Abstract
It is well known that chloroplasts move in response to changes in blue light intensity in order to optimize light interception, however, little is known about interspecific variation and the relative importance of this mechanism for the high light stress tolerance of plants. We characterized chloroplast movement behavior as changes in light transmission through a leaf in a variety of species ranging from ferns to monocots and eudicots and found a wide spectrum of responses. Most species exhibited a distinct accumulation response compared to the dark positioning, and all species showed a distinct avoidance response. The speed with which transmission values changed during the avoidance response was consistently faster than that during the accumulation response and speeds varied greatly between species. Plants thriving in higher growth light intensities showed greater degrees of accumulation responses and faster changes in transmission than those that prefer lower light intensities. In some species, the chloroplasts on both the adaxial and abaxial leaf surfaces changed their positioning in response to light, while in other species only the chloroplasts on one leaf side responded. No correlation was found between high light stress tolerance and the speed or degree of transmission changes, indicating that plants can compensate for slow and limited transmission changes using other photoprotective mechanisms.
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References
Alonso JM, Stepanova AN, Leisse TJ, Kim CJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657
Augustynowicz J, Gabryś H (1999) Chloroplast movement in fern leaves: correlation of movement dynamics and environmental flexibility of the species. Plant Cell Environ 22:1239–1248
Berg R, Königer M, Schjeide B-M, Dikmak G, Kohler S, Harris GC (2006) A simple low-cost microcontroller-based photometric instrument for monitoring chloroplast movement. Photosynth Res 87:303–311
DeBlasio SL, Luesse DL, Hangarter RP (2005) A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol 139:101–114
Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39(5):474–482
Gorton HL, Williams WE, Vogelmann TC (1999) Chloroplast movement in Alocasia macrorrhiza. Physiol Plant 106:421–428
Grabalska M, Malec P (2004) Blue light induced chloroplast reorientations in Lemna trisulca L. (duckweed) are controlled by two separable cellular mechanisms as suggested by different sensitivity to wortmannin. Photochem Photobiol 79:343–348
Jarillo JA, Gabryś H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954
Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakano A, Wada M (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106(31):13106–13111
Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141
Kagawa T, Wada M (2004) Velocity of chloroplast avoidance movement is fluence rate dependent. Photochem Photobiol Sci 3:592–595
Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832
Kodama Y, Suetsugu N, Kong S-G, Wada M (2010) Two interacting coiled-coil proteins, WEB1 and PMI2, maintain the chloroplast photorelocation movement velocity in Arabidopsis. Proc Natl Acad Sci USA 107(45):19591–19596
Königer M, Delamaide JA, Marlow ED, Harris GC (2008) Arabidopsis thaliana leaves with altered chloroplast numbers and chloroplast movement exhibit impaired adjustments to both low and high light. J Exp Bot 59:2285–2297
Königer M, Harris GC, Pearcy RW (1998) Interaction between photon flux density and elevated temperatures on photoinhibition in Alocasia macrorrhiza. Planta 205:214–222
Königer M, Harris GC, Virgo A, Winter K (1995) Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest species: a comparative field study on canopy, gap and understory plants. Oecologia 104:280–290
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260
Luesse DR, DeBlasio SL, Hangarter RP (2006) Plastid movement impaired 2, a new gene involved in normal blue-light-induced chloroplast movements in Arabidopsis. Plant Physiol 141:1328–1337
Luesse DR, DeBlasio SL, Hangarter RP (2010) Integration of Phot1, Phot2, and PhyB signalling in light-induced chloroplast movements. J Exp Bot 61(15):4387–4397
Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815
Oikawa K, Yamasato A, Kong S-G, Kasahara M, Nakai M, Takahashi F, Ogura Y, Kagawa T, Wada M (2008) Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement. Plant Physiol 148:829–842
Park Y-I, Chow WS, Anderson JM (1996) Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem II against light stress. Plant Physiol 111:867–875
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969–6974
Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQP, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107(19):8860–8865
Trojan A, Gabryś H (1996) Chloroplast distribution in Arabidopsis thaliana (L.) depends on light conditions during growth. Plant Physiol 111:419–425
Tsuboi H, Wada M (2010) Speed of signal transfer in the chloroplast accumulation response. J Plant Res 123(3):381–390
Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468
Walczak T, Gabryś H (1980) New type of photometer for measurements of transmission changes corresponding to chloroplast movements in leaves. Photosynthetica 14:65–72
Wen F, Xing D, Zhang L (2008) Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in Arabidopsis. J Exp Biol 59(10):2891–2901
Williams WE, Gorton HL, Witiak SM (2003) Chloroplast movements in the field. Plant Cell Environ 26:2005–2014
Yamada M, Kawasaki M, Sugiyama T, Miyake H, Taniguchi M (2009) Differential positioning of C4 mesophyll and bundle sheath chloroplasts: aggregative movement of C4 mesophyll chloroplasts in response to environmental stresses. Plant Cell Physiol 50(10):1736–1749
Zurzycki J (1955) Chloroplast arrangement as a factor in photosynthesis. Acta Soc Bot Pol 24:27–63
Zurzycki J (1980) Blue light-induced intracellular movements. In: Senger H (ed) Blue light syndrome. Springer, New York, pp 50–68
Acknowledgments
We would like to thank Prof. Schleiff and the reviewers for helpful comments on the paper. Financial support was provided by a Howard Hughes Medical Institute Grant and the Georgeanne Miller Mulhern Fund.
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Königer, M., Bollinger, N. Chloroplast movement behavior varies widely among species and does not correlate with high light stress tolerance. Planta 236, 411–426 (2012). https://doi.org/10.1007/s00425-012-1619-9
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DOI: https://doi.org/10.1007/s00425-012-1619-9