ReviewSignal transduction in response to excess light: getting out of the chloroplast
Introduction
The amount of light energy encountered by plants in excess of that which they need for photosynthetic productivity is termed excess excitation energy (EEE) 1•., 2., 3., 4.. The amount of EEE that plants experience may also be dictated by additional environmental and developmental factors that cause the amount of light energy required for cellular processes to vary. Disease, nutrient and water limitation, and rapid changes in temperature can promote EEE even at light intensities that would not pose a problem under benign conditions.
The possibility of generating EEE is ever-present for land plants, which cannot move away from adverse environmental conditions. Failure to dissipate or avoid accumulating EEE leads to photooxidative damage to the photosynthetic apparatus, which is often manifested as bleaching, chlorosis or bronzing of leaves 1•., 2., 3., 4., 5.. Many mechanisms have evolved that serve to dissipate EEE and act as ‘safety valves’ to ensure that the harvesting of light energy does not inadvertently lead to cellular damage [1•]. Acclimation to a range of adverse environmental conditions might include increasing the number and efficiency of dissipatory mechanisms and developing physiological, biochemical and structural changes that avoid the accumulation of EEE.
Immediate responses to the conditions that promote EEE must initiate signalling pathways that lead to whole-plant acclimation. In this review, we draw on a wider literature to suggest ways in which such signalling pathways might be initiated and function.
Section snippets
Dissipation and avoidance of EEE
Several excellent reviews have been written recently that describe the protective mechanisms of dissipation and avoidance of EEE 1•., 2., 3., 6., 7.. Briefly, dissipation of EEE in plants is achieved by a combination of so-called non-photochemical and photochemical quenching processes.
Non-photochemical quenching processes include the transfer of triplet-state chlorophyll excitation energy to carotenoids that, in turn, dissipate the excess energy as heat during their return to a non-excited
Signal transduction pathways that respond to EEE
An emerging literature clearly indicates that signalling pathways are integrated into a regulatory network, such that many pathways may share common routes or interact with one another 19., 20., 21.. We could predict, therefore, that a major part of an EEE-responsive signalling pathway(s) may well join such a regulatory network in order to effect acclimation at the whole-plant level. The remainder of this review focuses on those features of EEE signalling responses that pose the following
The perception of EEE and the initiation of signal transduction
The photosynthetic apparatus is a prime candidate for the perception of EEE. In principle, any increase in the activity of dissipatory processes could initiate signalling pathways. In response to EEE, increases in electron transport rates and consequent redox changes in photosynthetic electron transport (PET) components would be almost instantaneous. The regulation of both nuclear and chloroplast genes that encode components of photosynthesis and antioxidant metabolism have been associated with
The transmission of signals across the chloroplast envelope
It should be noted that many of the hormones or signalling molecules associated with stress, such as jasmonic acid (JA) and abscisic acid (ABA), are synthesised wholly or in part within the chloroplast 34., 35.. The involvement of EEE in both abiotic and biotic stresses clearly shows that such molecules could, in effect, signal for EEE. For example, in drought-stressed plants, the recently described mediation of ABA-controlled stomatal closure by H2O2 [36••] is a clear indication of the way in
Joining the mainstream
In many of the schemes outlined above, H2O2 or other ROS are the end-products of signalling pathways that emanate directly or indirectly from the chloroplast. There are a number of ways in which one can envisage how such a signal might be propagated further. ROS could directly interact with redox-sensitive transcription factors paralleling OxyR and Sox/RS in E. coli or I-κB:NF-κB in animals 44., 45.. The activation of transcription factors would then lead to change in gene expression.
Conclusions
We have described briefly some of the means whereby EEE can initiate signalling leading to acclimation to changing environmental circumstances. Given the flexibility of plants’ responses to environmental change and the importance of protection against EEE, it would not be surprising to find that all of these possible signalling routes exist, reflecting the simultaneous operation of many different protective mechanisms.
There is a need to understand how wide a range of adverse environmental
Acknowledgements
PM acknowledges the support of the Biotechnology and Biological Sciences Research Council (BBSRC) through the Core Strategic Grant to the John Innes Centre. SK is grateful for the support of grants to Stockholm University from the Swedish Research Council and from the Swedish Council for International Cooperation in Research and Higher Education (STINT). We apologise to colleagues whose publications we did not cite or discuss in depth. This was because of space constraints.
References and recommended reading
Papers of particular interest, published within the annual period of review,have been highlighted as:
• of special interest
•• of outstanding interest
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