Photoinhibition and drought in Mediterranean woody saplings: scaling effects and interactions in sun and shade phenotypes

Interacting effects of high light and drought on the performance of sun and shade phenotypes were experimentally undertaken following survival, chlorophyll fluorescence and gas exchange in 2-year-old saplings of four Mediterranean trees (Quercus ilex and Q. coccifera as water-saving species, and Pistacia lentiscus and P. terebinthus as water-spending species). Half of the saplings were grown in full sunlight and the other half in the shade (6% sunlight). Half of each combination of species-phenotype was exposed to high light during a simulated late-summer drought. Light absorptance and gas exchange were scaled up to the whole plant with the 3-D geometrical model, Y-Plant. Quercus species were more plastic and tolerated high light and water stress better than Pistacia species, surviving longer and in drier soils, and exhibiting a less pronounced photoinhibition. There was no evidence of disadvantage for shade phenotypes under high light with increasing drought. By contrast, shade phenotypes survived longer despite larger initial decreases in photochemical efficiency and higher sensitivity to drought than sun phenotypes. The enhanced control of transpiration during drought in water-saving versus water-spending species (and also in shade versus sun phenotypes in three out of the four species) allowed extended survival. Photoinhibition reduced whole crown carbon gain in high light by c. 3% and affected significantly more the shaded leaves of a given plant (reducing their carbon gain by up to 7%) than those exposed to direct sunlight. Despite this apparently minor impact, whole plant carbon gain reduction by photoinhibition negatively correlated with survival and drought tolerance. The implications for succession and forest regeneration in arid environments, particularly under a global change scenario, are discussed.     

Photosynthesis and nitrogen allocation in needles in the sun and shade crowns of hybrid larch saplings: effect of nitrogen application

We studied the effects of applying 50 kg(N) ha^?1 year^?1 of nitrogen (N) on needle photosynthesis, N allocation and nutrient content in the sun- and shade crowns of the hybrid larch F₁ (Larix gmelinii var. japonica × L. kaempferi). The light-saturated net photosynthetic rate (P _Nmax) was not significantly affected by N application or crown position, although the contents of N, P, K, and chlorophyll (Chl), and the maximum rates of carboxylation and electron transport were lower in needles of the shade crown than of the sun crown. This difference was mainly due to an increase in the intercellular CO₂ concentration (C _i) in the needles of the shade crown. Analysis of N allocation in photosynthetic systems revealed that more N was allocated to functions related to electron transport and ribulose-1,5-bisphosphate (RuBP) regeneration in needles of the shade crown. N allocation in needles of the hybrid larch F₁ was regulated mainly by the light conditions, rather than by N application     

Herbivory in sun and shade

Observations of several plant species suggest that individuals incur greater herbivore damage in shaded than in nearby sunny areas. Two hypotheses are presented to explain this pattern of herbivory; a preliminary test of one suggests that plants growing in the sun are usually tastier, although eaten less, than those in the shade. The phenomenon has several implications for the nature of plant-herbivore interactions in terrestrial communities.     

Herbivory,foliar survival and shoot growth in fragmented populations of Aristotelia chilensis

Habitat fragmentation may modify ecological interactions such as herbivory, and these changes can impinge upon plant fitness. Through a natural experiment, we evaluated if herbivory, foliar survival and shoot growth of the evergreen tree Aristotelia chilensis differ between a continuous forest (600 ha) and small fragments (∼3 ha) of the Maulino forest. From September 2002, we monthly recorded leaf emergence, area lost to herbivores and survival in four cohorts of leaves. Although herbivory of A. chilensis was low overall (foliar area loss <12%), herbivory was higher in the continuous forest than in small fragments. Nevertheless, differences in herbivory hold only for the first cohort of leaves, which were the largest ones. At the end of the growing season, herbivory rates in the continuous forest and fragments converge for all cohorts. Except for the first cohort of leaves, whose survival was higher in the fragments than in the continuous forest, foliar survival and shoot growth was similar in the continuous forest and fragments, and there was no correlation between herbivory and foliar survival or shoot growth. Although Maulino forest fragmentation negatively affects the intensity of herbivory, this effect is only transient, affecting only leaves that emerge early in the season, and might not affect the vegetative fitness of A. chilensis adults. The consequences of changes in ecological interactions triggered by forest fragmentation ought to be assessed rather than inferred from variations in patterns of resource use.     

Photosynthetic efficiency in sun and shade plants

Photosynthetica - Photosynthesis is amongst the plant cell functions that are highly sensitive to any type of changes. Sun and shade conditions are prevalent in fields as well as dense forests....     

Anthocyanins in berries of Maqui (Aristotelia chilensis (Mol.) Stuntz)

The anthocyanin composition of berries of Maqui [Aristotelia chilensis (Mol.) Stuntz] was determined by HPLC with photodiode array and MS detection. Eight pigments corresponding to the 3-glucosides, 3,5-diglucosides, 3-sambubiosides and 3-sambubioside-5-glucosides of delphinidin and cyanidin were identified, the principal anthocyanin being delphinidin 3-sambubioside-5-glucoside (34% of total anthocyanins). The average total anthocyanin content was 137.6 +/- 0.4mg/100g of fresh fruit (211.9 +/- 0.6 mg/100g of dry fruit). The relative high anthocyanin content and the important presence of polar polyglycosylated derivatives makes the fruits of A. chilensis an interesting source of anthocyanin extracts for food and pharmaceutical uses.     

Effects of simulated browsing on the growth of Austrocedrus chilensis saplings

In the forests of Austrocedrus chilensis (D.Don) Florin et Boutleje (Cupressaceae) it is frequent to observe numerous mutilated and dwarfed saplings which have been browsed by domestic cattle and exotic deer. One way to assess the effects of browsing on plant growth is by simulating this process through defoliation. This study includes results from four years of artificial browsing at different intensities on A. chilensissaplings. Our objective was to evaluate the possible compensatory growth by A. chilensis. To that end we measured the effects of simulated browsing on the growth of saplings kept under two different experimental conditions, with and without water stress. Treatments were applied at the end of winter of 1993 and were repeated on 1994, 1995 and 1996. Treatments consisted in pruning and cutting. Neither cutting effects nor factors interactions were found. Pruning resulted in a reduction of saplings biomass of 44% and was only significant at the more intensive level. Watering produced saplings with five times more biomass, but the general response of A. chilensis to simulated browsing was the lack of compensation regardless the intensity of pruning or the quality of site.     

Photosynthetic units of sun and shade plants

A computer analysis of fluorescence induction curves of leaves treated with 3-(3,4-dichlorophenyl)-1,1 dimethylurea was done for several species. These measurements gave the ratios of the total chlorophyll to photosystem II reaction centers. This communication is a preliminary survey of sun and shade plants and demonstrates a significant variation in this ratio. In the sun plants, the photosynthetic unit sizes (chlorophyll reaction centers) varied between 220 to 480. The shade plants gave numbers mostly in the range between 630 to 940. The computer analysis of the fluorescence data also gave the connectivity parameter of energy transfer between photosynthetic units of photosystem II which varied between 0.2 and 0.5 but did not show any obvious correlation to the photosynthetic unit size.     

Mechanistic differences in photoinhibition of sun and shade plants

Leaf discs of the shade plant Tradescantia albiflora Kunth grown at 50 μmol · m^?2 · s^?1, and the facultative sun/shade plant Pisum sativum L. grown at 50 or 300 μmol · m^?2, s^?1, were photoinhibited for 4 h in 1700 μmol photons m^?2 · s^?1 at 22° C. The effects of photoinhibition on the following parameters were studied: i) photosystem II (PSII) function; ii) amount of D1 protein in the PSII reaction centre; iii) dependence of photoinhibition and its recovery on chloroplast-encoded protein synthesis; and, iv) the sensitivity of photosynthesis to photoinhibition in the presence or absence of the carotenoid zeaxanthin. We show that: i) despite different sensitivities to photoinhibition, photoinhibition in all three plants occurred at the reaction centre of PSII; ii) there was no correlation between the extent of photoinhibition and the degradation of the D1 protein; iii) the susceptibility to photoinhibition by blockage of chloroplas-tencoded protein synthesis was much less in shade plants than in plants acclimated to higher light; and iv) inhibition of zeaxanthin formation increased the sensitivity to photoinhibition in pea, but not in the shade plant Tradescantia. We suggest that there are mechanistic differences in photoinhibition of sun and shade plants. In sun plants, an active repair cycle of PSII replaces photoinhibited reaction centres with photochemically active ones, thereby conferring partial protection against photoinhibition. However, in shade plants, this repair cycle is less important for protection against photoinhibition; instead, photoinhibited PSII reaction centres may confer, as they accumulate, increased protection of the remaining connected, functional PSII centres by controlled, nonphotochemical dissipation of excess excitation energy.     

Herbivory on Diplacus aurantiacus shrubs in sun and shade

This study tested the hypothesis that carbon allocation to the production of leaf antiherbivore chemicals reflects the intensity of herbivory and interacts with resource allocation to photosynthesis. The amount of herbivory by Euphydryas chalcedona butterfly larvae was measured on Diplacus aurantiacus shrubs growing in different daily solar irradiance regimes. The amount of herbivory sustained by plants was directly related to the degree of solar irradiance the shrubs received and to characteristics which vary with light intensity, e.g. leaf specific weight, but not to leaf resin or nitrogen content. Carbon allocation to the defense of leaf area was marginally related to the light regime, but was not directly related to photosynthetic income.     

Photomorphogenesis of leaves: shade-avoidance and differentiation of sun and shade leaves.

Leaf shape is an important factor in optimal plant growth, because leaves are the main photosynthetic organs. Plants exhibit plasticity in leaf shape and structure, allowing them to optimize photosynthetic efficiency. In Arabidopsis thaliana(L.) Heynh., several types of leaves develop differentially, according to light intensity and quality. When shaded, the expansion of leaf lamina is inhibited, while the petiole elongation is enhanced. This phenomenon is part of the so-called shade-avoidance syndrome. Under low light, A. thaliana develops shade leaves with only one layer of palisade tissue, whereas under high light, it develops sun leaves that have nearly two complete layers of palisade tissue. Although the molecular mechanisms of these photomorphogenic phenomena in leaves are not well understood, recent studies of A. thaliana have provided some insight. For example, some cytochrome P450s may be involved in the specific control of the petiole length during photomorphogenesis. On the other hand, switching between sun and shade leaves is regulated by long-distance signaling from mature leaves in Chenopodium album. Here we provide an overview of the mechanisms of photomorphogenesis in leaves based on recent findings.     

Photosynthetic symmetry of sun and shade leaves of different orientations

Summary The photosynthetic responses to light of leaves irradiated on the adaxial or abaxial surfaces, were measured for plants with contrasting leaf orientations. For vertical-leaf species of open habitats (Eryngium yuccifolium and Silphium terebinthinaceum), photosynthetic rates were identical when irradiated on either surface. However, for horizontal-leaf species of open habitats (Ambrosia trifida and Solidago canadensis), light-saturated rates of photosynthesis for adaxial irradiation were 19 to 37% higher than rates for abaxial irradiation. Leaves of understory plants (Asarum canadense and Hydrophyllum canadense) were functionally symmetrical although they had horizontal orientation. Photosynthetic rates were measured at saturating CO₂, thus differences in the response to incident irradiance presumably resulted from complex interactions of light and leaf optical properties rather than from stomatal effects. Differences in absorptance (400–700 nm) among leaf surfaces were evident for horizontal-leaf species but the primary determinant of functional symmetry was leaf anatomy. Functionally symmetrical leaves had upper and lower palisade layers of equal thickness (vertical leaves of open habitats) or were composed primarily of a single layer of photosynthetic cells (horizontal leaves of understory habitats). Photosynthetic symmetry of vertical-leaf species may be an adaptation to maximize daily integrated carbon gain and water-use efficiency, whereas asymmetry of horizontal-leaf species may be an adaptation to maximize daily integrated carbon gain and photosynthetic nutrient-use efficiency.     

Water is allocated differently to chloroplasts in sun and shade leaves

Hydrogen-1 nuclear magnetic resonance spectroscopy was used to study water allocation in cell compartments of sun and shade leaves. NMR spectra of Acer platanoides were resolved into two peaks that were assigned to chloroplast and nonchloroplast water. Sun leaves contained 1.7 times more water per unit area of surface than shade leaves, and the water was allocated differently. Chloroplasts in sun leaves contained 17% of the total leaf water versus 47% in shade leaves. Comparing equal leaf surface areas, the chloroplasts in shade leaves contained 60% more water than those in sun leaves.     

Chlorophyll and light gradients in sun and shade leaves of Spinacia oleracea

Abstract. Light gradients were measured and correlated with chlorophyll concentration and anatomy of leaves in spinach (Spinacia oleracea L.). Light gradients were measured at 450, 550 and 680 nm within thin (455 μm) and thick (630 μm) leaves of spinach grown under sun and shade conditions. The light gradients were relatively steep in both types of leaves and 90% of the light at 450 and 680 nm was absorbed by the initial 140 μm of the palisade. In general, blue light was depleted faster than red light which, in turn was depleted faster than green light. Light penetrated further into the thicker palisade of sun leaves in comparison to the shade leaves. The distance that blue light at 450 nm travelled before it became 90% depleted was 120 μm in sun leaves versus 76 μm in shade leaves. Red light at 680 nm and green light at 550 nm travelled further but the trends were similar to that measured at 450nm. The steeper light gradients within the palisade-of shade leaves were caused by increased scattering of light within the intercellular air spaces and/or cells which were less compact than those in sun leaves. The decline in the amount of light within the leaf appeared to be balanced by a gradient in chlorophyll concentration measured in paradermal sections. Progressing from the adaxial epidermis, chlorophyll content increased through the palisade and then declined through the spongy mesophyll. Chlorophyll content was similar in the palisade of both sun and shade leaves. Chloroplast distribution within both sun and shade leaves was relatively uniform so that the chlorophyll gradient appeared to be caused by greater amounts of chlorophyll within chloroplasts located deeper within the leaf. These results indicate that the anatomy of the palisade may be of special importance for controlling the penetration of photo-synthetically active radiation into the leaf. Changing the structural characteristics of individual palisade cells or their arrangement may be an adaptation that maximizes the absorption of light in leaves with varying mesophyll thickness due to different ambient light regimes.     

Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings

Arthropods and pathogens damage leaves in natural ecosystems and may reduce photosynthesis at some distance away from directly injured tissue. We quantified the indirect effects of naturally occurring biotic damage on leaf-level photosystem II operating efficiency (Φ_PSII) of 11 understory hardwood tree species using chlorophyll fluorescence and thermal imaging. Maps of fluorescence parameters and leaf temperature were stacked for each leaf and analyzed using a multivariate method adapted from the field of quantitative remote sensing. Two tree species, Quercus velutina and Cercis canadensis, grew in plots exposed to ambient and elevated atmospheric CO₂ and were infected with Phyllosticta fungus, providing a limited opportunity to examine the potential interaction of this element of global change and biotic damage on photosynthesis. Areas surrounding damage had depressed Φ_PSII and increased down-regulation of PSII, and there was no evidence of compensation in the remaining tissue. The depression of Φ_PSII caused by fungal infections and galls extended >2.5 times further from the visible damage and was ∼40% more depressed than chewing damage. Areas of depressed Φ_PSII around fungal infections on oaks growing in elevated CO₂ were more than 5 times larger than those grown in ambient conditions, suggesting that this element of global change may influence the indirect effects of biotic damage on photosynthesis. For a single Q. velutina sapling, the area of reduced Φ_PSII was equal to the total area directly damaged by insects and fungi. Thus, estimates based only on the direct effect of biotic agents may greatly underestimate their actual impact on photosynthesis.     

Response of mitochondria to light intensity in the leaves of sun and shade species

The present authors have shown previously that both respiration rates and in vivo activities of the alternative oxidase (AOX) of leaves of Alocasia odora, a shade species, are lower than those in sun species, thereby optimizing energy production under limited light conditions (Noguchi et al., Australian Journal of Plant Physiology 28, 27–35, 2001). In the present study, mitochondria isolated from A. odora leaves were examined in order to investigate the biochemical basis for the differences in respiratory parameters. Alocasia odora and spinach plants were cultivated under both high and low light intensities, mitochondria were isolated from their leaves, and their respiratory properties compared. Mitochondrial content of leaf extracts from the two species was estimated using fumarase activities and antibody detection of porin (the voltage-dependent anion channel of the outer mitochondrial membrane). On a mitochondrial protein basis, spinach leaves showed higher capacities of the cytochrome pathway and cytochrome c oxidase (COX) than A. odora leaves. However, on a mitochondrial protein basis, A. odora showed higher capacities of AOX, which had a high affinity for ubiquinone when activated by pyruvate. Alocasia odora also had larger amounts of mitochondrial protein per leaf dry weight, even under severely shaded conditions, than spinach. Lower growth light intensity led to lower activities of most pathways and proteins tested in both species, especially glycine-dependent oxygen uptake. In the low light environment, most of the AOX protein in A. odora leaves was in its inactive, oxidized dimer form, but was converted to its reduced active form when plants were grown under high light. This shift may prevent over-reduction of the respiratory chain under photo-oxidative conditions.     

Density-dependent shoot-borer herbivory increases the age of first reproduction and mortality of neotropical tree saplings

Shoot herbivory by the sapling specialist shoot-borer Cromarcha stroudagnesia (Lepidoptera, Pyralidae, Chrysauginae) is shown to have large direct and indirect effects on the rates of height increment and mortality of saplings of its host tree, Tabebuia ochracea (Bignoniaceae), in the secondary successional tropical dry forests of the Area de Conservación Guanacaste, Costa Rica. Experiments and field observations over 3-4 years show a substantial reduction in sapling height increments due to C. stroudagnesia herbivory, of equivalent magnitude to the difference in height increments between undamaged saplings in canopy gaps and full understorey shade. Extrapolating this data at average amounts of C. stroudagnesia herbivory increases the duration of the pre-reproductive sapling life stage by about 40% relative to undamaged plants. This is an underestimate, as top shoot herbivory by C. stroudagnesia also increased the probability of canopy gap saplings being overtopped and shaded by surrounding vegetation. Sapling mortality was increased by C. stroudagnesia herbivory, with 11.8% of the most heavily damaged young saplings dying in 3 years while no undamaged saplings died. Cromarcha stroudagnesia herbivory strongly increases with the number of conspecific T. ochracea saplings and the number of conspecific shoots within 50 m of focal saplings. It is therefore likely to disproportionately decrease the number of saplings and rate of recruitment to reproductive age in areas of high conspecific sapling density. These results suggest that sapling herbivory, especially herbivory of terminal meristems, has an important but largely unexplored influence on the population dynamics of tropical tree species. They further demonstrate that sapling herbivory by insects, in addition to the well-studied insect predation and herbivory of seedlings, is likely to influence tree species coexistence in tropical forests.     

Developmental process of sun and shade leaves in Chenopodium album L.

The authors’ previous study of Chenopodium album L. revealed that the light signal for anatomical differentiation of sun and shade leaves is sensed by mature leaves, not by developing leaves. They suggested that the two‐cell‐layered palisade tissue of the sun leaves would be formed without a change in the total palisade tissue cell number. To verify that suggestion, a detailed study was made of the developmental processes of the sun and shade leaves of C. album with respect to the division of palisade tissue cells (PCs) and the data was expressed against developmental time (leaf plastochron index, LPI). The total number of PCs per leaf did not differ between the sun and shade leaves throughout leaf development (from LPI ?1 to 10). In both sun and shade leaves, anticlinal cell division of PCs occurred most frequently from LPI ?1 to 2. In sun leaves, periclinal division of PCs occurred synchronously with anticlinal division. The constancy of the total number of PCs indicates that periclinal divisions occur at the expense of anticlinal divisions. These results support the above suggestion that two‐cell‐layered palisade tissue is formed by a change of cell division direction without a change in the total number of PCs. PCs would be able to recognize the polarity or axis that is perpendicular to the leaf plane and thereby change the direction of their cell divisions in response to the light signal from mature leaves.