either possible limitations in the freshwater species to internal retention of glycerol as an osmoregulant, or formation and active release of high glycerol levels as a sink for photosynthetic electron transport when growth is not available as a sink. Continuous release of glycerol into the medium, or internal glycerol accumulation followed by periodic glycerol release via hypo-osmotic shock, are attractive potential options for continuous production of biomaterials and bioenergy from renewable sources in algae with high rates of solar energy conversion to photosynthetically produced energy carriers.
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- 2017
15. Quantification of Leaf Phloem Anatomical Features with Microscopy
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Jared J, Stewart, Onno, Muller, Christopher M, Cohu, Barbara, Demmig-Adams, and William W, Adams
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Plant Leaves ,Microscopy ,Cell Wall ,Histocytochemistry ,Carbohydrates ,Biological Transport ,Phloem ,Photosynthesis - Abstract
Measurements of vein density and foliar minor vein phloem cell numbers, minor vein phloem cell sizes, and transfer cell wall ingrowths provide quantitative proxies for the leaf's capacities to load and export photosynthates. While overall infrastructural capacity for sugar loading and sugar export correlated positively and closely with photosynthetic capacity, the specific targets of the adjustment of minor vein organization varied with phloem-loading mechanism, plant life-cycle characteristics, and environmental growth conditions. Among apoplastic loaders, for which sugar loading into the phloem depends on cell membrane-spanning transport proteins, variation in minor vein density, phloem cell number, and level of cell wall ingrowth (when present) were consistently associated with photosynthetic capacity. Among active symplastic loaders, for which sugar loading into the phloem depends on cytosolic enzymes, variation in vein density and phloem cell size were consistently associated with photosynthetic capacity. All of these anatomical features were also subject to acclimatory adjustment depending on species and environmental conditions, with increased levels of these features supporting higher rates of photosynthesis. We present a procedure for the preparation of leaf tissue for minor vein analysis, using both light and transmission electron microscopy, that facilitates quantification of not only phloem features but also xylem features that provide proxies for foliar water import capacity.
- Published
- 2019
16. Quantification of Leaf Phloem Anatomical Features with Microscopy
- Author
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William W. Adams, Jared J. Stewart, Christopher M. Cohu, Barbara Demmig-Adams, and Onno Muller
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0106 biological sciences ,0301 basic medicine ,Chemistry ,fungi ,food and beverages ,Xylem ,Transfer cell ,Photosynthesis ,01 natural sciences ,Photosynthetic capacity ,Apoplast ,Cell wall ,03 medical and health sciences ,030104 developmental biology ,Biophysics ,Phloem ,Sugar ,010606 plant biology & botany - Abstract
Measurements of vein density and foliar minor vein phloem cell numbers, minor vein phloem cell sizes, and transfer cell wall ingrowths provide quantitative proxies for the leaf's capacities to load and export photosynthates. While overall infrastructural capacity for sugar loading and sugar export correlated positively and closely with photosynthetic capacity, the specific targets of the adjustment of minor vein organization varied with phloem-loading mechanism, plant life-cycle characteristics, and environmental growth conditions. Among apoplastic loaders, for which sugar loading into the phloem depends on cell membrane-spanning transport proteins, variation in minor vein density, phloem cell number, and level of cell wall ingrowth (when present) were consistently associated with photosynthetic capacity. Among active symplastic loaders, for which sugar loading into the phloem depends on cytosolic enzymes, variation in vein density and phloem cell size were consistently associated with photosynthetic capacity. All of these anatomical features were also subject to acclimatory adjustment depending on species and environmental conditions, with increased levels of these features supporting higher rates of photosynthesis. We present a procedure for the preparation of leaf tissue for minor vein analysis, using both light and transmission electron microscopy, that facilitates quantification of not only phloem features but also xylem features that provide proxies for foliar water import capacity.
- Published
- 2019
17. Zeaxanthin, a Molecule for Photoprotection in Many Different Environments
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Barbara Demmig-Adams, William W. Adams, Jared J. Stewart, Stephanie K. Polutchko, and Marina López-Pozo
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0106 biological sciences ,energy dissipation ,Lutein ,Phytochemicals ,Pharmaceutical Science ,Review ,Environment ,Protective Agents ,Photosynthesis ,01 natural sciences ,Analytical Chemistry ,lcsh:QD241-441 ,03 medical and health sciences ,chemistry.chemical_compound ,lcsh:Organic chemistry ,Zeaxanthins ,Drug Discovery ,violaxanthin ,Nutritional Physiological Phenomena ,human nutrition ,Physical and Theoretical Chemistry ,Weather ,Plant Physiological Phenomena ,030304 developmental biology ,chemistry.chemical_classification ,Flexibility (engineering) ,lutein ,0303 health sciences ,chlorophyll fluorescence ,Non-photochemical quenching ,Organic Chemistry ,xanthophyll cycle ,Carotenoids ,carotenoid ,Biosynthetic Pathways ,Plant Leaves ,Zeaxanthin ,photoprotection ,chemistry ,Chemistry (miscellaneous) ,Photoprotection ,Xanthophyll ,Sunlight ,Molecular Medicine ,Biological system ,non-photochemical quenching ,010606 plant biology & botany ,Violaxanthin - Abstract
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.
- Published
- 2020
18. Leaf Vasculature and the Upper Limit of Photosynthesis
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Barbara Demmig-Adams, William W. Adams, Jared J. Stewart, and Stephanie K. Polutchko
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0106 biological sciences ,0301 basic medicine ,education.field_of_study ,fungi ,Population ,food and beverages ,Xylem ,Biology ,Photosynthesis ,biology.organism_classification ,01 natural sciences ,Acclimatization ,Photosynthetic capacity ,03 medical and health sciences ,030104 developmental biology ,Botany ,Arabidopsis thaliana ,Phloem ,education ,010606 plant biology & botany ,Transpiration - Abstract
The foliar vascular network is responsible for (1) structural support of the lamina as a platform for absorbing photons of light to drive photosynthesis, (2) transfer of information carriers like hormones and other signaling molecules between the leaf and other parts of the plant, (3) distribution of water and nutrients to leaf tissues via the xylem, and (4) movement of photosynthetic products, as well as chemical components remobilized during senescence, from mesophyll tissue into the phloem, and from source leaves to the plant’s many sinks. Foliar venation is thus central to the leaf’s primary role as a photosynthetic organ. Positive relationships between hydraulic conductance of the xylem, foliar vein density, and photosynthesis have been studied, and close links between foliar phloem capacity and intrinsic photosynthetic capacity were identified more recently. In this chapter, the relationship between various features of the foliar vasculature and photosynthetic capacity in mesophytic species with high rates of photosynthesis is explored. These metrics include foliar vein density, numbers and/or cross-sectional areas of xylem, phloem, and companion (including intermediary) cells, tracheary and sieve elements, and expansion of cell membrane area due to cell wall ingrowths in phloem transfer cells. Total xylem conduit volume per leaf area (the product of vein density and xylem cell metrics) of minor foliar veins exhibited a strong positive relationship with photosynthetic capacity per leaf area among multiple summer annuals. In the winter annual Arabidopsis thaliana, acclimation to contrasting growth temperatures involves differential acclimation of photosynthesis versus transpiration and is matched by similar differential acclimation of phloem versus xylem features. Photosynthetic capacity was positively correlated with various phloem metrics among all species and conditions examined, including summer annuals, winter annuals, and biennial species under various temperature and light conditions during growth. Given the essential role of vasculature in leaf functioning, it is not surprising that foliar vascular metrics are adjusted in response to environmental conditions (temperature, light levels, etc.). The vascular grid of the leaf and its xylem and phloem components thus underlies efficient leaf and plant functioning by facilitating the exchange of water, nutrients, and energy and information carriers between photosynthetic and non-photosynthetic parts of the plant. Recognition of this centrality of the foliar vasculature is critical to the effective selection, breeding, and engineering of crop plants to meet the nutritional, energy, fiber, material, and pharmaceutical needs of an expanding human population.
- Published
- 2018
19. Photosynthetic Modulation in Response to Plant Activity and Environment
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William W. Adams, Jared J. Stewart, and Barbara Demmig-Adams
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0106 biological sciences ,0301 basic medicine ,03 medical and health sciences ,030104 developmental biology ,Modulation ,Biophysics ,Biology ,Photosynthesis ,01 natural sciences ,010606 plant biology & botany - Published
- 2018
20. Acclimation of Swedish and Italian ecotypes of Arabidopsis thaliana to light intensity
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William W. Adams, Jared J. Stewart, Stephanie K. Polutchko, and Barbara Demmig-Adams
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0106 biological sciences ,0301 basic medicine ,Light ,Acclimatization ,Arabidopsis ,Plant Science ,Biology ,Photosynthesis ,01 natural sciences ,Biochemistry ,03 medical and health sciences ,chemistry.chemical_compound ,Botany ,Sweden ,Water transport ,Ecotype ,food and beverages ,Cell Biology ,General Medicine ,Carbon Dioxide ,Photosynthetic capacity ,Plant Leaves ,Light intensity ,030104 developmental biology ,chemistry ,Italy ,Photosynthetic acclimation ,Chlorophyll ,010606 plant biology & botany - Abstract
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.
- Published
- 2017
21. Insights from Placing Photosynthetic Light Harvesting into Context
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Barbara Demmig-Adams, Tyson A. Burch, Jared J. Stewart, and William W. Adams
- Subjects
business.industry ,Computer science ,Nanotechnology ,Context (language use) ,Photosynthesis ,Photon yield ,Food chain ,General Materials Science ,Biochemical engineering ,Physical and Theoretical Chemistry ,Maximal rate ,business ,Function (biology) ,Downstream (petroleum industry) - Abstract
Solar-energy conversion through natural photosynthesis forms the base of virtually all food chains on Earth and provides fiber, materials, and fuels, as well as inspiration for the design of biomimetic energy-conversion systems. We summarize well-known as well as recently discovered feedback loops between natural light-harvesting systems and whole-organism function in natural settings. We propose that the low effective quantum yield of natural light-harvesting systems in high light is caused by downstream limitations rather than unavoidable intrinsic vulnerabilities. We evaluate potential avenues, and their costs and benefits, for increasing the maximal rate and photon yield of photosynthesis in high light in plants and photosynthetic microbes. By summarizing mechanisms observable only in complex systems (whole plants, algae, or, in some cases, intact leaves), we aim to stimulate future research efforts on reciprocal feedback loops between light harvesting and downstream processes in whole organisms and to provide additional arguments for the significance of research on photosynthetic light harvesting.
- Published
- 2014
22. Association between photosynthesis and contrasting features of minor veins in leaves of summer annuals loading phloem via symplastic versus apoplastic routes
- Author
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Johanna A. Protheroe, Barbara Demmig-Adams, Christopher M. Cohu, William W. Adams, Jared J. Stewart, and Onno Muller
- Subjects
Citrullus lanatus ,Physiology ,Temperature ,Xylem ,Biological Transport ,Cell Biology ,Plant Science ,General Medicine ,Phloem ,Biology ,biology.organism_classification ,Photosynthesis ,Apoplast ,Oxygen ,Plant Leaves ,Magnoliopsida ,Cucurbita pepo ,Tracheid ,Botany ,Helianthus annuus ,Genetics ,Plant Proteins - Abstract
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).
- Published
- 2014
23. Light, temperature and tocopherol status influence foliar vascular anatomy and leaf function in Arabidopsis thaliana
- Author
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Jared J. Stewart, Stephanie K. Polutchko, William W. Adams, Christopher M. Cohu, Coleman A. Wenzl, and Barbara Demmig-Adams
- Subjects
0106 biological sciences ,0301 basic medicine ,Light ,Physiology ,Arabidopsis ,Tocopherols ,Plant Science ,Photosynthesis ,01 natural sciences ,Acclimatization ,03 medical and health sciences ,Botany ,Genetics ,Arabidopsis thaliana ,Transpiration ,biology ,fungi ,Temperature ,food and beverages ,Xylem ,Cell Biology ,General Medicine ,biology.organism_classification ,Photosynthetic capacity ,Plant Leaves ,Light intensity ,030104 developmental biology ,Phloem ,010606 plant biology & botany - Abstract
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.
- Published
- 2016
24. Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe
- Author
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Jared J. Stewart, Christopher M. Cohu, Barbara Demmig-Adams, Coleman A. Wenzl, William W. Adams, and Onno Muller
- Subjects
0106 biological sciences ,0301 basic medicine ,Physiology ,Arabidopsis ,Growing season ,Tocopherols ,Context (language use) ,Plant Science ,01 natural sciences ,Hot Temperature ,03 medical and health sciences ,Botany ,Arabidopsis thaliana ,Transpiration ,Sweden ,Ecotype ,biology ,Temperature ,Xylem ,Plant Transpiration ,biology.organism_classification ,Plant Leaves ,030104 developmental biology ,Italy ,Phloem ,Plant Vascular Bundle ,010606 plant biology & botany - Abstract
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.
- Published
- 2015
25. Differences in light-harvesting, acclimation to growth-light environment, and leaf structural development between Swedish and Italian ecotypes of Arabidopsis thaliana
- Author
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Elizabeth Lombardi, William W. Adams, Jared J. Stewart, Stephanie K. Polutchko, Barbara Demmig-Adams, and Christopher M. Cohu
- Subjects
Ecotype ,biology ,Light ,Acclimatization ,fungi ,Arabidopsis ,Plant Science ,biology.organism_classification ,Photosynthesis ,Chloroplast ,chemistry.chemical_compound ,chemistry ,Species Specificity ,Zeaxanthins ,Chlorophyll ,Photoprotection ,Botany ,Genetics ,Arabidopsis thaliana ,Shade tolerance - Abstract
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.
- Published
- 2015
26. Leaf architectural, vascular and photosynthetic acclimation to temperature in two biennials
- Author
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Christopher M. Cohu, Jared J. Stewart, Stephanie K. Polutchko, William W. Adams, Barbara Demmig-Adams, and Onno Muller
- Subjects
Chloroplasts ,Light ,Physiology ,Verbascum phoeniceum ,Acclimatization ,Plant Science ,Phloem ,Photosynthesis ,Verbascum ,Botany ,Genetics ,Malva ,biology ,fungi ,Temperature ,food and beverages ,Biological Transport ,Cell Biology ,General Medicine ,biology.organism_classification ,Apoplast ,Chloroplast ,Plant Leaves ,Photosynthetic acclimation ,Malva neglecta ,Carbohydrate Metabolism ,Seasons - Abstract
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.
- Published
- 2014
27. Chloroplast Photoprotection and the Trade-Off Between Abiotic and Biotic Defense
- Author
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Jared J. Stewart, William W. Adams, and Barbara Demmig-Adams
- Subjects
Abiotic component ,Chloroplast ,Resistance (ecology) ,Photoprotection ,fungi ,Botany ,food and beverages ,Context (language use) ,Phloem ,Biology ,Oxylipin ,Trade-off - Abstract
This chapter places two key photoprotective processes in the chloroplast (thermal dissipation of excess excitation energy and removal of reactive oxygen species, ROS, by anti-oxidants) into the context of whole-leaf and whole-plant function in the environment. The emerging evidence for possible trade-offs between effects of altered thermal dissipation and/or anti-oxidation capacity on plant resistance to abiotic stresses (unfavorable physical conditions) versus biotic stresses (pests and pathogens) is summarized. We conclude that more research on this topic is urgently needed, especially for specific crop species and agriculturally relevant environments, including various combinations of multiple abiotic and biotic stresses. As an example of a key redox-signaling pathway impacted by thermal dissipation and/or anti-oxidation capacity, the formation of lipid-peroxidation-derived hormonal messengers of the oxylipin family, with critical roles in plant growth, development, and defenses, is discussed. The available evidence for specific effects of the capacities of thermal dissipation and/or anti-oxidation on sugar loading into foliar phloem conduits, sugar export from leaves, whole-plant growth rate, and plant biotic defenses is reviewed. Lastly, leaf responses to moderate versus massive ROS formation via multiple feedback loops are compared and contrasted.
- Published
- 2014
28. Non-Photochemical Fluorescence Quenching in Contrasting Plant Species and Environments
- Author
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Jared J. Stewart, Christopher M. Cohu, Barbara Demmig-Adams, Seok-Chan Koh, William W. Adams, and Onno Muller
- Subjects
Sunlight ,Zeaxanthin ,Horticulture ,chemistry.chemical_compound ,Quenching (fluorescence) ,Photosystem II ,Chemistry ,Evergreen ,Photosynthesis ,Chlorophyll fluorescence ,Overwintering - Abstract
This chapter summarizes the striking variation in the modulation of plant light-harvesting efficiency in nature. Extent and kinetics of changes in light-harvesting efficiency vary strongly in response to plant genetic background and plant growth environment. Concerning genetic differences, rapidly growing annuals possess higher maximal capacities for photosynthesis than slowly growing evergreens. Conversely, slowly growing evergreens possess much higher capacities for thermal dissipation of excess excitation energy (assessed via non-photochemical quenching of chlorophyll fluorescence, NPQ, in conjunction with decreases in intrinsic photosystem II efficiency). With regard to effects of growth environment, the ability to rapidly modulate light-harvesting efficiency depends on regular exposure to excess light during plant development. Leaves grown in natural sunlight, as well as leaves grown in natural shade (typically including periods of exposure to excess light during sunflecks), are capable of modulating of light-harvesting efficiency within seconds to minutes. In contrast, leaves grown under controlled conditions without regular exposure to excess light take many hours to strongly lower their light-harvesting efficiency when exposed to high light, and at least as many hours to return to a high light-harvesting efficiency. Some of the most long-lasting depressions in light-harvesting efficiency in nature – enduring throughout an entire season – are seen in overwintering evergreens. We furthermore illustrate that overwintering evergreens show similar features as photoinhibited leaves of evergreens grown under low, non-fluctuating light and subjected to prolonged experimental high light exposure. For all conditions described here for intact leaves, low intrinsic photosystem II efficiency is closely correlated with high levels of NPQ and high foliar zeaxanthin levels – irrespective of the widely different kinetics of onset and relaxation.
- Published
- 2014
29. Multiple feedbacks between chloroplast and whole plant in the context of plant adaptation and acclimation to the environment
- Author
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Barbara Demmig-Adams, Jared J. Stewart, and William W. Adams
- Subjects
Chloroplasts ,Acclimatization ,Context (language use) ,Environment ,Phloem ,Biology ,Photosynthesis ,Models, Biological ,Plant Physiological Phenomena ,General Biochemistry, Genetics and Molecular Biology ,Botany ,Feedback, Physiological ,Ecotype ,Ecology ,fungi ,food and beverages ,Photosynthetic capacity ,Carbon ,Plant Leaves ,Chloroplast ,Adaptation ,Energy Metabolism ,General Agricultural and Biological Sciences ,Part IV: Agricultural and ecological perspective of light responses in chloroplasts ,Signal Transduction - Abstract
This review focuses on feedback pathways that serve to match plant energy acquisition with plant energy utilization, and thereby aid in the optimization of chloroplast and whole-plant function in a given environment. First, the role of source–sink signalling in adjusting photosynthetic capacity (light harvesting, photochemistry and carbon fixation) to meet whole-plant carbohydrate demand is briefly reviewed. Contrasting overall outcomes, i.e. increased plant growth versus plant growth arrest, are described and related to respective contrasting environments that either do or do not present opportunities for plant growth. Next, new insights into chloroplast-generated oxidative signals, and their modulation by specific components of the chloroplast's photoprotective network, are reviewed with respect to their ability to block foliar phloem-loading complexes, and, thereby, affect both plant growth and plant biotic defences. Lastly, carbon export capacity is described as a newly identified tuning point that has been subjected to the evolution of differential responses in plant varieties (ecotypes) and species from different geographical origins with contrasting environmental challenges.
- Published
- 2014
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