Jared J. Stewart

Multiple feedbacks between chloroplast and whole plant in the context of plant adaptation and acclimation to the environment.

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 chloroplasts 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.

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 xylems 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).

Association between minor loading vein architecture and light- and CO2-saturated rates of photosynthetic oxygen evolution among Arabidopsis thaliana ecotypes from different latitudes

Through microscopic analysis of veins and assessment of light- and CO2-saturated rates of photosynthetic oxygen evolution, we investigated the relationship between minor loading vein anatomy and photosynthesis of mature leaves in three ecotypes of Arabidopsis thaliana grown under four different combinations of temperature and photon flux density (PFD). All three ecotypes exhibited greater numbers and cross-sectional area of phloem cells as well as higher photosynthesis rates in response to higher PFD and especially lower temperature. The Swedish ecotype exhibited the strongest response to these conditions, the Italian ecotype the weakest response, and the Col-0 ecotype exhibited an intermediate response. Among all three ecotypes, strong linear relationships were found between light- and CO2-saturated rates of photosynthetic oxygen evolution and the number and area of either sieve elements or of companion and phloem parenchyma cells in foliar minor loading veins, with the Swedish ecotype showing the highest number of cells in minor loading veins (and largest minor veins) coupled with unprecedented high rates of photosynthesis. Linear, albeit less significant, relationships were also observed between number and cross-sectional area of tracheids per minor loading vein versus light- and CO2-saturated rates of photosynthetic oxygen evolution. We suggest that sugar distribution infrastructure in the phloem is co-regulated with other features that set the upper limit for photosynthesis. The apparent genetic differences among Arabidopsis ecotypes should allow for future identification of the gene(s) involved in augmenting sugar-loading and -transporting phloem cells and maximal rates of photosynthesis.

Insights from Placing Photosynthetic Light Harvesting into Context.

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.

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.

Habitat Temperature and Precipitation of Arabidopsis thaliana Ecotypes Determine the Response of Foliar Vasculature, Photosynthesis, and Transpiration to Growth Temperature

Acclimatory adjustments of foliar vascular architecture, photosynthetic capacity, and transpiration rate in Arabidopsis thaliana ecotypes (Italian, Polish [Col-0], Swedish) were characterized in the context of habitat of origin. Temperatures of the habitat of origin decreased linearly with increasing habitat latitude, but habitat precipitation was greatest in Italy, lowest in Poland, and intermediate in Sweden. Plants of the three ecotypes raised under three different growth temperature regimes (low, moderate, and high) exhibited highest photosynthetic capacities, greatest leaf thickness, highest chlorophyll a/b ratio and levels of β-carotene, and greatest levels of wall ingrowths in phloem transfer cells, and, in the Col-0 and Swedish ecotypes, of phloem per minor vein in plants grown at the low temperature. In contrast, vein density and minor vein tracheary to sieve element ratio increased with increasing growth temperature – most strongly in Col-0 and least strongly in the Italian ecotype – and transpirational water loss correlated with vein density and number of tracheary elements per minor vein. Plotting of these vascular features as functions of climatic conditions in the habitat of origin suggested that temperatures during the evolutionary history of the ecotypes determined acclimatory responses of the foliar phloem and photosynthesis to temperature in this winter annual that upregulates photosynthesis in response to lower temperature, whereas the precipitation experienced during the evolutionary history of the ecotypes determined adjustment of foliar vein density, xylem, and transpiration to temperature. In particular, whereas photosynthetic capacity, leaf thickness, and foliar minor vein phloem features increased linearly with increasing latitude and decreasing temperature of the habitats of origin in response to experimental growth at low temperature, transpiration rate, foliar vein density, and minor vein tracheary element numbers and cross-sectional areas increased linearly with decreasing precipitation level in the habitats of origin in response to experimental growth at high temperature. This represents a situation where temperature acclimation of the apparent capacity for water flux through the xylem and transpiration rate in a winter annual responded differently from that of photosynthetic capacity, in contrast to previous reports of strong relationships between hydraulic conductance and photosynthesis in other studies.

Environmental regulation of intrinsic photosynthetic capacity: an integrated view

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.

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.

Chloroplast Photoprotection and the Trade-Off Between Abiotic and Biotic Defense

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.

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

AbstractMain conclusionLeaf morphological differences have an impact on light distribution within the leaf, photosynthesis, and photoprotection inArabidopsis thalianaecotypes 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.