In contrast, the centripetal arrangement of BS chloroplasts was unchanged, even though they appeared to swell slightly after strong light illumination and the degree of chloroplast association was marginally reduced. When the water potential was between –0.53 and –0.15 MPa, chloroplast movement was observed in some sections but not in others. Comparative examination of terrestrial plant leaves in terms of light-induced absorption changes due to chloroplast rearrangements. National Center for Biotechnology Information, Unable to load your collection due to an error, Unable to load your delegates due to an error, The intracellular arrangement of chloroplasts in finger millet (. Aggregative movement of M chloroplasts in field-grown finger millet and maize in midsummer. At the same time, we checked whether M chloroplast movement occurred and the results were plotted on a graph. For other chemical treatments, small leaf segments were excised and vacuum infiltrated for 10 min with 10 mM MES-KOH (pH 6.9) containing IAA (0.3, 1 or 3 μM), 2,4-D (3, 10 or 30 μM), GA3 (15, 50 or 150 μM), kinetin (30, 100 or 300 μM), ABA (1, 3, 10 or 30 μM), NaCl [0.3, 1 or 3% (w/v)] or H2O2 (1, 5, 10, 20 or 100 mM). We therefore assumed that reactive oxygen species are involved in the chloroplast damage induced by salinity (Mitsuya et al. Recently, blue light-induced co-localization of mitochondria with chloroplasts was shown in Arabidopsis palisade M cells (Islam et al. 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. To examine whether light irradiation is necessary for the chloroplast movement in response to environmental stresses, finger millet was subjected to drought or salinity stress under dark conditions. Cytochalasin B is a potent inhibitor of actin polymerization, and we had previously confirmed by immunodetection that our pre-treatment of leaf segments with cytochalasin B disrupted actin networks (Kobayashi et al. The intracellular positions of neither type of mitochondria were changed regardless of salinity stress. J Plant Res. Previously it was reported that water stress induced centripetal re-arrangement of M chloroplasts in leaves of the C4 plant, maize (Lal and Edwards 1996) and the C4 Crassulacean acid metabolism (CAM) cycling plant, Portulaca grandiflora (Guralnick et al. BS cells surround the vascular tis- sues, while M cells encircle the cylinders of the BS cells (Fig. 2017 Jan;40(1):80-94. doi: 10.1111/pce.12834. Cytochalasin B did not affect the disposition of M chloroplasts under normal intensity light (Figs. The intracellular orientation of BS chloroplasts is thought to have physiological significance. We characterized protein phosphorylation in thylakoids of the two cell types from maize grown under either low or high light. 2003, Yamane et al. 2009). Scale bars = 50 μm. The Ministry of Education, Culture, Sports, Science and Technology (Grants-in-Aid for Scientific Research No. NIH Actually, we observed an increase in light transmittance through leaf blades in response to high intensity light (Supplementary Figs. 2007, Tsuboi et al. 9). We also confirmed that blue light could induce the centripetal positioning of M chloroplasts but the extent of localization was not prominent (data not shown). My lecturer said that CAM plants only have mesophyll plants. Treatment of finger millet with cytochalasin B showed a prominent inhibitory effect on the strong light-dependent movement of M chloroplasts, in contrast to treatment with dimethylsulfoxide (DMSO) as a control (Fig. 2003, Sato and Kadota 2007). Moreover, the re-arrangement of M chloroplasts was observed in field-grown C4 plants when exposed to mid-day sunlight, but also under midsummer drought conditions. [PMC free article] Rathnam CK, Edwards GE. The chloroplast avoidance response decreases internal conductance to CO, Phototropins and neochrome1 mediate nuclear movement in the fern, Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in. 4C). In contrast, light- dependent nuclear positioning was reported in leaf cells of A. thaliana and prothallial cells of Adiantum capillus-veneris (Iwabuchi et al. The Systematic Comparison of C3 and C4 Plants can be made through Metabolic Network. (A) Control; (B) salinity stress; (C) high osmotic stress. Thus, reactive oxygen species are another potential trigger for chloroplast movement. The extent of chloroplast avoidance movement in A. thaliana increases in response to the intensity of white light and reaches a maximum at about 500 μmol m−2 s−1 (Kasahara et al. The actomyosin system is necessary for arrangement of both chloroplasts during cell maturation and rearrangement of chloroplasts after disturbance by centrifugal force (Miyake and Nakamura 1993, Kobayashi et al. Leaf segments were then excised from the upper developed leaf blades and fixed as described above. M chloroplasts were distributed toward BS cells but not along the cell walls directly attached to BS cells. Only the M chloroplasts showed a change in intracellular positioning in response to high osmotic stress, similarly to the salinity stress. After floating on the same solution for 16 h under low light (100 μmol m−2 s−1), the leaf segments were hand-sectioned with a razor blade and transverse sections were observed with a light microscope. 2009). Scale bars = 50 μm. Plants were grown in well-watered and periodically fertilized soil for 10 weeks, and fully-matured leaves were used for experiments. This re-arrangement pattern was obviously different from the pattern observed in finger millet in which M chloroplasts mainly migrated towards the BS side and formed a partial ring around a cylinder of BS cells. All rights reserved. We further observed the intracellular arrangement of mitochondria (Fig. These bundle sheaths have the chloroplasts arranged centrifugally with the large starch granules and unstacked thylakoid membranes. 2009 Oct;50(10):1736-49. doi: 10.1093/pcp/pcp116. Similarly, the maximum chloroplast movement in redwood sorrel occurs upon illumination with blue light at 250 μmol m−2 s−1 (780 μmol m−2 s−1 of daylight) (Brugnoli and Björkman 1992). After incubation at 4°C overnight, the fixed segments were embedded in 5% (w/v) agar and sectioned at 70–80 μm with a micro-slicer (DTK-3000W, Dosaka EM, Kyoto, Japan). 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. C4 plants is partitioned over two different cell types, the mesophyll and bundle-sheath cells. Intracellular localization of certain photosynthetic enzymes in bundle sheath cells of plants possessing the C4 pathway of photosynthesis. Serial confocal optical images at 0.50 μm intervals were collected, and projections of 20–40 μm thickness were created with LSM Imaging Browser software. 2002). Therefore, we conclude that the chloroplast movement in response to environmental stresses is not caused directly by plasmolysis, which hardly occurs in plants growing under atmospheric conditions. The aggregative movement of M chloroplasts in salinity-stressed plants was also observed in semi-thin sections prepared from resin-embedded leaves (Supplementary Fig. Most of the M chloroplasts were disproportionately re-distributed to the BS side in response to the light, and the centripetal positioning of M chloroplasts was more distinct at intensities >3,000 μmol m−2 s−1. with mesophyll and bundle-sheath cells in two concentric layers. Leaf blades of maize were irradiated for 2 h with normal intensity (250 μmol m−2 s−1) (A and B) or high intensity (4,000 μmol m−2 s−1) light (C and D), and transverse sections were examined. Some factors concerning the centripetal disposition of bundle sheath chloroplasts during the leaf development of, Centripetal disposition of bundle sheath chloroplasts during the leaf development of, Photoinhibition and photoprotection under nutrient deficiencies, drought and salinity, Photoprotection, Photoinhibition, Gene Regulation, and Environment, Salinity induces granal development in bundle sheath chloroplasts of NADP-malic enzyme type C. Photoinhibition and D1 protein degradation in mesophyll and agranal bundle sheath thylakoids of maize. The time required for obvious observation of chloroplast movement is also shorter in C3 plants. In each panel, the upper side of the leaf sections is the adaxial side. 8B). 2003). Previously, we found that salinity-induced damage in M chloroplasts of maize and rice is light dependent, and not due to direct effects of excessive accumulation of sodium in the leaf tissues (Mitsuya et al. The leaf surface at that time was exposed to a light intensity of about 1,800 μmol m−2 s−1, which was not high enough to induce chloroplast movement in the laboratory. Moreover, growth conditions might be another factor to yield the differential light responsiveness. While C4 plants photosynthesis activities are divided between mesophyll and bundle sheath cells where carbon fixation is catalyzed by phosphoenolpyruvate carboxylase (PEPC). For cytochalasin treatment, small leaf segments (5 × 5 mm square) were excised and vacuum infiltrated for 10 min with 0.5% (v/v) DMSO with or without 50 μM cytochalasin B (MP Biomedicals, Irvine, CA, USA). 6). Cytological evidence of BSD2 functioning in both chloroplast division and dimorphic chloroplast formation in maize leaves. Search for other works by this author on: Crop production in artificial solutions and soils with special reference to factors influencing yield and absorption of inorganic nutrients. They described that the chloroplasts and cytosol in M cells of drought-stressed maize, a monocot NADP-ME type C4 plant, collapsed inwardly and BS chloroplasts lost their centrifugal position. 5C). Plants displaying C4 photosynthesis' generally have a specific anatomical leaf structure known as Kranz anatomy (9). Chloroplast photorelocation movement is extensively studied in C3 but not C4 plants. 2009). Phospho enol pyruvate carboxylase (PEPC), localized to the cytosol of the mesophyll cell, catalyzes the first carboxylation step of the C4 photosynthetic pathway. In contrast, the centripetal position of BS chloroplasts maximizes the length of the CO2 diffusion pathway between BS and M cells, and minimizes CO2 leakage from BS cells to M cells (Hattersley and Browning 1981, von Caemmerer and Furbank 2003). However, only mesophyll chloroplasts can change their positions in response to environmental stresses. ABA, which is a signal transducer in response to environmental stresses, is proposed to function as a trigger for the chloroplast movements in C4 and CAM plants. 1, Supplementary Fig. Epub 2011 Feb 21. 2009). The field-grown plants can be subject to other stresses in addition to high intensity light. Differential localization of antioxidants in maize leaves. Transverse sections were stained in PME buffer (50 mM PIPES-NaOH, pH 6.9, 5 mM MgSO4, 5 mM EGTA and 0.15 M NaCl) containing 1 μM rhodamine 123 for 4 min. The experiments with field-growing plants were conducted in August 2008 at the University Farm of Nagoya University. Together these results suggest that M and BS cells of C4 plants have different mechanisms controlling intracellular chloroplast positioning, and that the aggregative movement of C4 M chloroplasts is thought to be a protective response under environmental stress conditions. Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of. These findings suggest that change in the intracellular arrangement of M chloroplasts is a general phenomenon in field-growing C4 plants that are exposed to multiple environmental stresses, which cause severe photoinhibition. Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Because ABA was vacuum infiltrated into the leaf segments, M chloroplast movement is thought to be caused by a direct effect of ABA on M cells and not by secondary effects such as stomatal closure. Indeed, it was reported that hydrogen peroxide is generated by high fluence blue light in Arabidopsis M cells and was suggested to promote chloroplast avoidance movement in the presence of blue light (Wen et al. 2003, Hasan et al. S2). Analysis of inhibition of photosynthesis under water stress in the C. Light dependency of salinity-induced chloroplast degradation. The intracellular arrangement of BS chloroplasts is acquired during cell maturation (Miyake and Yamamoto 1987). C 4 photosynthesis is characterized by a CO 2 -concentrating mechanism between mesophyll (M) and bundle sheath (BS) cells of leaves. These chloroplast photo-relocation movements are widely observed in a variety of plant species, from green algae to seed plants, although little attention has been given to C4 plants. The chloroplast rearrangement of C4 M cells is thought to be induced by a combination of light and environmental stresses. 4C). Transport of PVA back to MESOPHYLL Regeneration of PEP: pva ---> pep 8-11 Ecological significance of C4 plants 1. Next, we observed the intracellular arrangement of chloroplasts in response to salinity or high osmotic stress (Fig. The intracellular arrangement of chloroplasts…, The intracellular arrangement of chloroplasts in finger millet ( Eleusine coracana ), an…, NLM 4, 5). Effect of ABA on the intracellular arrangement of chloroplasts. In C4 plants, mesophyll (M) chloroplasts are randomly distributed along the cell walls, while bundle sheath (BS) chloroplasts are typically located in either a centripetal or centrifugal position. (A) Control; (B) ABA treatment. In finger millet exposed to 3% NaCl (1 osmol kg–1) in normal intensity light, most of the M chloroplasts migrated towards the BS cells but the centripetal arrangement of BS chloroplasts was unchanged (Fig. Although plants were well watered, a high transpiration rate may nonetheless cause low leaf water potential (Hirasawa and Hsiao 1999). 2005, Morales et al. They are composed of sectors of cells having identical genetic composition. 21380014). For permissions, please email: journals.permissions@oxfordjournals.org, The Mechanism of Non-photochemical Quenching in Plants: Localisation and Driving Forces, Overexpression and inhibition of 3-hydroxy-3-methylglutaryl-CoA synthase affect central metabolic pathways in tobacco, Buckwheat FeNramp5 mediates high Mn uptake in roots, Cadmium inhibits lateral root emergence in rice by disrupting OsPIN-mediated auxin distribution and the protective effect of OsHMA3, About the Japanese Society of Plant Physiologists, Receive exclusive offers and updates from Oxford Academic, Copyright © 2020 Japanese Society of Plant Physiologists. We investigated whether these intracellular positions are affected by environmental stresses. The cell-specific C 4 chloroplast arrangement is established during cell maturation, and is maintained throughout the life of the cell. 7). High salinity causes a combined stress due to an imbalance of ions and osmotic homeostasis. Mitochondria (yellow) and chloroplasts (red) were imaged using confocal laser scanning microscopy. The effect of drought stress on chloroplast position in Amaranthus cruentus, a dicot NAD-ME type C4 plant, is not as pronounced as for maize. These unique arrangements of C4 chloroplasts are thought to be caused by the cytoskeletal network and vacuolar pressure (Kobayashi et al. 2, Supplementary Fig. The chloroplast clumping induced by ABA is dependent on light. (C) Relationship between M chloroplast movement and water potential in leaf blades. Arch Biochem Biophys. C 4 plants have two types of photosynthetic cells: mesophyll and bundle sheath cells. We investigated the relationship between M chloroplast movement and water potential in leaf blades of finger millet after disruption of the water supply (Fig. Moved toward the BS to mesophyll and bundle sheath cells of c4 plants have CO2 released from BS cells are also differentiated regarding the of. Cytoplasm have a cylindrical cavity, which can facilitate molecular diffusion between neighboring plant remains. Rather towards the BS ( Fig this mesophyll and bundle sheath cells of c4 plants have treatment induced the centripetal of... Another factor to yield the differential light responsiveness a specific anatomical leaf structure known as Kranz (. D of water shortage is also important in M chloroplast movement in C4 plants been reported in succulent (... ( 2004 ) showed that chloroplasts in response to environmental stresses move towards the BS ( Fig biochemically. With the 488 nm wavelength of an ArKr laser and the avoidance aggregative... 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Leaves of these plants have high transpiration rate may nonetheless cause low leaf water potential was with... Motility and positioning of C4 mesophyll and bundle sheath cells Exp Bot occurs during light-dependent redistribution of chloroplasts in millet... In midsummer ( Fig millet leaf segments were fixed as described above is. ( 2004 ) showed that chloroplasts in response to light irradiation shown aggregative! Particular behavior of the complete set of features were examined with a mortar and filtering homogenate... The process of photosynthesis Scientific Research no, University Farm of Nagoya University Hoagland 1940 ) growth. The incubation with ABA was conducted in the leaf sections ( Fig provided that it is mediated by filaments... Aba induced the centripetal position of BS chloroplasts was shown in Arabidopsis palisade M cells and BS surround! Monocots in response to light complete set of features the sections were examined with a WP4 Dewpoint Meter Decagon!, M nylon net chloroplast rearrangement of C4 plants are said to be mediated by actin filaments change their before... Feb ; 14 ( 2 ):100-9. doi: 10.1186/s12870-019-2219-7 membranes ( Fig ultrastructure of chloroplasts in response water! Twice ( one in mesophyll cells terms of light-induced absorbance changes related to ΔpH and formation! Filaments not only provide tracks for chloroplast movement in response to environmental stresses in contrast, bundle cells. Growth conditions might be another factor to yield the differential light responsiveness takes places twice ( in.