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Clumping and Dispersal of Chloroplasts in Succulent Plants

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Clumping and Dispersal of Chloroplasts in Succulent Plants Planta (2004) 219: 500–506 DOI 10.1007/s00425-004-1252-3 ORIGINAL ARTICLE Ayumu Kondo Æ Jun Kaikawa Æ Toru Funaguma Osamu Ueno Clumping and dispersal of chloroplasts in succulent plants Received: 23 October 2003 / Accepted: 21 January 2004 / Published online: 3 April 2004 Ó Springer-Verlag 2004 Abstract Plants have evolved various photoprotective the photosynthetic apparatus, causing photoinhibition. mechanisms to mitigate photodamage. Here we report This occurs when the absorbed light energy exceeds the the diurnal movement of chloroplasts in the leaves of capacity for photosynthetic light use and thermal dissi- succulent crassulacean acid metabolism (CAM) plants pation of the excess (Long et al. 1994; Cornic and under combined light and water stress. In leaves of Masacci 1996; Niyogi 1999). However, plants are water-stressed plants, the chloroplasts became densely equipped with various photoprotective mechanisms to clumped in one or sometimes two areas in the cytoplasm mitigate photodamage (Demming-Adams and Adams under light and dispersed during darkness. The chloro- 1996; Niyogi 1999). plast clumping resulted in leaf optical changes, with a Plants have acquired light-regulated systems that decrease in absorptance and an increase in transmit- operate widely from the organ level to the cellular level. tance. The plant stress hormone abscisic acid induced Of these, the phenomenon of chloroplast movement has chloroplast clumping in the leaf cells under light. We long been recognized, in which the arrangement of suggest that the marked chloroplast movement in these chloroplasts in cells changes in response to light direc- CAM plants is a photoprotective strategy used by the tion and intensity (see review by Wada et al. 2003 and plants subjected to severe water stress. references therein). Under high light intensity, chlorop- lasts settle beside the cell wall in the area where exposure Keywords Abscisic acid Æ Chloroplast movement Æ to light is minimal, and under low light intensity they Photoinhibition Æ Succulent plant Æ Water stress settle in the area of the cell where light exposure is maximal. This chloroplast movement has a marked ef- Abbreviations ABA: Abscisic acid Æ CAM: Crassulacean fect on the absorption of light (Brugnoli and Bjorkman acid metabolism 1992; Terashima and Hikosaka 1995; Park et al. 1996; Gorton et al. 1999). Recently, the mechanism regulating chloroplast movement has been studied at a molecular level in mutants of Arabidopsis thaliana that are defec- Introduction tive in chloroplast avoidance movement (Jarillo et al. 2001; Kagawa et al. 2001; Oikawa et al. 2003; Wada For plants, light is not only an energy source for et al. 2003). It has also recently been demonstrated that assimilating CO2 in photosynthesis, but also an essential the avoidance response under strong light plays a role in signal factor for differentiation and morphogenesis (Lin protection against photoinhibition (Kasahara et al. 2000). However, excessive amounts of light may damage 2002). In plants growing in natural environments, however, one would expect chloroplast movement to be modulated in a more complex manner by environmental O. Ueno (&) factors other than light intensity. Water stress is known Plant Physiology Department, to be one of the factors that intensify the effects of National Institute of Agrobiological Sciences, photodamage (Long et al. 1994; Cornic and Masacci Tsukuba, Ibaraki 305-8602, Japan 1996). E-mail: [email protected]ffrc.go.jp Fax: +81-29-8387417 Here we report marked chloroplast movement in leaves of succulent crassulacean acid metabolism (CAM) A. Kondo Æ J. Kaikawa Æ T. Funaguma Faculty of Agriculture, plants under combined light and water stress. We sug- Meijo University, Tempaku-ku, gest that this phenomenon represents a morphological Nagoya 468-8502, Japan photoprotective mechanism in leaves. 501 sodium phosphate (pH 6.8) were hand-sectioned with a Materials and methods razor blade and used for light microscopy. Plant materials and growth conditions Measurement of leaf optical properties Eight species with thick, succulent leaves were used for the water stress experiment (Table 1). Zygocactus Both transmittance (T) and reflectance (R) were mea- truncatus belongs to the Cactaceae, and the other seven sured by use of a spectrophotometer with an integrating species to the Crassulaceae. Each plant was propagated sphere (Hitachi 340S). Absorptance (A) was calculated vegetatively in a 3-l pot filled with a mixture of field soil from the measured values of T and R as A=1)(T+R). and leaf mold (7:3, v/v) and set in a greenhouse for Leaves from well-watered and water-stressed plants of several months from spring to summer. The plants were Z. truncatus and K. blossfeldiana, which differ from each then transferred to a growth chamber maintained at 30/ other in chloroplast arrangement but are almost the 20°C (light/dark temperature) and grown under well- same in chlorophyll content per unit leaf area and leaf watered conditions for 1 month. Photon irradiance, ) ) thickness, were used for measurement. provided by metal-halide lamps, was 300 lmol m 2 s 1 (14 h light). Subsequently, some plants were subjected to water stress by withholding water. Four herbaceous species were also grown under the same conditions ABA treatment of leaf segments (Table 1). For the abscisic acid (ABA) experiment, plants of Leaves of well-watered K. fedtschenkoi and K. blossfel- Kalanchoe¨ fedtschenkoi and K. blossfeldiana were grown diana plants, in which the chloroplasts were dispersed, in hydroponic pots (3 l) containing Hoagland’s solution were cut into small segments (5 mm·10 mm). Immedi- diluted to 1:5 in water. Air was bubbled through the ately, the leaf segments were floated on a 5-lM aqueous nutrient solution, which was renewed once a week. The solution of ABA ([±]-cis, trans-isomers; Wako Pure pots were placed in the growth chamber. The ABA Chemical Industries, Osaka, Japan) in the dark or under experiment was performed after about 1 month of ) ) light (photon irradiance 200 lmol m 2 s 1)at30°C. In hydroponic culture. the controls, the ABA solution was replaced by distilled water. Leaves from which either side or both sides of the epidermis had been peeled off were also examined. Light and electron microscopy Small segments of leaves were vacuum-infiltrated with fixative (3% glutaraldehyde in 50 mM sodium phos- Results phate, pH 6.8) for about 5 min and fixed for 1.5 h. They were then washed in phosphate buffer and post-fixed in The eight succulent species (Table 1) had thick leaves 2% OsO4 in buffer. After the segments had been dehy- composed of large, spherical, vacuolated mesophyll cells drated through an acetone series, they were embedded in as shown for K. fedtschenkoi (Fig. 1a,b), Zygocactus Spurr’s resin, as described previously (Kondo et al. truncatus (Figs. 1c, 2a) and K. blossfeldiana (Fig. 3). The 1998). Ultrathin sections were stained with uranyl ace- mesophyll was not clearly differentiated into palisade tate and lead citrate and observed under an electron and spongy parenchyma, and intercellular spaces were microscope (Hitachi 7100U; Hitachi, Tokyo, Japan). scarce (Figs. 1, 2, 3; cf. also Kondo et al. 1998; Borland Semithin sections were stained with toluidine blue O. et al. 2000). In the leaves of well-watered plants, chlo- Leaf segments fixed in 3% glutaraldehyde in 50 mM roplasts were always dispersed in the peripheral cytosol Table 1 Leaf characteristics Species Leaf Chloroplast and occurrence of chloroplast a clumping in the plants characteristic clumping examined in this study Crassula argentea Thunb. Succulent + Kalanchoe¨ blossfeldiana Poelln. Succulent + K. daigremontiana Ham. et Perr. Succulent + K. fedtschenkoi Ham. et Perr. Succulent + K. hildebrandtii Baill. Succulent + K. pinnata (Lam.) Pers. Succulent + Sedum rubrotinctum R. T. Clausen Succulent + Zygocactus truncatus (Haw.) K. Sch. Succulent + Fagopyrum esculentum Moench (buckwheat) Non-succulent ) Oryza sativa L. (rice) Non-succulent ) Pisum sativum L. (pea) Non-succulent ) a (+) Chloroplast clumping; ()) Zea mays L. (maize) Non-succulent ) no chloroplast clumping 502 Fig. 1a–c Comparison of chloroplast arrangements during the light period in leaves of succulent plants grown with adequate water (a) and under water stress (b,c). a,b Mesophyll cells of Kalanchoe¨ fedtschenkoi with (a) dispersed and (b) clumped chloroplasts. c Mesophyll cell of Zygocactus truncatus with clumped chloroplasts. CC Clumped chloroplasts, DC dispersed chloroplasts, E epidermis. Bars =50lm of the mesophyll cells (Figs. 1a, 2a,d). However, in the greater than that of reflectance. Similar results were also leaves of water-stressed plants, the chloroplasts became obtained from leaves of Kalanchoe¨ blossfeldiana with densely clumped in one, or sometimes two, areas of the dispersed and clumped chloroplasts (data not shown). cytoplasm under light (Figs. 1b,c, 2b,c,e). The intracel- The plant hormone ABA is known to play a central lular locations of the clumps of chloroplasts varied, and role in mediating plant responses to abiotic environ- the clumps were frequently found close together at mental stresses, including water stress (Hartung and adjoining cells (Fig. 2b,e). Sometimes a clump of chlo- Davies 1991; Rock 2000). When 5 lM of ABA was roplasts formed at the boundaries of two or three absorbed through the roots of K. fedtschenkoi and adjacent cells (Fig. 2c,e). The nucleus was often local- K. blossfeldiana plants grown in hydroponic culture, ized within the clump (Fig. 2b,c), whereas the mito- clumping of leaf chloroplasts was observed at about chondria were distributed in the peripheral cytosol day 1 (data not shown). To confirm whether ABA di- (Fig. 2e,f) as well as in the clumps of chloroplasts rectly induced the clumping of chloroplasts, we floated (Fig. 2e,g). We found no indication of cellular damage leaf segments of well-watered Kalanchoe¨ plants on a by water stress, such as plasmalemma or tonoplast 5-lM aqueous solution of ABA (Fig. 6). We observed breakdown, or organelle disruption, although vesicles of chloroplast clumping in the leaf segments after about 3 h various sizes occurred more frequently in the cytosol of under light (Fig.
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