sign in sign up
<<
Home , Plant hormone, Sedum rubrotinctum, Tradescantia

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 in succulent

Received: 23 October 2003 / Accepted: 21 January 2004 / Published online: 3 April 2004 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 of capacity for photosynthetic light use and thermal dissi- succulent crassulacean acid (CAM) plants pation of the excess (Long et al. 1994; Cornic and under combined light and water . 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 mitigate photodamage (Demming-Adams and Adams under light and dispersed during darkness. The chloro- 1996; Niyogi 1999). plast clumping resulted in optical changes, with a Plants have acquired light-regulated systems that decrease in absorptance and an increase in transmit- operate widely from the level to the cellular level. tance. The stress induced Of these, the phenomenon of 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 in the area where exposure Keywords Abscisic acid Æ Chloroplast movement Æ to light is minimal, and under low light intensity they Photoinhibition Æ 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 , 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 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 , 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 (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 . 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 20C (light/dark temperature) and grown under well- same in 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 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)at30C. In hydroponic culture. the controls, the ABA solution was replaced by distilled water. Leaves from which either side or both sides of the 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 + 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 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. 6b). No clumping was found in leaf leaves of water-stressed plants (Fig. 2e) than in that segments floated on distilled water under light (Fig. 6a) of leaves of well-watered plants (Fig. 2d). The time or in those floated on a 5-lM aqueous solution of ABA taken for clumping to appear first differed by species and in darkness (Fig. 6c). The induction of chloroplast plant size but was generally more than 10 days under clumping by ABA under light also occurred in leaf seg- our growth conditions. ments without epidermis on one or both sides (Fig. 6d). The clumping phenomenon depended on light expo- These results suggest that ABA is involved in the sig- sure as well as water stress, because the chloroplast naling pathway leading to the clumping of chloroplasts arrangement changed diurnally. At the beginning of within mesophyll cells, but not via the stomatal effect. exposure of water-stressed plants to light, the chlorop- lasts were dispersed (Fig. 3a) but then began to clump (Fig. 3b). At the beginning of darkness the chloroplasts Discussion were clumped (Fig. 3c), but with continuous darkness they began to disperse again (Fig. 3d). When part of a It is unlikely that the clumping of chloroplasts was an leaf of a water-stressed plant was covered with alumi- artifact of the fixation process, because (i) fixative is num foil, clumped chloroplasts were found only in the rapidly absorbed in vacuum-infiltrated leaf tissues, and exposed region, not in the covered region (Fig. 4). (ii) the clumped chloroplasts were also observed under a We examined whether the clumping of chloroplasts light microscope in hand-cut sections of leaves prepared resulted in spectral changes in the light absorptance, rapidly without fixation (data not shown). In addition, transmittance, and reflectance of leaves (Fig. 5). Leaves leaves of water-stressed plants had generally a paler of Zygocactus truncatus showed high absorptance at all green colour than those of well-watered plants because wavelengths and a flattened spectral curve; these features of the chloroplast clumping; this has also been observed are characteristic of thick leaves (Moss and Loomis during studies of the chloroplast movement of other 1952). Leaves with clumped chloroplasts showed a de- plants (Park et al. 1996; Gorton et al. 1999; Kagawa crease in absorptance at all wavelengths compared with et al. 2001). The chloroplast movements that are induced leaves with dispersed chloroplasts. This occurred be- by changes in the light conditions (Figs. 3, 4) also indi- cause of a concomitant increase in both the transmit- cate that the clumping of chloroplasts is not caused by tance and reflectance of leaves with clumped cellular damage and is not an artifact that arises during chloroplasts. The contribution of transmittance was sample preparation. 503

Fig. 2a–g Comparison of chloroplast arrangements during the light period in leaves of Zygocactus truncatus grown with adequate water (a,d) and under water stress (b,c,e). a Mesophyll cells with dispersed chloroplasts. b Mesophyll cells with clumped chloroplasts. c Clumps of chloroplasts lying between two adjacent mesophyll cells. d Mesophyll cells with dispersed chloroplasts. e Mesophyll cells with clumped chloroplasts. The mitochondria are scattered in the peripheral cytosol, as well as in the clumps of chloroplasts. The locations enlarged in f and g are shown by rectangles. f Enlargement of rectangle in e, showing mitochondria in the peripheral cytosol. g Enlargement of another rectangle in e, showing clumped chloroplasts with mitochondria and peroxisomes. C Chloroplast, CC clumped chloroplasts, DC dispersed chloroplasts, mt mitochondrion, N nucleus, P peroxisome, Vc vesicle. Bars =50lm(a–c), 10 lm(d,e), 1 lm(f), 2 lm(g)

Many plants, including , mosses, , and The succulent plants examined here (Table 1) use CAM plants, exhibit variable amounts of chloroplast move- (Smith and Lu¨ ttge 1985; Kondo et al. 2000). For most of ment with changes in light intensity (reviewed in Haupt the daytime the stomata are closed, and the stored malic 1999; Wada et al. 2003). However, we did not find acid is decarboxylated to supply CO2 for photosynthesis chloroplast clumping in the leaves of the herbaceous within the leaves (Borland et al. 2000). Thus, succulent plants buckwheat, rice, pea, and maize (Table 1) when CAM plants have a high tolerance for dry environments. they were subjected to water stress. Their leaves withered CAM plants are also known to be subject to photoin- because of the severe water deficit. The leaves of the hibition (Borland et al. 2000), which may be amplified succulent plants, however, can survive under such con- under severe water deficits owing to the reduction in the ditions because they have traits that constrain water external uptake of CO2 caused by stomatal closure loss, such as small surface-to-volume ratio, low stomatal (Lu¨ ttge 2000). We conclude that the chloroplast move- frequency, a thick cuticle, and epidermal waxes (Os- ment found in the succulent plants is a photoprotective mond et al. 1999). When subjected to drought, plants mechanism within the leaf. However, it remains to be regulate their water loss via stomatal closure in order to solved whether CAM is directly involved in this maintain their water status (Cornic and Masacci 1996). phenomenon. 504

Fig. 3a–d Diurnal changes in chloroplast arrangement in leaves of In thick, succulent leaves, most light would be ab- a water-stressed plant of Kalanchoe¨ blossfeldiana. a At the sorbed. If chloroplasts are dispersed within the leaf, the beginning of the light period the chloroplasts are dispersed. b After 4 h of light, the chloroplasts are beginning to clump. c At upper cell layers might receive saturating and photoin- the beginning of the dark period (following 14 h of light) the hibitory amounts of light, but the cell layers located chloroplasts are completely clumped. d After 6 h of darkness the deeper within the leaf might receive sub-saturating chloroplasts have dispersed again. CC Clumped chloroplasts, DC quantities (Vogelman and Martin 1993; Terashima and dispersed chloroplasts, E epidermis, M mesophyll cell, VB vascular Hikosaka 1995; Gorton et al. 1999). In leaves with bundle. Bar = 100 lm clumped chloroplasts, however, light could penetrate to the deeper layers because of the sieve effect of the The occurrence of chloroplast clumping has already clumping. This might help to distribute the light more been observed in some other plants (Drew 1979; Vaughn evenly within the leaf and might have an additional ef- et al. 1990; Guralnick et al. 2002). In the submerged fect on light avoidance. seagrass Halophila stipulacea the clumping of chlorop- Our data demonstrate that the clumping of chlorop- lasts could contribute to the mitigation of photoinhibi- lasts does result in changes in leaf optical properties tion (Drew 1979). Our study demonstrates that the (Fig. 5). The degrees of spectral change observed in the clumping of chloroplasts results in a decrease in succulent plants studied here were somewhat lower than absorptance and increases in transmittance and reflec- those reported in some shade-adapted species of Oxalis tance in succulent leaves. Thus, it appears that less light and Marah, which have thin leaves with pronounced is trapped inside leaves with clumped chloroplasts, and chloroplast movement (Brugnoli and Bjorkman 1992). light avoidance may primarily come from a decreased total absorptance. With this particular arrangement, most of the chloroplasts in the clump may be also pro- tected from excessive light exposure by mutual shading.

Fig. 4 Cross-section of a leaf of a water-stressed plant of Kalanchoe¨ blossfeldiana, in which the right half of the leaf was shielded by aluminum foil (thick black bar) and the left half was exposed to Fig. 5 Absorptance (A), transmittance (T ), and reflectance (R)of light. Note that the chloroplasts in the right half are dispersed, leaves of Zygocactus truncatus with dispersed (solid lines) and whereas those in the left half are clumped. CC Clumped clumped chloroplasts (broken lines). The chlorophyll content was chloroplasts, DC dispersed chloroplasts, E epidermis, M mesophyll 46.5±1.2 and 47.6±0.7 lgcm)2 leaf area (means ± SD, n=3) in cell, VB . Bar = 200 lm leaves with dispersed and clumped chloroplasts, respectively 505

Fig. 6a–d Induction of clumping of chloroplasts in leaves of a well-watered plant of Kalanchoe¨ blossfeldiana by ABA. a Section from a leaf segment floated on distilled water for 3 h under light. b Section from a leaf segment floated on a 5-lM aqueous solution of ABA for 3 h under light. c Section from a leaf segment floated on a 5-lM aqueous solution of ABA for 3 h in darkness. d Section from a leaf segment without the adaxial and abaxial epidermises floated on a 5-lM aqueous solution of ABA for 3 h under light. CC Clumpedchloroplasts, DC dispersed chloroplasts, E epidermis. Bar = 50 lM

Presumably this fact is because of the thicker leaves of It has been shown that, in most plants, blue-light the succulent plants. photoreceptors are implicated in the mechanism of If a simple sieve effect caused by chloroplast movement chloroplast movement, whereas in some plants such as were occurring within the leaves with clumped chlorop- Mougeotia, Mesotaenium, Adiantum, and Physcomitrel- lasts, one would expect transmittance changes to peak la, is also involved in this mechanism (re- near the blue and red spectral regions owing to chloro- viewed in Haupt 1999; Wada et al. 2003). Calcium phyll absorption (Zurzycki 1961; Britz and Briggs 1987). have been implicated as an important signaling com- In our experiment, however, increases in transmittance at ponent following light absorption by both phytochrome a wavelength of around 550 nm in the green spectral re- and/or blue-light photoreceptors (Khurana et al. 1998). gion were also found in leaves with clumped chloroplasts, In the signaling pathway of chloroplast movement, too, as compared with leaves with dispersed chloroplasts. In calcium ions have been considered as a candidate for the contrast, almost no differences in reflectance between signal connecting photoreceptors and chloroplasts leaves with clumped and dispersed chloroplasts were (Haupt 1999; Tlalka and Fricker 1999; Wada et al. found in this spectral region. Anthocyanins show an 2003). Calcium ions have also been implicated as a absorption peak in the green region (peaking at 525 nm). second messenger for ABA signaling (Rock 2000). This substance is synthesized upon exposure to environ- Furthermore, an interaction of phytochrome action and mental stresses such as strong light and drought, confer- ABA has been found in the regulation of expression of ring the potential to mitigate photodamage (Neill and some genes in Lemna gibba (Weatherwax et al. 1996, Gould 2003). Thus, it would be difficult to relate the 1998). Currently, our understanding of the signaling spectral changes in the green region in water-stressed pathway of chloroplast movement is still rudimentary leaves of succulent plants to this substance. Changes in (Haupt 1999; Wada et al. 2003). Our study suggests that transmittance at around 550 nm similar to those in our the succulent plants have evolved this particular mor- succulent plants have also been observed in leaves of phological strategy to protect them against light stress Oxalis oregana and Marah fabaceus differing in chloro- combined with water stress. The findings may provide plast arrangement (Brugnoli and Bjorkman 1992) and a important clues to the signaling mechanisms underlying rainforest understorey plant, Alocasia macrorrhiza (Gor- chloroplast movement. ton et al. 1999), although it is not known why such changes in transmittance occur in these leaves. Acknowledgements We thank Akiko Higuchi, Kyoko Hirasawa, Closure of stomata can be induced by ABA (Hartung and Atsushi Kato (Meijo University) for their assistance with some and Davies 1991). The induction of chloroplast clump- aspects of this study; Haruhiko Ito (Nagoya Municipal Industrial ing by ABA in the succulent plants studied (Fig. 6) Research Institute) for technical assistance in the measurement of leaf optical properties; and Dr. Akihiro Nose (Saga University) for suggests that ABA is involved in the signaling pathway his encouragement. resulting in the clumping of chloroplasts within the mesophyll cells. Since the effect of ABA was also ob- served in leaf segments without epidermis and stomata (Fig. 6), ABA seemingly does not act via a stomatal References effect. As far as we know this is the first evidence indi- Borland AM, Maxwell K, Griffiths H (2000) Ecophysiology of cating that a plant hormone can induce chloroplast plants with crassulacean acid metabolism. In: Leegoods RC, movement, although the precise cellular mechanism re- Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiol- mains unknown. ogy and metabolism. Kluwer, Dordrecht, pp 583–605 506

Britz SJ, Briggs WR (1987) Chloroplast movement and light Lu¨ ttge U (2000) Light-stress and crassulacean acid metabolism. transmission in Ulva: the sieve effect in a light-scattering system. Phyton (Austria) 40:65–82 Acta Physiol Plant 9:149–162 Moss RA, Loomis WE (1952) Absorption spectra of leaves. I. The Brugnoli E, Bjorkman O (1992) Chloroplast movements in leaves: visible spectrum. Plant Physiol 27:370–391 influence on chlorophyll fluorescence and measurements of Neill SO, Gould KS (2003) Anthocyanins in leaves: light attenua- light-induced absorbance changes related to pH and zeaxanthin tors or antioxidants? Funct Plant Biol 30:865–873 formation. Photosynth Res 32:23–35 Niyogi KK (1999) Photoprotection revised: genetic and molecular Cornic G, Masacci A (1996) Leaf photosynthesis under drought approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333– stress. In: Barker NR (ed) Photosynthesis and the environment. 359 Kluwer, Dordrecht, pp 347–366 Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Ta- Demming-Adams B, Adams WW III (1996) The role of xantho- kahashi F, Kanegae T, Kadota A, Wada M (2003) CHLO- phyll cycle carotenoids in the protection of photosynthesis. ROPLAST UNUSUAL POSITIONING is essential for proper Trends Plant Sci 1:21–26 chloroplast positioning. 15:2805–2815 Drew EA (1979) Physiological aspects of primary production in Osmond B, Maxwell K, Popp M, Robinson S (1999) On being seagrasses. Aquat Bot 7:139–150 thick: fathoming apparently futile pathways of photosynthesis Gorton HL, Williams WE, Vogelmann TC (1999) Chloroplast and metabolism in succulent CAM plants. In: movement in Alocasia macrorrhiza. Physiol Plant 106:421–428 Bryant JA, Burrell MM, Kruger NJ (eds) Plant carbohydrate Guralnick LJ, Edwards G, Ku MSB, Hockema B, Franceschi VR biochemistry. BIOS, Oxford, pp 183–200 (2002) Photosynthetic and anatomical characteristics in the C4- Park Y-I, Chow WS, Anderson JA (1996) Chloroplast movement crassulacean acid metabolism-cycling plant, Portulaca grandi- in the shade plant albiflora helps protect photo- flora. Funct Plant Biol 29:763–773 system II against light stress. Plant Physiol 111:867–875 Hartung W, Davies WJ (1991) Drought-induced changes in phys- Rock CD (2000) Pathways to abscisic acid-regulated gene expres- iology and ABA. In: Davies WJ, Jones HG (eds) Abscisic acid: sion. New Phytol 148:357–396 physiology and biochemistry. BIOS, Oxford, pp 63–79 Smith JAC, Lu¨ ttge U (1985) Day–night changes in leaf water Haupt W (1999) Chloroplast movement: from phenomenology to relations associated with the rhythm of crassulacean acid molecular biology. Prog Bot 60:1–36 metabolism in Kalanchoe¨ daigremontiana. Planta 163:272–282 Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore Terashima I, Hikosaka K (1995) Comparative ecophysiology of AR (2001) Phototropin-related NPL1 controls chloroplast leaf and canopy photosynthesis. Plant Cell Environ 18:1111– relocation induced by blue light. Nature 410:952–954 1128 Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tlalka M, Fricker M (1999) The role of calcium in blue-light- Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a dependent chloroplast movement in Lemna trisulca L. Plant J phototropin homolog controlling the chloroplast high-light 20:461–473 avoidance response. Science 291:2138–2141 Vaughn KC, Hickok LG, Warne TR, Farrow AC (1990) Structural Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada analysis and inheritance of a clumped-chloroplast mutant in the M (2002) Chloroplast avoidance movement reduces photo- Ceratopteris. J Hered 81:146–151 damage in plants. Nature 420:829–832 Vogelmann TC, Martin G (1993) The functional significance of Khurana JP, Kochhar A, Tyagi AK (1998) Photosensory percep- palisade : penetration of directional versus diffuse light. tion and signal transduction in higher plants: molecular genetic Plant Cell Environ 16:65–72 analysis. Crit Rev Plant Sci 17:465–539 Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Kondo A, Nose A, Ueno O (1998) Leaf inner structure and im- Rev Plant Biol 54:455–468 munogold localization of some key enzymes involved in carbon Weatherwax SC, Ong MS, Degenhardt J, Bray EA, Tobin EM metabolism in CAM plants. J Exp Bot 49:1953–1961 (1996) The interaction of light and abscisic acid in the regula- Kondo A, Nose A, Yuasa H, Ueno O (2000) Species variation in tion of plant . Plant Physiol 111:363–370 the intracellular localization of pyruvate, Pi dikinase in leaves of Weatherwax SC, Williams SA, Tingay S, Tobin EM (1998) The crassulacean-acid-metabolism plants: an immunogold electron- phytochrome response of the Lemna gibba NPR1 gene is microscope study. Planta 210:611–621 mediated primarily through changes in abscisic acid levels. Lin C (2000) Plant blue-light receptors. Trends Plant Sci 5:337–342 Plant Physiol 116:1299–1305 Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of Zurzycki J (1961) The influence of chloroplast displacements on the photosynthesis in nature. Annu Rev Plant Physiol Plant Mol optical properties of leaves. Acta Soc Bot Pol 30:503–527 Biol 45:633–662