Structural Adaptation of the Leaf Mesophyll to Shading

Structural characteristics of the mesophyll were studied in five boreal grass species experiencing a wide range of light and water supply conditions. Quantitative indices of the palisade and spongy mesophyll tissues (cell and chloroplast sizes, the number of chloroplasts per cell, the total cell and chloroplast surface area per unit leaf surface area) were determined in leaves of each of the species. The cell surface area and the cell volume in spongy mesophyll were determined with a novel method based on stereological analysis of cell projections. An important role of spongy parenchyma in the photosynthetic apparatus was demonstrated. In leaves of the species studied, the spongy parenchyma constituted about 50% of the total volume and 40% of the total surface area of mesophyll cells. The proportion of the palisade to spongy mesophyll tissues varied with plant species and growth conditions. In a xerophyte Genista tinctoria, the total cell volume, cell abundance, and the total surface area of cells and chloroplasts were 30–40% larger in the palisade than in the spongy mesophyll. In contrast, in a shade-loving species Veronica chamaedris, the spongy mesophyll was 1.5–2 times more developed than the palisade mesophyll. In mesophyte species grown under high light conditions, the cell abundance and the total cell surface area were 10–20% greater in the palisade mesophyll than in the spongy parenchyma. In shaded habitats, these indices were similar in the palisade and spongy mesophyll or were 10–20% lower in the palisade mesophyll. In mesophytes, CO₂ conductance of the spongy mesophyll accounted for about 50% of the total mesophyll conductance, as calculated from the structural characteristics, with the mesophyll CO₂ conductance increasing with leaf shading.     

Structural and Functional Changes in the Leaves of Plants from Steppe Communities as Affected by Aridization of the Eurasian Climate

Morphological and physiological characteristics of leaves from plant species collected in steppe communities in the various climatic zones in Eurasia were compared. The changes in leaf structure correlated with the major climatic factors. The mean thickness of leaves increased with increasing mean temperature of July and decreasing mean precipitation, which corresponded to aridity increase. The increased leaf thickness correlated with an increase in the specific leaf weight. The content of chlorophylls (a + b) in leaves greatly varied with plant habitats, whereas the chlorophyll a/b ratio remained unchanged. The chlorophyll content in leaf tissues had a general tendency to decrease with increasing leaf thickness. The leaf chlorophyll content positively correlated (R ² = 0.77) with the proportion of chlorenchyma in leaf tissues. It is concluded that steppe plants adapt to climate aridization at the structural level by increasing the proportion of protective heterotrophic components of the leaf without changing the functional activity of photosynthetic tissues.     

Photosynthetic Metabolism and Activity of Carboxylating Enzymes in Emergent,Floating, and Submersed Leaves of Hydrophytes

Radioisotope techniques were used to compare photosynthetic CO₂ fixation, activities of carboxylating enzymes, and the composition of photosynthates in 42 species of aquatic plants (emergent, floating, and submersed hydrophytes) collected from rivers Sysert' and Iset' in Sverdlovsk oblast (Russia). The submersed leaves, in comparison with the emergent and floating leaves, featured lower rates of potential photosynthesis (by 2.2 mg CO²/(dm² h) on average), low content of the fraction I protein, and low activity of Rubisco and phosphoenolpyruvate carboxylase (PEPC). The averaged activities of Rubisco and PEPC were diminished in submersed leaves by 10 and 1 mg/(dm² h), respectively. Different hydrophyte groups showed similar composition of assimilates accumulated after 5-min photosynthesis and did not differ in this respect from terrestrial plants. However, the incorporation of ¹⁴C into sucrose and starch in submersed leaves (30 and 9% of total labeling, respectively) was lower than in emergent and floating leaves (45 and 15%, respectively). At the same time, the incorporation of ¹⁴C into C₄ acids (malate and aspartate) was 1.5 times higher in submersed leaves than in other leaf types. Analysis of leaf differentiation, the Rubisco/PEPC activity ratio, the PEPC activity, and the composition of primary photosynthates in the pulse–chase experiments revealed no evidence of the C₄ effect in the submersed hydrophytes examined. The adaptation of hydatophytes to specific conditions of an aquatic environment was structurally manifested in the reduction (by a factor of 3–5) in the number of chloroplasts per 1 cm² leaf area. This small number of chloroplasts was responsible for low photosynthetic rates in submersed leaves, although metabolic activities of individual chloroplasts were similar for all three hydrophyte groups.     

Structure of the Photosynthetic Apparatus in Leaves of Freshwater Hydrophytes: 2. Quantitative Characterization of Leaf Mesophyll and the Functional Activity of Leaves with Different Degrees of Submersion

The structure of leaf photosynthetic elements was investigated on 42 boreal plant species characterized by different degrees of submergence (helophytes, neustophytes, and hydatophytes). Six main types of mesophyll structures were identified. Quantitative characteristics for the mesostructure of the photosynthetic apparatus in these groups were determined, such as the size and abundance of cells and chloroplasts in the mesophyll and epidermis, the number of plastids per cell in each tissue, the total surface area of the mesophyll cells, epidermal cells, and chloroplasts per unit leaf area. Analysis showed that quantitative characteristics of the photosynthetic apparatus in hydrophytes are determined by two factors: (a) the degree of leaf submergence and (b) the type of mesophyll structure. With an increasing degree of immersion in water, the mesophyll types change in a sequence isopalisade dorsoventral homogeneous. The leaves become thinner, their weight per unit area diminishes, cells and chloroplasts become less numerous (on a per unit leaf area basis), but their dimensions become larger. Adaptation to aquatic medium is also manifested in the increasing contribution of the epidermal tissue to the overall photosynthesis: in submerged leaves, the epidermis accounts for more than 50% of the photosynthetic activity. The occurrence of six structural types of leaves contrasting in their characteristics was confirmed by discriminatory analysis according to the qualitative parameters of mesophyll.     

A comparative anatomical and biochemical analysis in salsola (Chenopodiaceae) species with and without a Kranz type leaf anatomy: a possible reversion of C4 to C3 photosynthesis

Leaf anatomy was studied by light and electron microscopy and the leaf activities of RUBP carboxylase, PEP carboxylase, and malic enzyme were assayed in: Salsola australis and S. oreophila grown on the West Pamirs at 1800 m altitude; in S. australis grown on the East Pamirs at 3860 m; and in S. arbusculiformis grown in the Kisil-Kum desert in Middle Asia near 500 m. Carbon isotope fractionation ratio values also were measured on whole leaf tissue for 18 Salsola species field collected in these and other regions of the former USSR. S. australis leaves are cylindrical and in cross section exhibit a peripheral ring of mesophyll and then an inner ring of bundle sheath type cells; and its biochemical characteristics and deltaC values are typical of a C4 species of the NADP-malic enzyme malate-forming group. These traits were expressed independent of the plant growth altitude up to 4000 m. C4 type deltaC values were obtained in 14 of the Salsola species. Anatomical, structural, and biochemical features typical of the C4 syndrome were absent in S. oreophila and S. arbusculiformis. Four Salsola species, including these two, had C3-type deltaC values. Their cylindrical leaves in cross section exhibited two to three peripheral rings as layers of palisade parenchyma. Although their vascular bundles were surrounded by green bundle sheath cells, their organelle numbers were comparable to those in mesophyll cells. Neither bundle sheath cell wall thickenings nor dimorphic chloroplasts in two leaf cell types were observed. In S. oreophila, there was a high activity of RuBP carboxylase, but a low activity of C4 cycle enzymes. Interpretation of these data lends evidence to the hypothesis that a small group of C3 Salsola species, including S. oreophila, S. arbusculiformis, S. montana, and S. pachyphylla, arose as the result of a reversion of a C4 to a C3 type of photosynthetic CO2 fixation in the cooler climates of Middle Asia.     

Structural and Functional Grounds for Ephedra sinica Expansion in Mongolian Steppe Ecosystems

Morphological and structural characteristics of photosynthetic organs, diurnal changes in photosynthetic and transpiration rates, and the efficiency of water use were studied in three plant species from mountain-steppe ecosystems in Mongolia, Ephedra sinica Stapf, Stipa glareosa P. Smirn., and Allium polyrhizum Furcz. ex Regel. The species studied differed in the structural and functional mechanisms for the adaptation of photosynthetic apparatus to arid conditions. E. sinica has thick, vertical assimilating shoots, which are characterized by a high density (620 mg/cm³) and a small proportion of photosynthetic tissues (13%). The proportion of meso-phyll in the leaves of A. polyrhizum and S. glareosa was two and three times higher, respectively. The low content of phototrophic tissues in E. sinica shoot was compensated for by a high photosynthetic activity of single chloroplasts (25 mg CO₂/(10⁹ chloroplast h)), which was six times higher, than in two other species. Daily course of photosynthesis and transpiration inE. sinica differed from those of A. polyrhizum and S. glareosa by the absence of the midday depression. E. sinica had the highest efficiency of water use (45 mg CO₂/g H₂O) due to a low transpiration rate (0.25 g/g fr wt h). It is concluded that, in E. sinica, the main strategy for adaptation to arid stress is to develop in the shoot a few photosynthesizing cells of high assimilation activity. Such structural organization of photosynthetic organs in ephedra contributes to its higher efficiency of water use and stability of physiological characteristics under changing environmental conditions. These specific features of the structure of assimilating organs and their functional features contribute to a greater expansion of E. sinica with increasing climate aridization in Mongolia.     

Photosynthesizing Tissue Development in C4 Cotyledons of Two Salsola Species (Chenopodiaceae)

The quantitative anatomy of developing cotyledons of NAD-malic enzyme species Salsola incanescens and NADP-malic enzyme species S. paulsenii (Chenopodiaceae) was studied. S. incanescens belongs to the group of species with foliar type of seedling development characterized by slowly growing cotyledons and a rosette form at juvenility. The rosette is the consequence of fast leaf formation, which was correlated with a low rate of leaf growth. S. paulsenii belongs to the group with the cotyledonous type of seedling development. A high growth rate of cotyledons, slow leaf formation, and absence of the rosette characterize this type. Slow leaf formation was correlated with a high rate of leaf growth. The Kranz–anatomy in cotyledons of S. incanescens (atriplicoid type) and S. paulsenii (salsoloid type) determines the duration of cotyledon development proceeding for 15 days after seed germination. The rate of growth changes during the developmental period was correlated with the type of seedling development. Cotyledons of a foliar species S. incanescens exhibit 2 to 5 times slower growth changes in cotyledon area, width, thickness, volume of mesophyll and bundle sheath cells, and number of chloroplasts per bundle sheath cell than the cotyledons of a cotyledonous species S. paulsenii. During cotyledon development in both species, the number of chloroplasts per mesophyll cell remained unchanged, and developmental changes in the bundle sheath occurred at higher rate than in mesophyll cells. Thus, these two indices seem to be independent of the type of Kranz–anatomy. The presence of atriplicoid type cotyledons in the species with salsoloid structure of true leaves might indicate a close genetic relationship between these two patterns of Kranz-anatomy.     

A Method for Calculating the Volume and Surface Area in Rice Mesophyll Cells

A method was developed for determining the surface area and volume of rice mesophyll cells of elaborate configuration. The method was employed to calculate these indices in several types of rice mesophyll cells found in seventy samples (53 species) of diverse origin coming from Japan, China, Korea, India, Nepal, Australia, France, Italy, Uzbekistan, Afghanistan, and Krasnodar and Primorskii regions. The cultivars of diverse geographic origin varied in cell shape and size due to the number, size, and arrangement of chloroplasts. When the volumes and surface areas of leaf mesophyll cells were compared using the method reported herein and a simple empirical model of the cell as a single ellipsoid, the two methods produced relatively similar data for cell volume; however, the surface area calculated by the former method was about two times larger than in the latter case. The method described in this paper allows for accurate calculations of the volume and surface area of rice mesophyll cells when data are available on the cell shape and linear dimensions and the number of chloroplasts per cell.     

Structure of the Photosynthetic Apparatus in Leaves of Freshwater Hydrophytes: 1. General Characteristics of the Leaf Mesophyll and a Comparison with Terrestrial Plants

The structure of photosynthetic elements was investigated in leaves of 42 boreal plant species featuring different degrees of submergence (helophytes, neustophytes, and hydatophytes). The mesophyll structure types were identified for all these species. Chlorenchyma tissues and phototrophic cells were quantitatively described by such characteristics as the sizes of cells and chloroplasts in the mesophyll and epidermis, the abundance of cells and chloroplasts in these tissues, the total surface area of cells and chloroplasts per unit leaf area, the number of plastids per cell, etc. The hydrophytes typically had thick leaves (200–350 m) with a well-developed aerenchyma; their specific density per unit area (100–200 mg/dm²) was lower than in terrestrial plants. Mesophyll cells in aquatic plants occupied a larger volume (5–20 × 10³m³) than epidermal cells (1–15 × 10³m³). The number of mesophyll cells per unit leaf area was nearly 1.5 times higher than that of epidermal cells. Chloroplasts were present in the epidermis of almost all species, including emergent leaves, but the ratio of the chloroplast total number to the number of all plastids varied depending on the degree of leaf submergence. The total number of plastids per unit leaf area (2–6 × 10⁶/cm²) and the surface of chloroplasts per unit leaf area (2–6 cm²/cm²) were lower in hydrophytes than in terrestrial plants from climatically similar habitats. The functional relations between mesophyll parameters were similar for hydrophytes and terrestrial plants (a positive correlation between the leaf weight per unit area, leaf thickness, and the number of mesophyll cells per unit leaf area), although no correlation was found in hydrophytes between the volume of mesophyll cells and the leaf thickness. Phototrophic tissues in aquatic plants contributed a larger fraction to the leaf weight than in terrestrial plants, because the mechanical tissues were less developed in hydrophytes. The CO₂assimilation rates by leaves were lower in hydrophytes than in terrestrial plants, because the total surface area of chloroplasts per unit leaf area is comparatively small in hydrophytes, which reduces the conductivity for carbon dioxide diffusion towards the carboxylation sites.     

Plant Construction Cost in the Boreal Species Differing in Their Ecological Strategies

Construction cost (CC) of leaves was studied in 73 boreal plant species differing in ecological strategy. CC is the energy cost, expressed as glucose weight, of the plant weight unit formation. The perennial species that exhibited the stress-tolerant (S) type of strategy had the highest, whereas the annual plants of the ruderal type (R) of strategy had the lowest CC values, and the individual plant species from these two groups significantly differed in their CC indices. Plant species of diverse strategies were regularly distributed in the Grime's triangle, according to their CC values. The analysis of leaf chemical components has shown that high CC values in plants of the S-group correlated with a higher content of energy-expensive organic compounds, pigments, lignin, waxes, phenolics, etc. In contrast, in the plants that exhibited the r-strategy, the majority of photosynthetically assimilated carbon was utilized in the synthesis of functional substances, namely, proteins and carbohydrates. Our data showed the differential organization of plant metabolism in the plants exhibiting different types of ecological strategies. The CC values of leaf, together with other known characteristics, can be used for the identification of the types of ecological strategies and the assessment of the resistance of plant species and varieties to environmental stress.