Abstract
Main conclusion
Green fruits display a high engagement in CEF and enhanced VAZ cycle activity as a response to the demands imposed by their internal aerial conditions, particularly low O 2 , due to gas exchange limitations.
In the present study, we used HPLC analysis, post-illumination changes in fluorescence yield under varying O2 and CO2 partial pressures and absorbance changes at 820 nm induced by far-red light to assess the carotenoid composition, the functionality of the xanthophyll cycle (VAZ) and the possibility of an active cyclic e − flow (CEF) in the fully exposed green fruits from Nerium oleander and Rosa sp. Equally exposed, mature leaves served as controls. Compared to leaves, fruits display less total chlorophylls and carotenoids but higher Car/Chl ratio, mainly shaped by the increased pools of the VAZ cycle components, in both species. The enhanced VAZ pool size in fruits is combined with a higher mid-day de-epoxidation state (DEPS). Moreover, fruits exhibit considerably lower levels of oxidizable P700, a faster re-reduction of PSI and significantly higher relative magnitude of CEF, irrespective of the O2/CO2 levels applied. We conclude that the higher VAZ investment may serve the enhanced heat dissipation needs in fruits, in the presence of a suppressed linear e − flow. In addition, the elevated potential of CEF may replenish the ATP lost due to hypoxia and concurrently facilitate the development of adequate non-photochemical quenching (NPQ), through its contribution to ΔpH increase. Since other non-foliar green organs exhibit a similar photosynthetic pattern, we argue that this may reflect a common strategy for green tissues under similar micro-environmental conditions, particularly hypoxia.
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References
Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Phys 37:93–136
Aschan G, Pfanz H (2003) Non-foliar photosynthesis—a strategy of additional carbon acquisition. Flora 198:81–97
Aschan G, Pfanz H, Vodnik D, Batič F (2005) Photosynthetic performance of vegetative and reproductive structures of green hellebore (Helleborus viridis L. agg.). Photosynthetica 43:55–64
Blanke MM, Lenz F (1989) Fruit photosynthesis. Plant Cell Environ 12:31–46
Borisjuk L, Rolletschek H (2009) The oxygen status of the developing seed. New Phytol 182:1–14
Borisjuk L, Nguyen TH, Neuberger T, Rutten T, Tschiersch H, Claus B, Feussner I, Webb AG, Jakob P, Weber H, Wobus U, Rolletschek H (2005) Gradients of lipid storage, photosynthesis and plastid differentiation in developing soybean seeds. New Phytol 167:761–776
Bukhov NG, Govindachary S, Rajagopal S, Joly D, Carpentier R (2004) Enhanced rates of P700+ dark-reduction in leaves of Cucumis sativus L. photoinhibited at chilling temperature. Planta 218:852–861
Cheng L, Ma F (2004) Diurnal operation of the xanthophyll cycle and the antioxidant system in apple peel. J Am Soc Hortic Sci 129:313–320
Choudhury N, Behera R (2001) Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents. Photosynthetica 39:481–488
Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci l:21–26
Demmig-Adams B, Winter K, Winkelmann E, Krüger A, Czygan FC (1989) Photosynthetic characteristics and the ratios of chlorophyll, β-carotene and the components of the xanthophyll cycle upon a sudden increase in growth light regime in several plant species. Bot Acta 102:319–325
Demmig-Adams B, Gilmore AM, Adams WW (1996) In vivo functions of carotenoids in higher plants. FASEB 10:403–412
Dima E, Manetas Y, Psaras GK (2006) Chlorophyll distribution pattern in inner stem tissues: Evidence from epifluorescence microscopy and reflectance measurements in 20 woody species. Trees Struct Funct 20:515–521
Esteban R, Olascoaga B, Becerril JM, García-Plazaola JI (2010) Insights into carotenoid dynamics in non-foliar photosynthetic tissues of avocado. Physiol Plant 140:69–78
Ferroni L, Pantaleoni L, Baldisserotto C, Aro EM, Pancaldi S (2013) Low photosynthetic activity is linked to changes in the organization of photosystem II in the fruit of Arum italicum. Plant Physiol Biochem 63:140–150
Filippou M, Fasseas C, Karabourniotis G (2007) Photosynthetic characteristics of olive tree (Olea europaea) bark. Tree Physiol 27:977–984
García-Plazaola JI, Hermandez A, Olano JM, Becerril JM (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Funct Plant Biol 30:319–324
García-Plazaola JI, Matsubara S, Osmond B (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34:759–773
Goffman FD, Ruckle M, Ohlrogge J, Shachar-Hill Y (2004) Carbon dioxide concentrations are very high in developing oilseeds. Plant Physiol Biochem 42:703–708
Hansen U, Fiedler B, Rank B (2002) Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees Struct Funct 16:354–364
Hetherington SE, Smillie RM, Davies WJ (1998) Photosynthetic activities of vegetative and fruiting tissues of tomato. J Exp Bot 49:1173–1181
Ivanov AG, Krol M, Sveshnikov D, Malmberg G, Gardeström P, Hurry V, Öquist G, Huner NPA (2006) Characterization of the photosynthetic apparatus in cortical bark chlorenchyma of Scots pine. Planta 223:1165–1177
Kalachanis D, Manetas Y (2010) Analysis of fast chlorophyll fluorescence rise (O-K-J-I-P) curves in green fruits indicates electron flow limitations at the donor side of PSII and the acceptor sides of both photosystems. Physiol Plant 139:313–323
Kotakis Ch, Petropoulou Y, Stamatakis K, Yiotis Ch, Manetas Y (2006) Evidence for active cyclic electron flow in twig chlorenchyma in the presence of an extremely deficient linear electron transport activity. Planta 225:245–253
Lemos Filho JP, Isaias RMS (2004) Comparative stomatal conductance and chlorophyll a fluorescence in leaves vs. fruits of the cerrado legume tree, Dalbergia miscolobium. Brazilian J Plant Physiol 16:89–93
Levizou E, Manetas Y (2007) Photosynthetic pigment contents in twigs of 24 woody species assessed by in vivo reflectance spectroscopy indicate low chlorophyll levels but high carotenoid/chlorophyll ratios. Environ Exp Bot 59:293–298
Levizou E, Manetas Y (2008) Maximum and effective PSII yields in the cortex of the main stem of young Prunus cerasus trees: effects of seasons and exposure. Trees Struct Funct 22:159–164
Levizou E, Petropoulou Y, Manetas Y (2004) Carotenoid composition of peridermal twigs does not fully conform to a shade acclimation hypothesis. Photosynthetica 42:591–596
Li P, Cheng L (2008) The shaded side of apple fruit becomes more sensitive to photoinhibition with fruit development. Physiol Plantarum 134:282–292
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 603:591–592
Manetas Y (2004) Probing corticular photosynthesis through in vivo chlorophyll fluorescence measurements: evidence that high internal CO2 levels suppress electron flow and increase the risk of photoinhibition. Physiol Plant 120:509–517
Mano J, Miyake C, Schreiber U, Asada K (1995) Photoactivation of the electron flow from NADPH to plastoquinone in spinach chloroplasts. Plant Cell Physiol 36:1589–1598
Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15:3975–3981
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Munné-Bosch S, Shikanai T, Asada K (2005) Enhanced ferredoxin-dependent cyclic electron flow around photosystem I and α-tocopherol quinone accumulation in water-stressed ndhB-inactivated tobacco mutants. Planta 222:502–511
Nilsen ET (1995) Stem photosynthesis: extent, patterns, and role in plant carbon economy. In: Gartner B (ed) Plant stems: physiology and functional morphology. Academic Press, San Diego, pp 223–240
Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460
Pfanz H, Aschan G, Langenfeld-Heyser R, Wittmann C, Loose M (2002) Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. Naturwissenschaften 89:147–162
Piechulla B, Glick RE, Bahl H, Melis A, Gruissem W (1987) Changes in photosynthetic capacity and photosynthetic protein pattern during tomato fruit ripening. Plant Physiol 84:911–917
Pilarski J (1999) Gradient of photosynthetic pigments in the bark and leaves of lilac (Syringa vulgaris L.). Acta Physiol Plant 21:365–373
Ranjan S, Singh R, Soni DK, Pathre UV, Shirke PA (2012) Photosynthetic performance of Jatropha curcas fruits. Plant Physiol Biochem 52:66–76
Rosevear MJ, Young AJ, Johnson GN (2001) Growth conditions are more important than species origin in determining leaf pigment content of British plant species. Funct Ecol 15:474–480
Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23:331–343
Yiotis C, Manetas Y (2010) Sinks for photosynthetic electron flow in green petioles and pedicels of Zantedeschia aethiopica: evidence for innately high photorespiration and cyclic electron flow rates. Planta 232:523–531
Yiotis C, Petropoulou Y, Manetas Y (2009) Evidence for light-independent and steeply decreasing PSII efficiency along twig depth in four tree species. Photosynthetica 47:223–231
Acknowledgments
This research has been co-financed by the European Union (European Social Fund, ESF) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF)—Research Funding Program: Heracleitus II. Investing in knowledge society through the European Social Fund. The authors thank Prof. Y. Manetas for his helpful comments on the manuscript.
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Kyzeridou, A., Stamatakis, K. & Petropoulou, Y. The non-foliar hypoxic photosynthetic syndrome: evidence for enhanced pools and functionality of xanthophyll cycle components and active cyclic electron flow in fruit chlorenchyma. Planta 241, 1051–1059 (2015). https://doi.org/10.1007/s00425-014-2234-8
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DOI: https://doi.org/10.1007/s00425-014-2234-8