Differential positioning of chloroplasts in C4 mesophyll and bundle sheath cells

Chloroplast photorelocation movement is extensively studied in C₃ but not C₄ plants. C₄ plants have two types of photosynthetic cells: mesophyll and bundle sheath cells. Mesophyll chloroplasts are randomly distributed along cell walls, whereas bundle sheath chloroplasts are located close to the vascular tissues or mesophyll cells depending on the plant species. The cell-specific C₄ chloroplast arrangement is established during cell maturation, and is maintained throughout the life of the cell. However, only mesophyll chloroplasts can change their positions in response to environmental stresses. The migration pattern is unique to C₄ plants and differs from that of C₃ chloroplasts. in this mini-review, we highlight the cell-specific disposition of chloroplasts in C₄ plants and discuss the possible physiological significances.Key words: abscisic acid, aggregative movement, avoidance movement, blue light, bundle sheath cell, C₄ plant, chloroplast, cytoskeleton, environmental stress, mesophyll cellChloroplasts can change their intracellular positions to optimize photosynthetic activity and/or reduce photodamage occurring in response to light irradiation. On treating with high-intensity light, the chloroplasts move away from the light to minimize photodamage (avoidance response). Meanwhile, on irradiating with low-intensity light, they move toward the light source to maximize photosynthesis (accumulation response). These chloroplast-photorelocation movements are observed in a wide variety of plant species from green algae to seed plants,^1–3 although little attention has been paid to C₄ plants. There is a report stating that monocotyledonous C₄ plants showed changes in the light transmission of leaves in response to blue light,⁴ although the direction of migration of the chloroplasts is not described.C₄ plants have two types of photosynthetic cells: mesophyll (M) cells and bundle sheath (BS) cells, which have numerous well-developed chloroplasts. BS cells surround the vascular tissues, while M cells encircle the cylinders of the BS cells (Fig. 1). The C₄ dicarboxylate cycle of photosynthetic carbon assimilation is distributed between the two cell types, and acts as a CO₂ pump to concentrate CO₂ in the BS chloroplasts.^5,6 C₄ plants are divided into three subtypes on the basis of decarboxylating enzymes: NADP-malic enzyme (ME), NAD-ME and phosphoenolpyruvate carboxykinase. Although the M chloroplasts of all C₄ species are randomly distributed along the cell walls, BS chloroplasts are located either in a centripetal (close to the vascular tissue) or in a centrifugal (close to M cells) position, depending on the species (Fig. 1A).⁷ Thus, C₄ M and BS cells have different systems for chloroplast positioning: an M cell-specific system for dispersing chloroplasts and a BS cell-specific system for holding chloroplasts in a centripetal or centrifugal disposition.Open in a separate windowFigure 1The intracellular arrangement of chloroplasts in finger millet (Eleusine coracana), an NAD-ME-type C₄ plant. (A) Light micrograph of a transverse section of a leaf blade from a control plant. Bundle sheath (BS) cells surround the vascular tissues, while mesophyll (M) cells encircle the cylinders of the BS cells. BS chloroplasts are well developed, and are located in a centripetal position, whereas M chloroplasts are randomly distributed along the cell walls. B, bundle sheath cell; M, mesophyll cell; V, vascular bundle. (B) Transverse section of a leaf blade from a drought-stressed plant. Most M chloroplasts are aggregatively distributed toward the BS side, while the centripetal arrangement of BS chloroplasts is unchanged. (C and D) Transverse sections of leaf segments irradiated with blue light of intensity 500 µmol m⁻² s⁻¹ with or without 30 µM ABA for 8 h (C and D, respectively). The adaxial side of each leaf section (upper side in the photograph) was illuminated. In the absence of ABA, M chloroplasts exhibited avoidance movement on the illuminated side and aggregative movement on the opposite side. In the presence of ABA, aggregative movement was observed on both sides. Scale bars = 50 µm.