FEATURE ESSAY 12.1 Perspectives on photoinhibition

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Figure 1 Professor C.B. Osmond, FAA, FRS

Barry Osmond

 Plants often harvest more light than they can use in photosynthesis. When they are exposed to excess light there is an ever-present possibility of photoinhibition. This may happen when tree fall produces a rainforest gap and suddenly exposes seedlings adapted to life on a forest floor to sustained 10- or 20-fold increases in photon irradiance, or when water stress or low temperature restricts access to CO2 in sun plants. The efficiency of light utilisation declines rapidly, and in most cases reversibly. Usually the excess light is wasted as heat, instead of being used to drive assimilation. These reversible changes in efficiency are known as photoprotection, and, if adequate, photoinhibitory damage is avoided.

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Figure 2 Photoinhibitory printing of excerpts from the front page of Ewart's paper on assimilatory inhibition on a leaf of the shade plant Cissus antarctica. A microfilm negative of the paper was appressed against the leaf which was exposed to full sunlight for 1 h. Chlorophyll fluorescence was subsequently imaged with a special video camera. Those areas of the leaf exposed to strong light show severely reduced fluorescence due to photoinhibition. This latent print remains on the leaf for several weeks because these shade plants repair photoinhibitory damage only slowly

(Photographs courtesy C.B. Osmond)

Some of the earliest systematic studies of photoinhibition were done by A.J. Ewart in Pfeffer’s laboratory in Leipzig and published in 1896 (Figure 2). He examined the effects of excess light on the ability of chloroplasts in leaves to evolve O2. He detected this by examining the movement of O2-requiring bacteria towards photosynthetically active cells in leaf sections. Ewart is best remembered because he went on to translate three volumes of Pfeffer’s famous textbook (The Physiology of Plants) into English, and later became the first Professor of Plant Physiology in Australia (University of Melbourne, 1904).

Modern research on photoinhibition has been strongly influenced by the Dutch biophysicist Bessel Kok (1956), responsible for so many advances in photosynthetic research, and by the early field studies of Björkman and Holmgren (1963) in Sweden. Björkman’s sabbatical in Australia in 1971 stimulated renewed interest in photoinhibition, and with Australian collaborators research in his Stanford laboratory has repeatedly changed the way people think in this field (Powles 1984; Björkman and Demmig-Adams 1994). Australian research in photoinhibition continues to attract attention worldwide (Anderson et al. 1997; Wydrzynski et al. 1995). Although modern research techniques such as in vivo chlorophyll fluorescence are much more quantitative and field portable, the questions being probed are remarkably similar to those studied by Ewart!

By and large, leaves on most plants cannot avoid harvesting light, but some have evolved with features to forestall absorption of excess radiation. For example, leaves of desert plants often reflect a large part of incident light, the high reflectivity being due to hairs, salt crusts (as in Australian saltbushes such as Atriplex nummularia) or epidermal waxes (see Figure 12.5). Such features are effectively mechanisms for external photoprotection. In others such as Townsville stylo (Macroptilium atropurpureum) leaves demonstrate very effective light-avoiding responses when water stressed. Ludlow and Björkman (1984) showed that if leaves of Townsville stylo were restrained perpendicular to incident sunlight, high-temperature-dependent photoinhibition ensued. It was obvious that unrestrained movement in the field preserved green and functional stylo leaves under conditions that accelerated senescence of leaves on adjacent herbs and grasses. By way of contrast, in some species like the compass plant (Lactuca scariola) leaves actually track the sun’s movement to maximise light interception. Sun plants in which the photo-synthetic apparatus is organised to take advantage of bright light have high capacities for CO2 fixation and retain high photosynthetic efficiency at relatively high photon irradiance (see Figure 12.9, and Case study 12.1).

Depending on photosynthetic pathway, and environmental conditions, sun plants may also sustain high rates of non-assimilatory electron transport in carbon recycling during oxygenase photorespiration (Section 2.3) and to O2 in the Mehler reaction. Sun plants are also well endowed with photoprotective mechanisms that facilitate a reversible downregulation of PSII efficiency and stimulate wastage of absorbed photons as heat in the antennae pigment–protein complexes, before transfer to the reaction centre of PSII. These processes, linked to the energetic status of thykaloids and the interconversion of xanthophyll pigments (Section 12.1.2), provide internal photoprotection for PSII reaction centres (Demmig-Adams and Adams 1992; Gilmore 1997).

For the most part, these antennae-based processes seem to accommodate photon excess in most natural environments. However, when photon excess is sustained, especially in combination with other stresses, photoinhibitory damage in PSII reaction centres may follow. The site of damage in most cases seems to be D1 protein which is the psbA gene product and the most rapidly turned over protein in chloroplasts. D1 protein is also the binding site for the triazine family of herbicides and accounts for their lethal effects. Turnover of D1 is accelerated in bright light, and it is often described as the ‘suicide protein’ (Aro et al. 1993). Sun plants have high rates of chloroplast protein synthesis, and are thus able to repair damage to the critical D1 protein of PSII reaction centres more readily than in shade plants (Section 1.2).

Photoinhibitory damage at chilling temperatures seems to involve PSI rather than PSII, and is especially significant among C4 grasses and C3 plants of tropical origin. In these chilling-sensitive plants, a photon irradiance of only 100 µmol quanta m–2 s–1 at 0–10ºC for about 5 h is sufficient to cause a selective photoinhibition of PSI (Sonoike 1996).

Shade plants, in which the photosynthetic apparatus is organised to take advantage of low light, are poorly endowed with all of the above processes. Structural organisation of the photosynthetic apparatus reflects these biophysical and bio-chemical realities, and not surprisingly the very different granal structures of shade and sun plants have important implications for photoinhibitory damage (Anderson and Aro 1994). In the short term, shade plants accommodate bright light in sunflecks without photoinhibitory damage, and even exploit it for additional post-illumination CO2 exchange (Pearcy 1994; Chazdon and Pearcy 1986). When exposed to sustained bright sunlight, in excess of that encountered during growth, shade-tolerant plants such as Alocasia macrorrhiza at the margins of Queensland rainforests suffer photoinhibitory damage. Photoacclimation to bright light, the successful long-term accommodation of photoinhibitory processes, is genetically limited in many species, being dependent on adequate nutrition (especially nitrogen) and permissive temperatures (Anderson and Osmond 1987).

Although unicellular algae such as Chlamydomonas sp. have been widely used to research mechanisms of photoinhibitory damage, relatively little is known of photoinhibition in either marine or freshwater environments. Under natural conditions, vertical movement of unicellular algae in water columns is an important determinant of photon exposure and photoinhibitory responses, which almost certainly involve many of the same processes as in higher plants. Thus the ubiquitous marine macrophyte Ulva is susceptible to desiccation and high-temperature-dependent photoinhibitory damage in rock pools and estuaries when low tides occur at midday. However, the diversity of photosynthetic pigments among marine macrophytic algae suggests several alternative photoinhibitory mechanisms that are yet to be investigated.

Clearly, photoinhibition is an integral and indispensable component of photosynthesis. The inefficiencies it produces in light utilisation are essential to the stability of the photosynthetic apparatus in organisms that depend on light for life, and especially in environments where they can do little to regulate the incoming flux of this basic resource. The costs of these inefficiencies are difficult to estimate (Long et al. 1994) and the extent to which plant distribution in relation to sunlight is governed by photoinhibitory responses remains controversial. Perhaps one of the most convincing examples is the interaction of bright light and low temperature which restricts re-establishment of eucalyptus seedlings to the shaded south side of parent trees on the Southern Highlands of New South Wales (Ball et al. 1991; Case study 14.1).

References

Anderson, J.M. and Aro, E.-M. (1994). ‘Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: an hypothesis’, Photosynthesis Research, 41, 315–326.

Anderson, J.M. and Osmond, C.B. (1987). ‘Shade–sun responses: compromises between acclimation and photoinhibition’, in Photoinhibition, eds D.J. Kyle, C.B. Osmond and C.J. Arntzen, 1–38, Elsevier: Amsterdam.

Anderson, J.M., Park, Y.-I. and Chow, W.S. (1997). ‘Photoinhibition and photoprotection in nature’, Physiologia Plantarum, 100, 214–223.

Aro, E.-M., Virgin, I. and Andersson, B. (1993). ‘Photoinhibition of photosystem II. Inactivation, protein damage and turnover’, Biochimica et Biophysica Acta, 1134, 113–134.

Ball, M.C., Hodges, V.S. and Laughlin, G.P. (1991). ‘Cold-induced photoinhibition limits regeneration of snow gum at treeline’, Functional Ecology, 5, 663–668.

Björkman, O. and Demmig-Adams, B. (1994). ‘Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants’, in Ecophysiology of Photosynthesis, Ecological Studies, Vol. 100, eds E.-D. Schulze and M.M. Caldwell, 17–47, Springer-Verlag: Berlin.

Björkman, O. and Holmgren, P. (1963). ‘Adaptability of the photosynthetic apparatus to light intensity in ecotypes from exposed and shaded habitats’, Physiologia Plantarum, 16, 889–914.

Chazdon, R.L. and Pearcy, R.W. (1986). ‘Photosynthetic responses to light variation in rainforest species. II Carbon gain and photosynthetic efficiency during lightflecks’, Oecologia, 69, 524–531.

Demmig-Adams, B. and Adams III, W.W. (1992). ‘Photoprotection and other responses of plants to high light stress’, Annual Review of Plant Physiology and Plant Molecular Biology, 43, 599–626.

Gilmore, A.M. (1997). ‘Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves’, Physiologia Plantarum, 99, 197–209.

Kok, B. (1956). ‘On the inhibition of photosynthesis by intense light’, Biochimica et Biophysica Acta, 21, 234–244.

Long, S.P., Humphries, S. and Falkowski, P.G. (1994). ‘Photoinhibition of photosynthesis in nature’, Annual Review of Plant Physiology and Plant Molecular Biology, 45,633–662.

Ludlow, M.M. and Björkman, O. (1984). ‘Paraheliotropic leaf movement in Siratro as a protective mechanism against drought-induced damage to primary photosynthetic reactions: damage by excessive light and heat’, Planta, 161, 505–518.

Pearcy, R.W. (1994). ‘Photosynthetic response to sunflecks and light gaps: mechanisms and constraints’, in Photoinhibition of Photosynthesis, eds N.R. Baker and J.R. Bowyer, 255–272, Bios Scientific: Oxford.

Powles, S.B. (1984). ‘Photoinhibition of photosynthesis by visible light’, Annual Review of Plant Physiology, 35, 15–44.

Sonoike, K. (1996). ‘Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants’, Plant Cell Physiology, 37, 239–247.

Wydrzynski, T.J., Chow, W.S. and Badger, M.R. (eds) (1995). ‘Chlorophyll fluorescence: origins, measurements, interpretations and applications’, Australian Journal of Plant Physiology, 22, 123–355.

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