Since potentially harmful ultraviolet radiation (UVR, 280–400？nm) and high photosynthetically active radiation (PAR, 400–700？nm) are present in the shallow waters of the Gulf of Aqaba where part of the seagrass Halophila stipulacea's population thrives, we examined the effects of high PAR with and without UVR on its photosynthesis and midday chloroplast “clumping phenomenon” (Sharon and Beer 2008). It was found that midday clumping occurred only under high PAR in the presence of UVR, which resulted in a 44% reduction in the absorption cross section (or absorption factor, AF) of the leaves and, accordingly, a parallel lowering of midday electron transport rates (ETR). In addition, UVR had a direct effect on the photosynthetic apparatus by lowering quantum yields and, thus, ETRs, while pigment relations remained unaltered. We conclude that the potentially harmful effects of UVR and high PAR on the photosynthetic apparatus of Halophila stipulacea are mitigated by their activation of chloroplast clumping, which functions as a means of protecting most chloroplasts from high irradiances, including UVR. 1. Introduction While the mechanisms underlying chloroplast movements in plants have been studied on the intracellular and molecular levels [1, 2] their ecophysiological role(s) is less understood. These movements are in many plants induced by blue light [3–8], but in a few studies it was suggested that also ultraviolet (UV), or “near to UV”, wavelengths could trigger chloroplast movements [9, 10]. Interestingly, Kondo et al. [11] reported that in many cases the chloroplast clumps are formed near or around the nuclei so as to protect them from high irradiances. The only seagrass so far for which chloroplast movements have been described is Halophila stipulacea [12, 13]. In the latter work, it was found that chloroplast clumping occurred during midday only in plants growing under high irradiances (>450？μmol？photons？m？2？s？1), while lower-irradiance grown plants maintained their chloroplasts evenly dispersed during the day. It was then suggested that the chloroplast clumping during midday may have a protective role against high irradiances. In addition to high photosynthetically active radiation (PAR, 400–700？nm), coastal waters, especially clear tropical waters, also feature high levels of ultraviolet radiation (UVR, 280–400？nm) in their upper layers ([14, 15] and this study). Various marine plants respond to such high UVR levels by producing mycosporine-like amino acids (MAA, [16, 17]) and other UV absorbing compounds (i.e., flavones and flavones glycosides in
References
[1]
N. Suetsugu and M. Wada, “Chloroplast photorelocation movement mediated by phototropin family proteins in green plants,” Biological Chemistry, vol. 388, no. 9, pp. 927–935, 2007.
[2]
W. Yamashita, T. Kanegae, and A. Kadota, “Analyses on the actin dynamics during chloroplasts photorelocation movement in the moss Physcomitrella patens by use of tdTomato-talin,” Plant and Cell Physiology, vol. 48, article 55, 2007.
[3]
H. Gabry？, “Blue light-induced orientation movements of chloroplasts in higher plants: recent progress in the study of their mechanisms,” Acta Physiologiae Plantarum, vol. 26, no. 4, pp. 473–478, 2004.
[4]
S. L. DeBlasio, J. L. Mullen, D. R. Luesse, and R. P. Hangarter, “Phytochrome modulation of blue light-induced chloroplast movements in arabidopsis,” Plant Physiology, vol. 133, no. 4, pp. 1471–1479, 2003.
[5]
N. Sakuri, K. Domoto, and S. Takagi, “Blue light-induced reorganization of the actin filaments and the avoidence response of chloroplasts in epidermal cells of Vallisneria gigatea,” Planta, vol. 221, pp. 66–74, 2005.
[6]
D. R. Luesse, S. L. DeBlasio, and R. P. Hangarter, “Plastid movement impaired 2, a new gene involved in normal blue-light-induced chloroplast movements in Arabidopsis,” Plant Physiology, vol. 141, no. 4, pp. 1328–1337, 2006.
[7]
W. Krzeszowiec, B. Rajwa, J. Dobrucki, and H. Gabry？, “Actin cytoskeleton in Arabidopsis thaliana under blue and red light,” Biology of the Cell, vol. 99, no. 5, pp. 251–260, 2007.
[8]
I. Shihira-Ishikawa, T. Nakamura, S. I. Higashi, and M. Watanabe, “Distinct responses of chloroplasts to blue and green laser microbeam irradiations in the centric diatom Pleurosira laevis,” Photochemistry and Photobiology, vol. 83, no. 5, pp. 1101–1109, 2007.
[9]
H. Yatsuhashi, “Photoregulation systems for light-oriented chloroplast movement,” Journal of Plant Research, vol. 109, no. 1094, pp. 139–146, 1996.
[10]
V. Rodrigues, R. Bhandari, J. P. Khurana, and P. K. Sharma, “Movement of chloroplasts in mesophyll cells of Garcinia indica in response to UV-B radiation,” Current Science, vol. 92, no. 11, pp. 1610–1613, 2007.
[11]
A. Kondo, J. Kaikawa, T. Funaguma, and O. Ueno, “Clumping and dispersal of chloroplasts in succulent plants,” Planta, vol. 219, pp. 500–506, 2004.
[12]
E. A. Drew, “Physiological aspects of primary production in seagrasses,” Aquatic Botany, vol. 7, pp. 139–150, 1979.
[13]
Y. Sharon and S. Beer, “Diurnal movements of chloroplasts in Halophila stipulacea and their effect on PAM fluorometric measurements of photosynthetic rates,” Aquatic Botany, vol. 88, no. 4, pp. 273–276, 2008.
[14]
R. P. Dunne and B. E. Brown, “Penetration of solar UVB radiation in shallow tropical waters and its potential biological effects on coral reefs; results from the central Indian Ocean and Andaman Sea,” Marine Ecology Progress Series, vol. 144, no. 1—3, pp. 109–118, 1996.
[15]
S. Agustí and M. Llabrés, “Solar radiation-induced mortality of marine pico-phytoplankton in the oligotrophic ocean,” Photochemistry and Photobiology, vol. 83, no. 4, pp. 793–801, 2007.
[16]
K. Whitehead and M. Vernet, “Influence of mycrosporine-like amino acids (MAAs) on UV absorption by particulate and dissolved organic matter,” Limnology and Oceanography, vol. 45, pp. 1788–1796, 2000.
[17]
K. Gao, Y. Wu, G. Li, H. Wu, V. E. Villafa？e, and E. W. Helbling, “Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword,” Plant Physiology, vol. 144, no. 1, pp. 54–59, 2007.
[18]
M. J. Durako, J. I. Kunzelman, W. J. Kenworthy, and K. K. Hammerstrom, “Depth-related variability in the photobiology of two populations of Halophila johnsonii and Halophila decipiens,” Marine Biology, vol. 142, pp. 1219–1228, 2003.
[19]
J. I. Kunzelman, M. J. Durako, W. J. Kenworthy, A. Stapleton, and J. L. C. Wright, “Irradiance-induced changes in the photobiology of Halophila johnsonii,” Marine Biology, vol. 148, no. 2, pp. 241–250, 2005.
[20]
Y. Meng, A. J. Krzysiak, M. J. Durako, J. I. Kunzelman, and J. L. C. Wright, “Flavones and flavone glycosides from Halophila johnsonii,” Phytochemistry, vol. 69, no. 14, pp. 2603–2608, 2008.
[21]
K. Monro and A. G. B. Poore, “Light quantity and quality induce shade-avoiding plasticity in a marine macroalga,” Journal of Evolutionary Biology, vol. 18, no. 2, pp. 426–435, 2005.
[22]
S. P. Dawson and W. C. Dennison, “Effects of ultraviolet and photosynthetically active radiation on five seagrass species,” Marine Biology, vol. 125, no. 4, pp. 629–638, 1996.
[23]
F. L. Figueroa, C. Jiménez, B. Vi？egla et al., “Effects of solar UV radiation on photosynthesis of the marine angiosperm Posidonia oceanica from southern Spain,” Marine Ecology Progress Series, vol. 230, pp. 59–70, 2002.
[24]
K. S. Beach, H. B. Borgeas, and C. M. Smith, “Ecophysiological implications of the measurement of transmittance and reflectance of tropical macroalgae,” Phycologia, vol. 45, no. 4, pp. 450–457, 2006.
[25]
R. P. Trocine, J. D. Riceand, and G. N. Wells, “Inhibition of seagrass photosynthesis by Ultraviolet-B radiation,” Plant Physiology, vol. 68, pp. 74–81, 1981.
[26]
L. A. Brandt and E. W. Koch, “Periphyton as a UV-B filter on seagrass leaves: a result of different transmittance in the UV-B and PAR ranges,” Aquatic Botany, vol. 76, no. 4, pp. 317–327, 2003.
[27]
Y. Sharon, J. Silva, R. Santos, J. W. Runcie, M. Chernihovsky, and S. Beer, “Photosynthetic responses of Halophila stipulacea to a light gradient. II. Acclimations following transplantation,” Aquatic Biology, vol. 7, no. 1-2, pp. 153–157, 2009.
[28]
J. T. O. Kirk, Light and Photosynthesis in Aquatic Systems, Cambridge University Press, Cambridge, UK, 1994.
[29]
R. Moran, “Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide,” Plant Physiology, vol. 69, pp. 1376–1381, 1982.
[30]
C. C. Gradinaru, I. H. M. van Stokkum, A. A. Pascal, R. Van Grondelle, and H. van Amerongen, “Identifying the pathways of energy transfer between carotenoids and chlorophylls in LHCII and CP29. A multicolor, femtosecond pump-probe study,” Journal of Physical Chemistry B, vol. 104, no. 39, pp. 9330–9342, 2000.
[31]
J. W. Runcie, D. Paulo, R. Santos, Y. Sharon, S. Beer, and J. Silva, “Photosynthetic responses of Halophila stipulacea to a light gradient. I. In situ energy partitioning of non-photochemical quenching,” Aquatic Biology, vol. 7, no. 1-2, pp. 143–152, 2009.
[32]
G. Winters, Y. Loya, R. R？ttgers, and S. Beer, “Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ,” Limnology and Oceanography, vol. 48, no. 4, pp. 1388–1393, 2003.
[33]
A. E. Kahn and M. J. Durako, “Photophysiological responses of Halophila johnsonii to experimental hyposaline and hyper-CDOM conditions,” Journal of Experimental Marine Biology and Ecology, vol. 367, pp. 230–235, 2008.
[34]
W. C. Dunlap and J. M. Shick, “Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective,” Journal of Phycology, vol. 34, no. 3, pp. 418–430, 1998.
[35]
U. Karsten, T. Sawall, D. Hanelt et al., “An inventory of UV-absorbing mycosporine-like amino acids in macroalgae from polar to warm-temperate regions,” Botanica Marina, vol. 41, no. 5, pp. 443–453, 1998.
[36]
B. Demmig-Adams and W. W. Adams, “Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation,” New Phytologist, vol. 172, no. 1, pp. 11–21, 2006.
[37]
M. Kimura, Y. Y. Yamamoto, M. Seki et al., “Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray,” Photochemistry and Photobiology, vol. 77, no. 2, pp. 226–233, 2003.
[38]
R. P. Sinha, M. Klisch, A. Groniger, and D. P. Hader, “Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae,” Journal of Photochemistry and Photobiology B, vol. 47, no. 2-3, pp. 83–94, 1998.
