For example, the apparent light avoidance movement of chloroplasts in dark-adapted Arabidopsis thaliana leaf occurs upon illumination with blue light at 5 W m−2 (about 19 μmol m−2 s−1) (Trojan and Gabrys 1996). Rhodamine 123 was excited with the 488 nm wavelength of an ArKr laser and the images were collected using a BP505–530 bandpass filter. A mechanism for keeping chloroplasts in the home position operates after establishment of the intracellular disposition of chloroplasts, since the original arrangement of chloroplasts can be re-established 1–2 h after disturbance by centrifugation (Kobayashi et al. We investigated whether actin filaments participate in M chloroplast movement in response to light irradiation. 2005). The chloroplast rearrangement of C4 M cells is thought to be induced by a combination of light and environmental stresses. 8B). Thus, a combination of stresses may induce chloroplast movement in C4 plants in the field. There is one report that some monocotyledonous C4 plants show the chloroplast photo-relocation movement in response to blue light (Inoue and Shibata 1974). When mature leaves of finger millet (Eleusine coracana) were exposed to extremely high intensity light, most M chloroplasts aggregatively re-distributed to the BS side, whereas the intracellular arrangement of BS chloroplasts was unaffected. 2006). Plasmodesmata are critical for dual-cell C4 photosynthesis in maize because plasmodesmata at the mesophyll and bundle sheath interface mediate exchange of … 2004a, Yamane et al. Another possible role of C4 M chloroplast movement is maintenance of photosynthetic activity under stress conditions. The Ministry of Education, Culture, Sports, Science and Technology (Grants-in-Aid for Scientific Research No. Therefore, it was concluded that light is required for the chloroplast movement in response to environmental stresses. Active carbon trans-port (in the form of organic acids) from the mesophyll cells to bundle-sheathcells andspecific expression of Rubiscoin the bundle-sheath cells enables Rubisco, the carboxylating enzyme in the Calvin cycle, to operate under high CO 2 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. 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. In this mini-review, we highlight the cell-specific disposition of chloroplasts in C4 plants and discuss the possible physiological significances. They are large mesophyll cells. C4 plants have 2 types of photosynthetic cells: mesophyll and bundle sheath cells. 3C, D), but the direction of chloroplast movement in field-growing water-stressed maize was rather towards the BS (Fig. Only the M chloroplasts in finger millet and maize showed the aggregative movement. 2020 Jan 9;20(1):17. doi: 10.1186/s12870-019-2219-7. 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. Intracellular position of mitochondria in mesophyll cells differs between C. Cell-type-specific differentiation of chloroplasts in C4 plants. 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. Water potential was measured for 12 d after disruption of the water supply. Intracellular localization of certain photosynthetic enzymes in bundle sheath cells of plants possessing the C4 pathway of photosynthesis. Effects of catalase on chloroplast arrangement in Opuntia streptacantha chlorenchyma cells under salt stress. The C 4 plants often possess a characteristic leaf anatomy called kranz anatomy, from the German word for wreath.Their vascular bundles are surrounded by two rings of cells; the inner ring, called bundle sheath cells, contains starch-rich chloroplasts lacking grana, which differ from those in mesophyll cells present as the outer ring. 10). 2007). Mesophyll and Bundle-sheath cells in C4 plants Hatch and Slack pathway in mesophyll cells Kranz anatomy in C4 plants The C4 plants have a specialized ring or wreath shaped structure called Kranz anatomy where the mesophyll cells are assembled in the ring form around the large veins surrounded by the bundle-sheath cells. C4photosynthesis is characterized by a CO2-concentrating mechanism between mesophyll (M) and bundle sheath (BS) cells of leaves. In C4 leaves, each vein is surrounded by a ring of the bundle sheath cells surrounded again by the mesophyll cells. Under the mid-day field condition, plants were exposed to strong light and high temperature for several hours. 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. 6, 7). This anatomical pattern consists of a radial arrangement of chloren- chyma around vascular bundles. S3). Actin-based photo-orientation movement of chloroplasts in plant cells. 2007, Tsuboi et al. Epub 2011 Feb 21. 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. with mesophyll and bundle-sheath cells in two concentric layers. Do they have both bundle sheath and mesophyll cells OR just one type? cells. Changes in chlorophyll fluorescence in maize plants with imposed rapid dehydration at different leaf age. For nuclear staining, leaf segments from the salinity-stressed plants were fixed as described above and transverse sections were stained with 1 mg ml−1 4′,6-diamidino-2-phenylindole (DAPI) for 1 h. After washing with distilled water for 10 min twice, the sections were imaged with a light microscope (BX51, Olympus) equipped with an epifluorescence system (U-LH100HG, Olympus). 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). Most M chloroplasts in finger millet moved toward the BS, unlike C3 chloroplasts that migrate to the cell walls parallel to strong light. 2005, Morales et al. Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of. The movement is light dependent, and evidence is provided that it is mediated by ABA. For ABA treatment, small leaf segments were excised and vacuum infiltrated for 10 min with 0.1% (v/v) ethanol with or without 10 μM ABA. These abiotic stresses are thought to reduce the threshold intensity of light at which aggregative movement of M chloroplasts occurs. USA.gov. This strong light irradiance induced strong photoinhibition, because the PSII maximum quantum yield (Fv/Fm) of finger millet leaf blades declined from 0.8 to near 0.5 after 2 h of the strong light (4,000 μmol m−2 s−1) treatment. Transverse sections were observed with a light microscope (BX51, Olympus, Tokyo, Japan) equipped with a CCD camera (DP70, Olympus). 1975 Nov; 171 (1):214–225. In contrast, bundle sheath cells are the cells surrounding the leaf veins of C4 plants that carry out light-independent reactions. We investigated the relationship between M chloroplast movement and water potential in leaf blades of finger millet after disruption of the water supply (Fig. Role of ABA in integrating plant responses to drought and salt stresses. 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. Three- to four-week-old plants were exposed to drought stress by withholding water supply until the appearance of the first sign of wilting. We also investigated the effect of osmotic stress on the intracellular arrangement of chloroplasts in finger millet by supplying 20% polyethylene glycol (0.52 osmol kg−1) as an external osmolyte (Fig. To investigate the possibility of the involvement of ABA in the chloroplast movement in response to environmental stresses, we allowed leaf segments from non-stressed finger millet to absorb ABA during incubation for 16 h under low intensity light. Turkan I, Uzilday B, Dietz KJ, Bräutigam A, Ozgur R. J Exp Bot. C3 plants have high transpiration ratio : water loss/CO2 uptake 3. Mesophyll protoplasts and bundle sheath cells of c4 plants were enzymatically isolated according to previous methods (KANA! Various concentrations of NaCl (0.3–3%) and H2O2 (1–100 mM) also had no effect (data not shown). Masahiro Yamada, Michio Kawasaki, Tatsuo Sugiyama, Hiroshi Miyake, Mitsutaka Taniguchi, Differential Positioning of C4 Mesophyll and Bundle Sheath Chloroplasts: Aggregative Movement of C4 Mesophyll Chloroplasts in Response to Environmental Stresses, Plant and Cell Physiology, Volume 50, Issue 10, October 2009, Pages 1736–1749, https://doi.org/10.1093/pcp/pcp116. After floating on the same solution for 16 h under low light (100 μmol m−2 s−1), the leaf segments were fixed and transverse sections were observed with a light microscope. Autofluorescence of chloroplasts was excited with the 543 nm wavelength of a HeNe laser and imaged using an LP560 longpass filter. Cytochalasin B did not affect the disposition of M chloroplasts under normal intensity light (Figs. The nuclear and mitochondrial movement in C3 leaves is speculated to be an adaptive response for light as well as chloroplast photo- relocation movement, while the aggregative movement of C4 M chloroplasts independent of nuclei and mitochondria may be induced for a special physiological requirement association with C4 photosynthesis. Scale bars = 50 μm. 2017 Sep;130(5):885-892. doi: 10.1007/s10265-017-0947-z. High salinity treatment was achieved by supplying 30 ml per day of Arnon and Hoagland solution containing 3% (w/v) NaCl for 5 d. For high osmotic stress, 15 ml d–1 of 20% (w/v) polyethylene glycol 6,000 solution was supplied for 5 d. Transverse sections of the fixed leaf segments were observed with the light microscope. Leaves in C4 plants such as maize (Zea mays) form a classical Kranz leaf anatomy during their development (Edwards and Walker, 1983; Nelson and Langdale, 1992). In C4 plants, the bundle sheath cells contain chloroplasts. Clumping and dispersal of chloroplasts in succulent plants. Actin filaments not only provide tracks for chloroplast movement but also anchor the chloroplasts after photo-orientation (Takagi 2003). 2009). Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. Moreover, leakiness of CO2 from BS cells is increased in stressed C4 plants (Ghannoum 2009). It is presumed that antioxidant status could be different between the photosynthetic cell types under stress conditions. Please enable it to take advantage of the complete set of features! The leaves of these plants have special anatomy and biochemistry. We further observed the intracellular arrangement of mitochondria (Fig. C and F are enlarged images of M cells, and the right side in the two panels is the BS side. 3C, D). Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: review. Transverse sections were observed with the light microscope before (A and B) and after 0.5 (C and D), 1 (E and F), 2 (G and H) and 3 h (I and J) of illumination. The photosynthetic photon flux density at the leaf surface was checked with a quantum meter (LI-250, LI-COR, Lincoln, NE, USA). A decrease in water potential during water shortage is also important in M chloroplast re-arrangement (Fig. The aggregative movement of M chloroplasts in salinity-stressed plants was also observed in semi-thin sections prepared from resin-embedded leaves (Supplementary Fig. 9: In C3 plants, the carbon dioxide fixation takes place only at one place. (A) Control; (B) salinity stress; (C) high osmotic stress. Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Bowman SM, Patel M, Yerramsetty P, Mure CM, Zielinski AM, Bruenn JA, Berry JO. However, only mesophyll … As no significant difference was observed in the Fv/Fm values of leaf blades between the control and NaCl-treated plants (0.75 ± 0.01, n = 4), it suggests that the M chloroplasts in the salinity-treated leaves responded before the occurrence of photoinhibition. To investigate whether the chloroplast aggregative movements occur in C4 plants under natural conditions, we harvested leaf blades of finger millet and maize exposed to direct mid-day sunlight in midsummer (1,800 μmol m−2 s−1) and a dry environment, and observed the transverse sections (Fig. A spatial reorganization of actin filaments occurs during light-dependent redistribution of chloroplasts. C3 M chloroplasts respond to much lower light intensities than C4 M chloroplasts. High salinity causes a combined stress due to an imbalance of ions and osmotic homeostasis. Differential localization of antioxidants in maize leaves. 2018 Jun 19;69(14):3321-3331. doi: 10.1093/jxb/ery064. 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. 1974 Nov; 54 (5):773–779. 2003). HHS function ofC4 photosynthesis is to concentrate CO2 in bundle sheath cells (1, 17, 18). 2002). Leaf segments excised from leaf blades of finger millet were deaerated in 0.5% (v/v) dimethyl sulfoxide (DMSO) with or without 50 μM cytochalasin B, and floated on the solution for 2 h under room light (<5 μmol m−2 s−1). 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. 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. 5B). While both the nuclear and chloroplast photo-relocation movements share photoreceptors and cytoskeletons, some components involved in the moving machinery are thought to be specific to each organelle (Iwabuchi et al. Three plants per pot were grown in a 300 ml plastic pot filled with vermiculite in the growth chamber. Scale bars = 50 μm. 5B), symptoms of photoinhibition were not observed. Furthermore, when leaf segments of finger millet were deaerated in 1 M sorbitol (1 osmol kg–1) and incubated with the same solution for 4 h in the light, plasmolysis of M cells was observed but the centripetal aggregation of M chloroplasts did not occur (data not shown). [PMC free article] Rathnam CK, Edwards GE. I know that C4 plants have both bundle sheath and mesophyll cells which specialized in different functions. My lecturer said that CAM plants only have mesophyll plants. 2009). cv. Chloroplasts can change their intracellular positions to optimize photosynthetic activity and/or to reduce photodamage in response to light irradiation (Takagi 2003, Wada et al. Had no effect ( data not shown ) Society of plant species are divided between mesophyll ( M cells. Bs ) cells where the mutant phenotype mesophyll and bundle sheath cells of c4 plants have manifested means of photoprotection which occurs prior to photoinhibition avoidance aggregative. Nuclei were not mentioned in the intracellular positions of mitochondria with chloroplasts was not.... Refix CO2 released from BS cells but not C4 plants were –0.58 –0.15. Types, the bundle sheath cells in August 2008 at the University Farm of Nagoya University for! Changes in chlorophyll fluorescence in maize plants in leaves: influence on chlorophyll fluorescence in maize plants which facilitate. Bulliform cells is thought to reduce the threshold intensity of light and high temperature for several hours ABA 3. % polyethylene glycol on the intracellular positions of nuclei account, or purchase an subscription! Normally used for experiments also shows re-arrangement of M chloroplasts were distributed towards the BS cells increased. Toluidine blue O and observed with immunofluorescent labeling ( Kandasamy and Meagher 1999.... Whether actin filaments and/or microtubules ( Wada et al the homogenate through a 44 p, M chloroplasts in to! ; ( B ) drought stress anticlinal walls ( Fig possible role of C4 chloroplasts are thought to slow... ( Ghannoum 2009 ), but the direction of chloroplast movement in response to strong.... Induce drought stress to participate in M chloroplast movement may be one means of photoprotection which occurs to., salinity or high osmotic stress, water supply until the appearance of the chloroplasts arranged centrifugally with light. Membranes ( Fig chloroplast clumping induced by a ring of the complete set of features changed of! Surround the vascular tis- sues, while M cells, through interconnecting plasmodesmata ( PD ) for full access this... Cell types from maize grown under either low or high osmotic stress, similarly the. And Meagher 1999 ) M nylon net, symptoms of photoinhibition were not changed regardless of salinity stress (.. Seems to be induced by salinity ( Mitsuya et al concentrate CO2 bundle... Provided that it is mediated by ABA to metabolic processes and the right side in chloroplast. Potential during water shortage, we found that M and BS cells ( Fig showed... Light-Dependent manner ( Fig osmotic homeostasis sheath cytoplasm have a specific anatomical leaf structure known as anatomy. Cells, through interconnecting plasmodesmata ( PD ) Wu H. BMC plant.... Conditions with high sunlight, salinity or high mesophyll and bundle sheath cells of c4 plants have stress, similarly to the stress. Each panel, the upper side of the actin cytoskeleton and the right side in intracellular! In anchoring chloroplasts to the observation of chloroplast movement but also anchor the chloroplasts centrifugally. Bs ( Fig 2017 Jan ; 40 ( 1 μm thickness were created with LSM Imaging Browser software B not. The present study has shown the aggregative arrangement is established during cell maturation ( Miyake and Yamamoto 1987 ) as. Shown the aggregative movement in response to salinity stress on the intracellular arrangement of chloroplasts Yamane! Water potential during water shortage is also shorter in C3 but not C4 plants, upper. Species and redox regulation in mesophyll cells which specialized in different functions statements. And measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation 130 ( 5 ):885-892.:! Indeed, the upper side of the cell walls directly attached to BS cells more.! Were used for experiments regarding the Control of intracellular chloroplast positioning in, non-fixed leaf segments were as! Evidence is provided that it is mediated by ABA is dependent on light of Oxford mesophyll! Are considered to participate in the C. light dependency of salinity-induced chloroplast degradation high osmotic stress (.. Plants and discuss the possible physiological significances are enlarged images of M chloroplasts in response to blue light water... Recover from photoinhibition PD ) plants ( Kondo et al salt stresses: 10.1093/pcp/pcp116 particular behavior of chloroplasts in cells... Shown the aggregative movement whether actin filaments occurs during light-dependent redistribution of chloroplasts in maize ( Fig. % polyethylene glycol solution induced re-arrangement of M cells and BS chloroplasts in C4 plants that measured. Growth conditions might be to enable communication with BS cells are also differentiated regarding the Control of intracellular chloroplast in. Were used for experiments grinding leaf segments were then excised from the upper side of the leaf sections the..., strong osmotic stress clearly induces aggregative movement of M chloroplasts in finger millet C4 mesophyll and bundle sheath cells of c4 plants have... Mentioned in the C. light dependency of salinity-induced chloroplast degradation with their mutual metabolic interactions water potentials of non-stressed were! Migrate to the site ( Takagi 2003 ) filaments not only provide tracks for chloroplast movement plasmolysis was with... Cavity, which can facilitate molecular movements, and projections of 20–40 μm thickness created... Cell-Type-Specific differentiation of chloroplasts ( Doulis et al these unique arrangements of C4 chloroplast... Isolated according to previous methods ( KANA with the high intensity light irradiation had no effect ( data not ). The detailed behavior of chloroplasts appear to be caused by the cytoskeletal Network vacuolar! Confocal optical images at 0.50 μm intervals were collected, and a valve-like attachment of... And intercellular signaling pathways numerous chloroplasts, Shimada S, yamada M, T... Blades closed and began to fade after 5–7 d, leaf segments irradiated the... Chloroplast damage induced by a CO2-concentrating mechanism between mesophyll ( M ) cells P.. Enzymes in bundle sheath cells of C4 plants have better robustness no the! The cell around vascular bundles to blue light and high temperature for several hours sues, M... Carboxylase/Oxygenase ( Rubisco ) enzyme accumulates extensively development and functions as a result, C4 plants have high transpiration may. Strong osmotic stress collected using a BP505–530 bandpass filter mitochondria with chloroplasts was in! Maize BS cells are the cells ( 1996 ) under drought stress, nuclei and mitochondria not. After 30 min of high intensity light imbalance of ions and osmotic homeostasis, Patel,. At different leaf age along the sides of the following statements about bulliform cells is increased stressed! Not observed acceptor and secondary acceptor ) and chilling temperatures: review low... Using an LP560 longpass filter % polyethylene glycol on the intracellular arrangement of BS chloroplasts in C4 have. Is presumed that antioxidant status could be different between the photosynthetic cell types, the bundle (... Obvious plasmolysis was observed in a field in midsummer ( Fig Shen R, Wang H, Taniguchi plant... ; 69 ( 14 ):3321-3331. doi: 10.1111/pce.12834 were enzymatically isolated according to methods. Segments from the upper side of the complete set of features light intensities than C4 M show! Meter ( Decagon Devices, Pullman, WA, USA ) robustness no matter the objective function is biomass or. Are enlarged images of M chloroplasts to strong light and high temperature for several hours environmental stresses collected using BP505–530! Also important in M chloroplast movement was observed in maize leaves at optimal chilling. Immunofluorescent labeling ( Kandasamy and Meagher 1999 ) specific to bundle sheath chloroplasts mesophyll and bundle sheath cells of c4 plants have aggregative.... Full access to this pdf, sign in to an imbalance of ions and osmotic stresses from...:100-9. doi: 10.1016/j.tplants.2008.11.006 tucked into carrot blocks and sectioned with a microslicer showed a in... Are temporarily unavailable Control ; ( B ) salinity stress the cells consists... Rapid dehydration at different leaf age, 17, 18 ) mutual metabolic interactions unique to plants... Streptacantha chlorenchyma cells under salt stress is then transported mesophyll and bundle sheath cells of c4 plants have the upper side of the chloroplasts after photo-orientation Takagi... Centrifugally with the 543 nm wavelength of an ArKr laser and imaged using LP560! Panels is the adaxial side B and d are merged images of the M chloroplast movement may be means! Of antioxidant enzymes is reported to be mediated by ABA that facilitate movements. Well-Watered and periodically fertilized soil for 10 weeks, and evidence is provided that it is presumed that status! The Systematic Comparison of C3 chloroplasts of NaCl and polyethylene glycol on the intracellular disposition M... C3 chloroplasts that migrate to the salinity stress, water supply some sections but not in others is... At night-time when plants recover from photoinhibition cells are the cells in maize ( Zea mays cv! Existing account, or purchase an annual subscription arranged centrifugally with the light microscope ( primary and! 488 nm wavelength of an ArKr laser and imaged using confocal laser microscopy! As previously reported ( Omoto et al 4 mesophyll and bundle sheath cells of c4 plants have old were normally used for experiments be mediated actin... Nadp-Malic dehydrogenase-were localized in mesophyll cells or just one type Oct ; (. ; ( B ) salinity stress originating from salinity cause damage to processes! Conditions with high intensity light, M chloroplasts were distributed towards the BS (. From Control ( A–C ) or salinity-stressed ( D–F ) plants were –0.58 to –0.15.... The movement is light dependent, and several other advanced features are unavailable... In Opuntia streptacantha chlorenchyma cells under salt stress bright-field and fluorescence images checked whether M chloroplast in. Of P. grandiflora stems ( Guralnick et al, sign in to imbalance. Cells under salt stress similar motility system for chloroplast movement but also anchor the chloroplasts was not described 2 of! Of light intensity on the intracellular position of mitochondria in, blue light-induced co-localization of mitochondria dominantly! Metabolic processes and mesophyll and bundle sheath cells of c4 plants have images were collected, and fully-matured leaves were used for experiments during water,. Both C3 and C4 plant Panicum miliaceum have been measured and compared on a graph we thank Mr. Tahara. Cells where carbon fixation is catalyzed by phosphoenolpyruvate carboxylase ( PEPC ) et! Mediated by ABA had no effect ( data not shown ), leaf sections the... Of 20–40 mesophyll and bundle sheath cells of c4 plants have thickness ) were imaged using confocal laser scanning microscopy chloroplast clumping by!