Onno Muller

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.

Sun-induced fluorescence - a new probe of photosynthesis: First maps from the imaging spectrometer HyPlant

Variations in photosynthesis still cause substantial uncertainties in predicting photosynthetic CO2 uptake rates and monitoring plant stress. Changes in actual photosynthesis that are not related to greenness of vegetation are difficult to measure by reflectance based optical remote sensing techniques. Several activities are underway to evaluate the sun-induced fluorescence signal on the ground and on a coarse spatial scale using space-borne imaging spectrometers. Intermediate-scale observations using airborne-based imaging spectroscopy, which are critical to bridge the existing gap between small-scale field studies and global observations, are still insufficient. Here we present the first validated maps of sun-induced fluorescence in that critical, intermediate spatial resolution, employing the novel airborne imaging spectrometer HyPlant. HyPlant has an unprecedented spectral resolution, which allows for the first time quantifying sun-induced fluorescence fluxes in physical units according to the Fraunhofer Line Depth Principle that exploits solar and atmospheric absorption bands. Maps of sun-induced fluorescence show a large spatial variability between different vegetation types, which complement classical remote sensing approaches. Different crop types largely differ in emitting fluorescence that additionally changes within the seasonal cycle and thus may be related to the seasonal activation and deactivation of the photosynthetic machinery. We argue that sun-induced fluorescence emission is related to two processes: (i) the total absorbed radiation by photosynthetically active chlorophyll; and (ii) the functional status of actual photosynthesis and vegetation stress.

Experimental warming studies on tree species and forest ecosystems: a literature review

Temperature affects a cascade of ecological processes and functions of forests. With future higher global temperatures being inevitable it is critical to understand and predict how forest ecosystems and tree species will respond. This paper reviews experimental warming studies in boreal and temperate forests or tree species beyond the direct effects of higher temperature on plant ecophysiology by scaling up to forest level responses and considering the indirect effects of higher temperature. In direct response to higher temperature (1) leaves emerged earlier and senesced later, resulting in a longer growing season (2) the abundance of herbivorous insects increased and their performance was enhanced and (3) soil nitrogen mineralization and leaf litter decomposition were accelerated. Besides these generalizations across species, plant ecophysiological traits were highly species-specific. Moreover, we showed that the effect of temperature on photosynthesis is strongly dependent on the position of the leaf or plant within the forest (canopy or understory) and the time of the year. Indirect effects of higher temperature included among others higher carbon storage in trees due to increased soil nitrogen availability and changes in insect performance due to alterations in plant ecophysiological traits. Unfortunately only a few studies extrapolated results to forest ecosystem level and considered the indirect effects of higher temperature. Thus more intensive, long-term studies are needed to further confirm the emerging trends shown in this review. Experimental warming studies provide us with a useful tool to examine the cascade of ecological processes in forest ecosystems that will change with future higher temperature.

Foliar phloem infrastructure in support of photosynthesis

Acclimatory adjustments of foliar minor loading veins in response to growth at different temperatures and light intensities are evaluated. These adjustments are related to their role in providing infrastructure for the export of photosynthetic products as a prerequisite for full acclimation of photosynthesis to the respective environmental conditions. Among winter-active apoplastic loaders, higher photosynthesis rates were associated with greater numbers of sieve elements per minor vein as well as an increased apparent total membrane area of cells involved in phloem loading (greater numbers of cells and/or greater cell wall invaginations). Among summer-active apoplastic loaders, higher photosynthesis rates were associated with increased vein density and, possibly, a greater number of sieve elements and companion cells per minor vein. Among symplastic loaders, minor loading vein architecture (number per vein and arrangement of cells) was apparently constrained, but higher photosynthesis rates were associated with higher foliar vein densities and larger intermediary cells (presumably providing a greater volume for enzymes involved in active raffinose sugar synthesis). Winter-active apoplastic loaders thus apparently place emphasis on adjustments of cell membrane area (presumably available for transport proteins active in loading of minor veins), while symplastic loaders apparently place emphasis on increasing the volume of cells in which their active loading step takes place. Presumably to accommodate a greater flux of photosynthate through the foliar veins, winter-active apoplastic loaders also have a higher number of sieve elements per minor loading vein, whereas symplastic loaders and summer-active apoplastic loaders have a higher total number of veins per leaf area. These latter adjustments in the vasculature (during leaf development) may also apply to the xylem (via greater numbers of tracheids per vein and/or greater vein density per leaf area) serving to increase water flux to mesophyll tissues in support of high rates of transpiration typically associated with high rates of photosynthesis.

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).

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.

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.

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.

Minor loading vein acclimation for three Arabidopsis thaliana ecotypes in response to growth under different temperature and light regimes

In light of the important role of foliar phloem as the nexus between energy acquisition through photosynthesis and distribution of the products of photosynthesis to the rest of the plant, as well as communication between the whole plant and its leaves, we examined whether foliar minor loading veins in three Arabidopsis thaliana ecotypes undergo acclimation to the growth environment. As a winter annual exhibiting higher rates of photosynthesis in response to cooler vs. warmer temperatures, this species might be expected to adjust the structure of its phloem to accommodate greater fluxes of sugars in response to growth at low temperature. Minor (fourth- and third-order) veins had 14 or fewer sieve elements and phloem tissue comprised 50% or more of the cross-sectional area. The number of phloem cells per minor loading vein was greater in leaves grown under cool temperature and high light vs. warm temperature and moderate light. This effect was greatest in an ecotype from Sweden, in which growth under cool temperature and high light resulted in minor veins with an even greater emphasis on phloem (50% more phloem cells with more than 100% greater cross-sectional area of phloem) compared to growth under warm temperature and moderate light. Likewise, the number of sieve elements per minor vein increased linearly with growth temperature under moderate light, almost doubling over a 27°C temperature range (21°C leaf temperature range) in the Swedish ecotype. Increased emphasis on cells involved in sugar loading and transport may be critical for maintaining sugar export from leaves of an overwintering annual such as A. thaliana, and particularly for the ecotype from the northern-most population experiencing the lowest temperatures.

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.