JXB Advance Access originally published online on July 16, 2004
Journal of Experimental Botany 2004 55(403):1607-1621; doi:10.1093/jxb/erh196
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REVIEW ARTICLE |
Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities
1Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK
2Department of Horticulture, Danish Institute of Agricultural Sciences, Kristinebjergvej 10, PO Box 102, DK-5792 Aarslev, Denmark
* To whom correspondence should be addressed. Fax: +44 (0)1206 873319. E-mail: baken{at}essex.ac.uk
Received 20 February 2004; Accepted 10 May 2004
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Abstract |
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 Top Abstract IntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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Chlorophyll fluorescence has been routinely used for many years to monitor the photosynthetic performance of plants non-invasively. The relationships between chlorophyll fluorescence parameters and leaf photosynthetic performance are reviewed in the context of applications of fluorescence measurements to screening programmes which seek to identify improved plant performance. The potential role of chlorophyll fluorescence imaging in increasing both the sensitivity and throughput of plant screening programmes is examined. Finally, consideration is given to possible specific applications of chlorophyll fluorescence for screening of plants for tolerance to environmental stresses and for improvements in glasshouse production and post-harvest handling of crops.
Key words: Agricultural production, environmental stress, herbicides, horticultural production, imaging, photosynthesis, photosynthetic induction, post-harvest physiology, screening
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Introduction |
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TopAbstractIntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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The problems associated with improving crop production encountered throughout the world are extremely diverse, for example, potentially ranging from millet production in arid regions to tropical flower production in glasshouses. However, common goals are, frequently, the improvement of crop production by the selection of improved varieties and cultivars to tolerate environmental stresses and by the determination of optimal fertilization and irrigation regimes during crop growth. In glasshouse industries optimization of day-length, light intensity, temperature, and CO2 concentration are often additional concerns. A further complication for many crop production systems is the necessity to keep produce alive and fresh during the post-harvest period until it reaches the consumer. Post-harvest conditions can impose many stresses that crops have not experienced in the field or glasshouse prior to harvesting, and which the crops are unable to tolerate effectively by the operation of acclimatory responses.
An important feature of crop development and improvement programmes is the effective evaluation of crop growth and performance, ideally using rapid, non-invasive techniques. Major developments in the instrumentation for measuring chlorophyll fluorescence from intact plants and improvements in the understanding of how changes in plant fluorescence characteristics relate to physiological performance have led to a widespread use of chlorophyll measurements in plant physiological studies. Potentially, the technique has many applications in crop production and development programmes, but as yet it has not been widely applied.
It has been known for a considerable time that changes in chlorophyll fluorescence emission from photosynthetic organisms are frequently indications of changes in photosynthetic activity (McAlister and Myers, 1940
; Kautsky and Zedlitch, 1941). More recently, the demonstrations that chlorophyll fluorescence measurements could be used to estimate, rapidly and non-invasively, the operating quantum efficiency of electron transport through PSII in leaves (Genty et al., 1989) and that this PSII operating efficiency was related to CO2 assimilation (Genty et al., 1989, 1990; Harbinson et al., 1990; Krall and Edwards, 1990, 1991; Krall et al., 1991; Cornic and Ghashghaie, 1991; Siebke et al., 1997) have led to the current widespread use of chlorophyll fluorescence for examining photosynthetic performance in leaves in laboratory, controlled environment, and field situations. There is no doubt that measurements of chlorophyll fluorescence, when applied with appropriate care, can provide useful information about leaf photosynthetic performance. An examination of the literature overwhelmingly reveals in excess of 3500 papers on chlorophyll fluorescence, of which c. 20% are relevant to eco-physiological performance and a similar proportion can be considered to have implications for agricultural or horticultural issues. However, there are many examples in this literature of inappropriate use and misinterpretation of fluorescence measurements that have frequently led to extravagant and unsubstantiated claims of the potential of fluorescence for evaluating plant performance in a wide range of applications. Consequently, there has been an understandable reluctance by the agricultural, horticultural, and agrochemical industries to include fluorescence techniques in crop improvement programmes.
In this review, the objective is to identify ways in which chlorophyll fluorescence may be used effectively to improve plant selection processes and rapidly evaluate plant performance in agricultural and horticultural crop improvement programmes. It is not the intention to provide a comprehensive review of chlorophyll fluorescence theory and applications, since this has been the subject of other recent reviews (Papageorgiou and Govindjee, 2004).
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Fluorescence parameters |
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TopAbstractIntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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There have been very many fluorescence parameters defined in the literature. It is not possible, nor appropriate, to give an extensive review of all of these here. The aim is to provide information on the parameters that can be usefully used in crop improvement programmes to identify differences in plant performance non-destructively and rapidly. Consequently, the focus will be on the fluorescence parameters associated with the induction of fluorescence on exposure of dark-adapted leaves to light and the operation of photosynthesis under growth and other light conditions.
Unfortunately, the literature on analyses of fluorescence induction transients and the processes that quench fluorescence is often extremely confusing because of the diverse, and frequently duplicated, nomenclature that has been used. The majority of the terms in historical and currently used nomenclature have been summarized by Rosenqvist and van Kooten (2003). Although many attempts have been made to establish a single nomenclature (van Kooten and Snell, 1990; Maxwell and Johnson, 2000; Baker et al., 2001), there are still many examples in recent publications of different terms being used to define the same fluorescence level or parameter. In this review the nomenclature suggested by Baker et al. (2001) and Barbagallo et al. (2003) will be used for consistency.
Fluorescence induction
During the induction of photosynthesis when a dark-adapted leaf is exposed to light, large changes in chlorophyll fluorescence occur (Fig. 1). The rapid changes in fluorescence that occur during the rapid induction to a peak have long been attractive for detecting differences in photosynthetic performance between plants. On immediate exposure to light, fluorescence rises to the minimal level of fluorescence, termed Fo level, which is the fluorescence level obtained when the PSII reaction centres are in the ‘open’ state (capable of photochemistry since QA, the primary quinone acceptor of PSII, is maximally oxidized). The fluorescence then rises rapidly to the transient inflection level, Fi, before reaching a peak level, Fp (Fig. 1). It should be noted that if the actinic PPFD being used to drive the fluorescence induction is saturating and effects maximal closure of PSII reaction centres (maximal reduction of QA) at Fp, then the maximal fluorescence level, defined as Fm will be attained. The difference between Fm and Fo is termed the variable fluorescence, Fv. The rapid rise to Fi reflects an increase in the rate of charge stabilization at PSII (as the primary quinone acceptor, QA, is reduced) that is independent of subsequent changes in the redox state of the plastoquinone pool. Changes in the fluorescence level between Fi and Fp are almost entirely due to increased reduction of the plastoquinone pool, which is largely determined by the relative rates of PSII photochemistry and oxidation of plastoquinol by electron transfer to PSI.
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It is not surprising to find that perturbations of photosynthetic metabolism, which can be induced by many biotic and abiotic factors, will modify significantly fluorescence emission kinetic characteristics of plants. However, there is also evidence that many inhibitors of metabolic processes that are not directly involved in photosynthetic metabolism can produce modifications to fluorescence induction kinetics (Blowers, 1989
; Percival and Baker, 1991; Crudace, 2000; Barbagallo et al., 2003). It is possible to quantitate the changes in fluorescence induction characteristics resulting from such perturbations by using ratios of fluorescence levels during induction (Habash et al., 1985). Absolute fluorescence values, such as Fo, Fi, Fm, and Fp, are dependent upon both the photochemical activities and the optical properties of the leaf and, consequently, it is essential to remove the variable of leaf optical properties when attempting to compare changes in fluorescence characteristics between different leaf samples. This can be achieved by comparing ratios of fluorescence values. The potential of the use of ratios of the fluorescence induction parameters Fo, Fi, Fm, Fv, and Fp to detect metabolic perturbations has been demonstrated by examining the effects of a number of herbicides that are known not to impact directly on photosynthetic metabolism (Barbagallo et al., 2003). Arabidopsis seedlings were treated with the recommended field application rate for Asulam, Bifenox, 2,4-D, Diclofop-methyl, Glyphosate, and Imazapyr and the fluorescence parameters 
and 
were monitored with time. After 6 h, significant decreases in all of the parameters were detected for plants treated with Asulam, Diclofop-methyl, Glyphosate, and Imazapyr, whereas the changes induced by Bifenox and 2,4-D were not significant. After 48 h, significant decreases in and were observed with all of the herbicides. Experiments with other species (Alopecurus myosuroides, Avena fatua, Phaseolus vulgaris, Sinapis alba, Triticum aestivum, and Zea mays) have demonstrated the wide applicability of these fluorescence parameters for the detection of herbicide-induced perturbations of metabolism (Habash et al., 1985; Blowers, 1989; Crudace, 2000). Clearly, these fluorescence parameters can be used successfully to detect a number of very different metabolic perturbations in leaves of many species. Although the mechanistic bases for the effects of non-photosynthetic inhibitors on fluorescence emission have not been unequivocally identified, it is likely that inhibition of metabolic reactions not involved directly in photosynthesis will modify the pool sizes of a range of metabolic intermediates, which could influence the rate of synthesis of key intermediates in photosynthetic metabolism and, consequently, interfere with the rate of photosynthesis and fluorescence emission characteristics. Similarly, environmental stress factors would be expected to impact indirectly on fluorescence induction characteristics by perturbing metabolic pools associated with photosynthetic metabolism.
After reaching the peak, a decline in fluorescence occurs, often termed quenching, until a steady-state is reached (Fig. 2). The quenching of Fp to the steady-state level is associated with changes in the photosynthetic apparatus that are associated with the induction of CO2 assimilation. Although many factors can induce modifications in the kinetics of quenching from Fp, the transients observed can be extremely variable. Consequently, analyses of such transients have not proved as useful as other fluorescence parameters for the rapid and sensitive detection of differences between plants. However, differences in the rate of fluorescence quenching from Fp have been used successfully to identify differences between cultivars' responses to environmental stresses (Flagella et al., 1996; Havaux and Lannoye, 1985).
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1 s duration, >6000 µmol photons m–2 s–1) that gives Fm in darkness and 
). The actinic light can be produced from a range of sources, for example, sunlight, halogen lamp, light-emitting diodes. The initial peak of fluorescence is denoted as Fp (without prime, since it originates from the nomenclature of the rapid phase of fluorescence induction, see 
from the dark-adapted leaf and 
All parameters, except Modulated fluorescence measurements
The majority of fluorescence measurements are now made using modulated fluorometers with the leaf poised in a known state. The procedures for making such measurements are shown in Fig. 2, together with the fluorescence levels for a leaf in specific states. For a dark-adapted leaf, Fo is determined using a very low PPFD (generally considerably below 1 µmol m–2 s–1), which ensures that almost all of the PSII reaction centres are in the open state (capable of photochemistry). When the dark-adapted leaf is exposed to a short actinic light pulse of very high PPFD (generally less than 1 s at several thousand µmol m–2 s–1), a maximal level of fluorescence (Fm) is generated as the majority of the PSII reaction centres have been closed (incapable of photochemistry). The ratio of
provides an estimate of the maximum quantum efficiency of PSII photochemistry (Butler, 1978). has been widely used to detect stress-induced perturbations in the photosynthetic apparatus, since decreases in can be due to the development of slowly relaxing quenching processes and photodamage to PSII reaction centres, both of which reduce the maximum quantum efficiency of PSII photochemistry.
The potential for the application of fluorescence measurements to study changes in leaf photosynthetic performance increased dramatically with the development of the light addition technique which could resolve fluorescence quenching into photochemical and non-photochemical components (Bradbury and Baker, 1981, 1984). When a leaf in the light-adapted state is exposed to a saturating pulse of very high PPFD, there is an increase in fluorescence from the F' level to a maximal level, 
(Fig. 2). The difference between and F' is termed 
since this is the fluorescence that has been quenched from the maximal level. The saturating light pulse maximally closes the PSII reaction centres and consequently removes any photochemical quenching by open PSII reaction centres. For a healthy leaf operating at steady-state photosynthesis under moderate to high PPFDs, the level generated by the saturating light pulse will be considerably less than the Fm level generated from a dark-adapted leaf by the same pulse (Fig. 2). This difference is due to the development of light-induced, non-photochemical quenching processes during the induction of photosynthesis in the leaf. The demonstration that the ratio 
was an estimate of the quantum yield of PSII photochemistry for a leaf at any given light condition (Genty et al., 1989) has led to this parameter being widely used to estimate the operating quantum efficiency of PSII electron transport (hereafter termed the PSII operating efficiency). From a physiological screening standpoint, this is a particularly useful parameter, since it is directly related to the rate at which CO2 is assimilated by the leaf (Genty et al., 1989, 1990; Harbinson et al., 1990; Krall and Edwards, 1990, 1991; Krall et al., 1991; Cornic and Ghashghaie, 1991; Edwards and Baker, 1993; Siebke et al., 1997). Consequently, measurements of have become widely used to examine perturbations of photosynthetic performance.
The PSII operating efficiency has been shown to be the product of two other important fluorescence parameters, 
(the maximum efficiency of PSII under the given light conditions, generally determined by the level of quenching in PSII reaction centres and antenna) and 
(the PSII efficiency factor which relates to the ability to maintain PSII reaction centres in the open state):
 | (1) |
is the variable fluorescence of a light-adapted leaf defined as (
) (Fig. 2). 
is the minimal level of fluorescence when PSII centres are maximally open for the leaf in a light-adapted state. has frequently been measured by exposing the leaf at F' to weak far-red light in the absence of actinic light (van Kooten and Snel, 1990; Maxwell and Johnson, 2000), since it is assumed that far red light will preferentially excite PSI relative to PSII thus removing electrons from the PSII electron acceptors and opening the PSII reaction centres. Unfortunately, during the far red light treatment there will almost certainly be relaxation of some non-photochemical quenching as well as an opening of the PSII reaction centres (Oxborough and Baker, 1997). Alternatively, can be calculated from measured values of Fo, Fm, 
and Fv using the following equation (Oxborough and Baker, 1997):
 | (2) |
has been shown to be valid, and it is potentially more accurate than using far red light to generate an level (Oxborough and Baker, 1997).
Non-photochemical quenching (heat dissipation) has been quantified using NPQ which compares the light-induced level to the dark-adapted Fm level (Bilger and Björkman, 1990):
 | (3) |
would be a good indication of this.
A list of the major fluorescence parameters referred to in this review is given in Table 1, together with a summary of what the parameters are measuring. A more comprehensive consideration of these parameters is given in Baker and Oxborough (2004).
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Fluorescence imaging
An important recent development in fluorescence measurements in the context of plant performance and selection is the imaging of fluorescence signals using charge coupled device (CCD) cameras (Oxborough, 2004
). The advantage that fluorescence imaging instruments have over conventional fluorometers is that images of fluorescence parameters can be obtained from whole leaves or large numbers of plants. Imaging of leaves has revealed that photosynthetic performance across leaves can be extremely heterogeneous (Genty and Meyer, 1995; Siebke and Weis, 1995a, b; Bro et al., 1996; Eckstein et al., 1996; Scholes and Rolfe, 1996; Oxborough and Baker, 1997; Leipner et al., 2001; Meng et al., 2001). The power of fluorescence imaging in resolving heterogeneity in photosynthetic function across a leaf can be readily demonstrated by images of PSII operating efficiency from a leaf that has been fed through the petiole with diuron (DCMU), a potent inhibitor of PSII electron transport (Fig. 3; Oxborough, 2004). Prior to uptake into the leaf lamina of the diuron there was little heterogeneity of the PSII operating efficiency across the leaf (Fig. 3A). However, 2 h after feeding with diuron, the PSII operating efficiency in cells close to the vascular tissues, where the herbicide will be initially delivered to the leaf lamina, had decreased to almost zero (Fig. 3B).
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Rapid screening of seedling performance |
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TopAbstractIntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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Frequently, a limitation to crop improvement programmes is the lack of rapid screening techniques to identify plants with improved or impaired metabolism and growth. This need within the agrochemical industry, where combinatorial chemistry is now used to generate large numbers of new chemicals, has resulted in the development of new microscreening or high throughput screening which can involve growing plants in 96-well microtitre plates and employing rapid assessment procedures (Berg et al., 1999
; Evans, 1999). Conventional glasshouse screening using visual assessment of plants over a period of weeks cannot be used for effective screening of such large numbers of plants. Chlorophyll fluorescence measurements offer great potential for rapidly screening large numbers of small plants. However, a major drawback in the past has been the small sampling area of commercially available fluorometers, since measurements could only be made on individual leaves and, consequently, screening large numbers of plants was extremely time-consuming. Recently, the development of chlorophyll fluorescence imaging systems that can image fluorescence parameters from areas in excess of 100 cm2 has allowed the application of the technique for the screening of many plants simultaneously (Fig. 4; Barbagallo et al., 2003; Oxborough, 2004).
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The efficacy of fluorescence imaging for rapidly identifying metabolic perturbations in large numbers of plants has been demonstrated recently by treatment of Arabidopsis and Agrostis tenuis seedlings with Imazapyr (Barbagallo et al., 2003
). This herbicide inhibits acetolactase synthase and, consequently, inhibits the synthesis of branched chain amino acids (Shaner et al., 1985; Singh et al., 1989). This would not be expected to have any direct effect on photosynthetic electron transport. However, 24 h after spraying with Imazapyr, at a concentration similar to that used for field applications, marked changes in fluorescence induction characteristics were detected with no apparent visual effects on plant growth and development (Barbagallo et al., 2003). Images of the fluorescence parameter for seedlings growing in a 96 well plate showed that a range of Imazapyr treatments had produced a marked decrease in this parameter after 24 h (Fig. 5), with the magnitude of the decreases being related to the concentration of herbicide applied (Barbagallo et al., 2003).
Besides detecting perturbations to metabolism and physiological performance, fluorescence imaging can be used for rapidly estimating leaf area in seedlings that have planophile leaves which do not significantly overlap, such as Arabidopsis. The number of pixels in which chlorophyll fluorescence emission is detected is directly related to the distribution of chlorophyll across the leaf, irrespective of pixel value. Consequently, provided chlorophyll is distributed across the whole of the leaf, as is the case in the majority of plants, the leaf area can be estimated from the area of chlorophyll fluorescence emission (Barbagallo et al., 2003). However, for non-planophile leaf growth, as shown by many monocotyledonous plants like A. tenuis, this may not always be the case and careful examination of the relationship between fluorescent leaf area and growth should be made for the system before routinely using fluorescent area to screen for growth differences.
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Fluorescence, leaf photosynthetic physiology and environmental stresses |
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TopAbstractIntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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The relationship between the PSII operating efficiency, estimated by
and CO2 assimilation in leaves allows fluorescence to be used to detect differences in the response of plants to environmental challenges and, consequently, to screen for tolerance to environmental stresses. The rate of leaf CO2 assimilation is sensitive to a wide range of environmental perturbations (e.g. atmospheric pollutants, high and low temperatures, high light, nutrient deficiency, UV-B irradiation, water deficits), although the sites of limitation of CO2 assimilation during these various stresses can be quite different (Baker, 1996). estimates directly the efficiency of light use for electron transport by PSII. A major factor determining this efficiency is the ability of the leaf to remove electrons from the quinone acceptors of PSII (the PSII efficiency factor given by ), which is directly related to the rate at which the products of photosynthetic electron transport (NADPH and ATP) are consumed. The importance of this sink limitation in determining electron transport rate is nicely demonstrated during the induction of CO2 assimilation in a maize leaf (Fig. 6). Images of 
and show that the changes in are similar to the changes in 
but not 
Consequently, changes in PSII efficiency are being determined by the ability to transfer electrons away from PSII and not by non-photochemical quenching in the PSII antennae.
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Decreases in the rate of consumption of NADPH and ATP can result from decreases in carboxylation efficiency, the rate of regeneration of ribulose 1,5-bisphosphate, the supply of CO2 via the stomata to the sites of carboxylation, or the transport of carbohydrates out of the cells (Fig. 7). Such restrictions on PSII electron transport can result in an increase in the proton electrochemical potential difference across the thylakoid membrane, resulting in an increase in non-photochemical quenching in the PSII antennae, which will be detected by a decrease in
and serve to reduce the rate of excitation of the PSII reaction centres and prevent the PSII quinone acceptors becoming highly reduced. With increasing levels of stress, the increases in non-photochemical quenching can be insufficient to maintain the PSII electron acceptors partially oxidized and then photodamage to PSII will occur unless alternative electron acceptors, such as oxygen, are used (Ort and Baker, 2002). Consequently, the ability to maintain the PSII quinone acceptors partially oxidized is a key factor in tolerating environmental stresses (Rosenqvist, 2001; Ort and Baker, 2002) and this can be screened for by monitoring 
Oxygen can act as an electron acceptor by accepting electrons from PSI to produce superoxide, which is rapidly dismutated to hydrogen peroxide, and which, in turn, is converted to water by an ascorbate peroxidase. This process is often termed the Mehler-peroxidase reaction or the water–water cycle (Fig. 7; Ort and Baker, 2002). Oxygen can also be reduced in the processes of photorespiration (Fig. 7; Ort and Baker, 2002).
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It will next be reviewed how fluorescence studies have been applied to investigate the effects of major abiotic stresses on photosynthesis during crop production and to identify cultivars that are tolerant to such stresses. The review is not intended to be exhaustive, but to identify some useful approaches that could be used as the bases for future programmes seeking to improve the stress tolerance of crops.
Drought
In many regions of the world anthropogenic climate change is resulting in extended periods of high temperatures and reduced water supply for crops (Houghton et al., 2001; McCarthy et al., 2001). Often coupled to problems of groundwater pollution (Postel, 2000), this decrease in water availability is increasing the potential for drought in many crop production systems.
Decreases in the relative water content (RWC) of leaves initially induce stomatal closure, imposing a decrease in the supply of CO2 to the mesophyll cells and, consequently, resulting in a decrease in the rate of leaf photosynthesis (Fig. 7; Williams et al., 1999; Lawlor and Cornic, 2002). Such stomatal effects on photosynthesis will not impact on the efficiency of the primary photochemical events of PSII or modify the associated fluorescence induction parameters, such as as has been demonstrated in apple (Massacci and Jones, 1990), cashew (Blaikie and Chacko, 1998), coffee (Lima et al., 2002), lavender and rosemary (Nogués and Alegre, 2002), papapya (Marler and Mickelbart, 1998), potato (Jeffries, 1994), tepary and common bean (Castonguay and Markhart III, 1991), and willow (Ögren, 1990). The stomatal limitations imposed on photosynthesis will be accompanied by a decrease in the rate of consumption of ATP and NADPH for CO2 assimilation (Fig. 7), which could result in decreases in the rate of linear electron transport and, consequently, in 
However, operation of the water–water cycle and, in C3 plants, an increase in photorespiration under the stress conditions may maintain rates of electron transport similar to those observed in non-stressed leaves despite the rate CO2 assimilation decreasing (Leegood and Edwards, 1996; Flexas et al., 1998, 2002; Noctor et al., 2002; Ort and Baker, 2002). This would result in little or no change in Such buffering effects of electron sinks other than CO2 assimilation have been identified in field-grown grapevine during a slowly imposed drought, where a 75% decrease in stomatal conductance resulted in a 54% decrease in CO2 assimilation, but only a 19% decrease in the estimated electron transport rate (Flexas et al., 2002).
Although mild drought stress does not affect the maximum efficiency of PSII primary photochemistry, decreases in intracellular CO2 concentration resulting from stomatal closure can modify the kinetics of photosynthetic induction (Ögren and Öquist, 1985; Ögren, 1990). In willow, the largest differences in the fluorescence induction kinetics between leaves of mild drought-stressed and well-watered plants were observed at low light (180 µmol m–2 s–1) and high (5%) atmospheric CO2 (Ögren, 1990). The parameter found to give the greatest difference between the mild drought-stressed and control leaves under these induction conditions was F' (normalized on Fp) after 25 s. The relative rate of fluorescence quenching in the later stages of the induction of photosynthesis in dessicated leaves has been used successfully to distinguish between drought-resistant and sensitive cultivars of wheat (Havaux and Lannoye, 1985).
With increasing water loss, inhibition of photosynthetic metabolism can occur and can result in a decline in photosynthetic potential which, when sufficiently large to overcome stomatal limitation, will result in a further decrease in CO2 assimilation rate (Lawlor and Cornic, 2002). When drought stress is severe, decreases in the rate of utilization of ATP and NADPH in photosynthetic metabolism will not be compensated for by increases in water–water cycling and photorespiration, or other electron sinks, and, consequently, decreases in will occur (Fracheboud and Leipner, 2003). Although such decreases in are often considerably less than the decreases in CO2 assimilation (Bota et al., 2001; Flexas et al., 2002; Maroco et al., 2002), monitoring of should prove useful for rapid screening of tolerance to severe water stress. In severely droughted grapevine leaves, which had a water potential of –4.5 MPa and negligible CO2 assimilation, significant rates of electron transport were still observed, although these were considerably less then in well-watered leaves (Bota et al., 2001).
Salinity
Salinization of soils is becoming an increasing problem in production systems where high rates of fertilization and irrigation are employed in climates with high evapotranspiration. The initial effects of increasing soil salinity are very similar to those observed when plants are exposed to drought. Reductions in leaf water potential will reduce stomatal conductance and eventually inhibit photosynthetic metabolism, which will result in changes in as discussed in the previous section. Salinity appears not to affect PSII primary photochemistry initially, as demonstrated by the lack of change in when maize was grown in high concentrations of NaCl (Shabala et al., 1998). As with drought, fluorescence induction characteristics are modified by salinity, and have the potential to be used for screening for salt-tolerant varieties (Smillie and Nott, 1982).
Freezing
At freezing temperatures, leaf metabolism is severely inhibited and the potential for slowly recovering down-regulation and photodamage to PSII is great. Consequently, it is not surprising that measurements of have been used successfully to identify differences in freezing tolerance (Lindgren and Hällgren, 1993; Binder and Fielder, 1996). In white spruce showed a sigmoid correlation to the visible damage to needles after freezing at different temperatures (Binder and Fielder, 1996). In lodgepole pine and Scots pine a linear correlation was observed between and needle damage, and could be used to estimate the critical temperature for 50% needle damage after freezing (Lindgren and Hällgren, 1993).
Many evergreen and hardy deciduous nursery stock plants are lifted during the autumn and are kept bare-rooted in cold store during the winter before being planted in the spring. In Douglas fir it was found that if of needles was high at the time of lifting in the autumn, then survival of plants was low when planted out in the spring (Perks et al., 2001). Clearly, plants which had effectively down-regulated photosynthetic electron transport in the autumn were better fitted to begin growth after the winter period of cold storage. Both and measured at the end of the cold storage showed a sigmoid relationship to root growth potential (Perks et al., 2001). Besides being used to establish optimum lifting time before winter storage, has been used to evaluate the effects of various cultivation techniques on improving survival after freezing (Percival et al., 1999). Regular application of Ca2+ in the nutrient solution was shown to improve survival after freezing in both the freezing-tolerant white poplar and the susceptible hornbeam, with showing higher correlation to survival of plants than ion leakage from roots or leaves, which are the standard assays to test for winter hardiness.
Chilling
The response of crops to low temperatures is generally dependent upon the climatic conditions of the regions from where the plants originated. Crops originating in temperate zones are usually much more tolerant of decreases in temperature than subtropical and tropical species, and depressions in growth and metabolism are rapidly reversed when temperatures rise. However, many crops grown in temperate regions have subtropical and tropical origins and are very sensitive to cool temperatures since they have not developed effective acclimatory responses to cool temperatures which are found in plants native to temperate climates. The growth and physiology of crops of subtropical and tropical origin can be perturbed by exposure to temperatures as high as 15 °C. A widespread response of chilling-sensitive crops to chilling temperatures is the rapid development of inhibition of photosynthesis (Ort, 2002), which, even at moderate light intensities, can result in down-regulation and photodamage to PSII.
A primary effect of reductions in temperature is the inhibition of photosynthetic carbon metabolism (Leegoood and Edwards, 1996; Allen and Ort, 2001; Ort, 2002) which results in a decrease in the sink for the products of electron transport (ATP and NADPH) and (Brüggermann and Linger, 1994; Andrews et al., 1995; Gray et al., 1997; Fracheboud and Leipner, 2003). Generally, this decrease in the rate of utilization of photoreductants and ATP, which results in a decrease in the PSII efficiency factor (), is also accompanied by an increase in the non-photochemical dissipation of excitation energy as down-regulation of PSII occurs, which is reflected by decreases in (Groom and Baker, 1992; Brüggermann and Linger, 1994; Andrews et al., 1995; Gray et al., 1997; Fracheboud and Leipner, 2003). Differences in chilling tolerance have been identified between chilling-acclimated and non-acclimated Lycopersicon peruvianum from the chill-induced decrease in (Brüggermann and Linger, 1994).
Inevitably, chilling stress also results in decreases in and this has been widely used to screen for differences in tolerance to chilling. A particularly interesting example was its use to evaluate the progeny of crosses between chilling-tolerant and high-yielding rice cultivars in Nepal (Sthapit et al., 1995).
For many crops chilling during leaf development can result in chlorotic leaves. A striking example of this problem has been observed in maize where chloroplasts in leaves grown at 14 °C exhibit incomplete development and photosynthetic capacity is limited (Baker and Nie, 1994). The cause of this appears to be an inhibition of the accumulation of a number of chloroplast-encoded thylakoid proteins compared with the nuclear-encoded chloroplast proteins (Nie and Baker, 1991). A similar effect on accumulation of chloroplast-encoded proteins has been observed when tomato leaves are chilled in the dark (Ort, 2002). Such chill-induced perturbations of chloroplast development result in very large reductions in the values of and (Fryer et al., 1995). Consequently, these fluorescence parameters could potentially be used to screen for cultivars tolerant to chilling during leaf development. However, caution is needed when attempting to use and in such screens, since acclimation of maize leaves to growth at low temperatures can result in a relative increase in electron flux to acceptors other than CO2, most probably to oxygen, and this results in elevated values of (Fryer et al., 1998). However, the relative increases in are associated with an increase in the ability to scavenge reactive oxygen species (Fryer et al., 1998) and, consequently, can be considered to reflect tolerance to the chilling stress. When this is a possible complication, the relationship between and the quantum efficiency of CO2 assimilation of the leaves should be examined (Fryer et al., 1998).
High temperatures
High temperature stress can restrict crop growth and productivity (Boyer, 1982) and is likely to become an increasingly important factor with the changing climate. Inactivation of PSII and thylakoid disorganization are considered key features of high temperature stress and have been followed by monitoring the sharp rise in Fo as a function of temperature that indicates the critical temperature for PSII inactivation (Smillie and Nott, 1979; Havaux, 1993). Both the rise in Fo and a decrease in have been used to determine differences in the response of potato cultivars (Havaux, 1995) and species of birch (Ranney and Peet, 1994) to high temperatures. As CO2 assimilation and electron transport are inhibited at high temperatures, measurements of and also have potential for use in screens to identify tolerance to high temperatures.
Nutrition
Nitrogen is one of the most important and managed nutrients in plant production. For many species, a strong correlation exists between total leaf nitrogen and CO2 assimilation at high irradiance (Evans, 1989), consequently, fluorescence is an obvious method to probe nitrogen status. Decreasing nitrogen content of apple leaves was associated with decreases in and (Cheng et al., 2000), although nitrogen contents have to reach very low levels before is affected. However, it is likely that changes in the status of many other nutrients in leaves will have little effect on fluorescence characteristics. For example, reduction of sulphur levels in leaves of sugar beet had to reach starvation levels before any changes in and were observed (Kastori et al., 2000). Consequently, careful studies of the effects of deficiency of specific nutrients on leaf fluorescence characteristics are required before using fluorescence parameters to screen for nutrient deficiencies.
In acidic soils aluminium toxicity can affect crop production. Differences in the fluorescence induction parameters 
and 
(see Fig. 1 for definition) can be used to identify wheat cultivars with tolerance to aluminium (Moustakas et al., 1995). Decreases in 
have been used to detect aluminium stress in cultivars of sorghum (Peixoto et al., 2002) and Citrus species (Pereira et al., 2000). was used in these studies to amplify the rather small changes observed in and enable more readily detection of differences between cultivars; for example, a decrease in from 0.8 to 0.6 corresponds to a decrease in from 4.0 to 1.5. However, it should be noted that 
unlike is non-linearly related to the maximum quantum efficiency of PSII photochemistry.
The use of sewage sludge and incinerator flyash from domestic waste processing for improving the nutrient status of soils has resulted in the build-up of heavy metals in soils (Tan et al., 1999). Decreases in have been shown to distinguish differences in the sensitivity of ornamental plants to heavy metals in such soils (Tan et al., 1999). The use of chlorophyll fluorescence to study effects of cadmium, copper, and mercury on photosynthesis has been recently reviewed (Popovic et al., 2003).
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Glasshouse production |
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TopAbstractIntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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The commercial production of vegetables and ornamental pot plants is a high technology business involving balancing the optimization of plant production with the control of energy costs. Optimization of the daily carbon gain by the crops in the summer and energy saving in the winter can be achieved by dynamic climate control (Hansen et al., 1996
; Aaslyng et al., 2003). It is becoming clear that many subtropical, tropical, and temperate species can cope and grow effectively under much more dynamic climatic conditions than had traditionally been thought to be the case by the horticultural industry. However, a potential limitation to effective optimization of carbon gain by crops is a lack of non-invasive techniques to monitor this parameter in a commercial glasshouse environment. From the above sections it can be seen that fluorescence measurements can be useful in rapidly evaluating the effects of climatic factors, as well as water and nutrient regimes, on plant performance. Consequently, application of fluorescence techniques to study the responses of plants to dynamic climate control have great potential in the future development of systems for optimizing crop production and cost saving in glasshouses.
The use of elevated CO2 is widespread throughout the glasshouse horticultural industry. Elevation of CO2 can increase the temperature optimum for photosynthesis in C3 plants (Leegood and Edwards, 1996) and increase the critical temperature for damage to PSII, which has been monitored from decreases in and increases in Fo (Taub et al., 2000). Also, the ability of plants to acclimate to different light conditions can be monitored by changes in and NPQ (Rosenqvist, 2001), and can potentially provide information for the management of shade screens and supplementary lighting during production. Fluorescence has already proved valuable in investigating the effects of changing climatic conditions (light intensity, temperature, and CO2) on hybrids of the CAM plant Phalaenopsis (Lootens and Heursal, 1998).
An extremely stressful time in the life of potted plants is the propagation phase. Most ornamental cultivars are propagated from cuttings. Fluorescence imaging has been used on stem cuttings from roses to evaluate the role of the leaf in relation to the quality of the propagation (Costa, 2002).
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Post-harvest physiology |
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TopAbstractIntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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In commercial horticultural production, crops are generally either harvested and transported as fresh produce, such as fruits and vegetables, or transported from the sites of production to market as intact plants, such as potted or bare-rooted ornamental and landscape plants. During harvest and transport, plants and produce may be exposed to a range of stress factors that are not normally encountered during the growth of the crop and which can be potentially damaging. Harvested vegetables and cut flowers can experience drought stress after harvest if not handled properly. Fruits, vegetables, and flowers originating in subtropical and tropical regions may be damaged by the chilling temperatures used during storage. Many fruits are exposed to high temperature treatments to remove any infestations prior to transport. Fresh fruit and vegetables are often transported in packages with modified atmosphere to delay senescence; O2 is reduced and CO2 elevated to reduce the rate of metabolic processes linked to the onset of senescence (DeEll and Toivonen, 2003
). Potted plants can be subjected to many days in darkness during transport and are frequently kept in very low light levels in the homes of customers.
Fluorescence can be used to detect perturbations caused by handling and transport of green crops (DeEll and Toivonen, 2003) and even to detect damage in fruits that have chlorophyll in their peels (Nedbal et al., 2000). For example, fluorescence imaging of lemons demonstrated that different types of peel damage had different fluorescence signatures (Nedbal et al., 2000). Damaged regions that became mouldy after a few days had low values, whereas damaged regions that did not develop mould exhibited much higher values. Changes in the mouldy areas when was low were followed by using 
which is inversely and non-linearly related to but will show greater changes than when systems have low PSII photochemical activities. This study demonstrated that fluorescence imaging could be used for automatic sorting of lemons for future fruit quality (Nedbal et al., 2000).
Fluorescence has also been successfully used to determine the optimum O2 and CO2 concentrations to be used in modified atmosphere packages (MAP) used for the transport and storage of vegetables. Measurements made through the unbroken packaging during storage of broccoli showed that decreases and correlated with the production of ethanol, ethyl acetate, and the development of odour, which are all characteristic of deteriorating quality (Toivonen and DeEll, 2001).
Many harvested crops are refrigerated during transport and storage. Many crops are very chilling-sensitive and it has already been discussed above how fluorescence has been used successfully to identify sensitivities and tolerances to chilling conditions. However, fluorescence has also been used to evaluate new storage practices, such as hydrocooling of cucumber (DeEll et al., 2000) and treatment of green bell pepper with the antioxidant diphenylamine to decrease chill-induced pitting (Purvis, 2002). Fluorescence has also been used to investigate the effects of storage at chilling temperatures on cut flowers. Although a linear relationship was found between and days to wilting for cut kangaroo paw flowers stored at 0 °C and 1 °C, this was not the case for flowers stored at 2 °C and above, where flowers showing only small changes in exhibited wilting (Joyce and Shorter, 2000). Clearly, this indicates that factors not affecting primary PSII photochemistry are important in maintaining flower quality at these temperatures and that this fluorescence parameter should not be used to assess quality. However, it is quite possible that measurements of may prove to be a much more useful indicator of the physiological status of cut flowers.
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Concluding remarks |
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TopAbstractIntroductionFluorescence parametersRapid screening of seedling...Fluorescence, leaf...Glasshouse productionPost-harvest physiologyConcluding remarksReferences |
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It is evident that chlorophyll fluorescence can be a very sensitive probe of the physiological status of leaves, which can provide very rapid assessment of plant performance in a wide range of situations. A key factor for the successful application of chlorophyll fluorescence measurements in crop improvement programmes will no doubt be the careful selection of appropriate fluorescence parameters to identify changes in plant performance. This process can often involve considerable investigation of the systems in question in order to provide a satisfactory calibration of the changes in fluorescence parameters with key plant performance indicators. However, once a satisfactory calibration has been achieved, fluorescence will provide an extremely powerful analytical tool for plant selection. Although the attractiveness of fluorescence for screening programmes has been considerably enhanced by the recent development of fluorescence imaging systems that can image quite large areas and allow simultaneous measurement of many plants, further improvements in the size of the surface areas that can be imaged will no doubt be made in the future. Coupling of such technical developments in fluorescence imaging systems with automated sampling systems should enable the agricultural and horticultural industries to improve the quality and rate of many of their plant screening programmes.
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Acknowledgements |
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We are grateful to the very many colleagues who have contributed to our studies on chlorophyll fluorescence and its application to a range of problems. We thank Kevin Oxborough for providing the images used in Fig. 3.
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Footnotes |
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Abbreviations: 2,4-D, 2,4-dichlorophenoxyacetic acid; DCMU, 3-(3',4'-dichlorophenyl) 1,1-dimethylurea; F', fluorescence level at any point between
and ; Fi, transient inflection level of fluorescence immediately after exposure of dark-adapted leaf to actinic light; Fm, maximal fluorescence level from dark-adapted leaves; maximal fluorescence level from leaves in light; Fo, minimal fluorescence level from dark-adapted leaves; 
minimal fluorescence level of leaves in light; Fp, peak level of fluorescence reached on exposure of dark-adapted leaf to actinic light; 
difference in fluorescence between and F' (
); Fv, variable fluorescence level from dark-adapted leaves (
); 
variable fluorescence level of leaves in light (
); PSII operating efficiency (the quantum yield of PSII photochemistry for a leaf in light); the PSII efficiency factor which relates to the ability to maintain PSII reaction centres in the open state; maximum quantum efficiency of PSII photochemistry; PSII maximum efficiency which estimates the maximum quantum efficiency of PSII under given light conditions; NPQ, non-photochemical quenching; PSI, photosystem I; PSII, photosystem II; QA, primary quinone electron acceptor of PSII. |
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 N. Gottig, B. S. Garavaglia, L. D. Daurelio, A. Valentine, C. Gehring, E. G. Orellano, and J. Ottado Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide-like protein to modify host homeostasis PNAS, November 25, 2008; 105(47): 18631 - 18636. [Abstract] [Full Text] [PDF]
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A. Solti, L. Gaspar, I. Meszaros, Z. Szigeti, L. Levai, and E. Sarvari Impact of Iron Supply on the Kinetics of Recovery of Photosynthesis in Cd-stressed Poplar (Populus glauca) Ann. Bot., November 1, 2008; 102(5): 771 - 782. [Abstract] [Full Text] [PDF]
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 J.I.L Morison, N.R Baker, P.M Mullineaux, and W.J Davies Improving water use in crop production Phil Trans R Soc B, February 12, 2008; 363(1491): 639 - 658. [Abstract] [Full Text] [PDF]
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T. Hura, S. Grzesiak, K. Hura, E. Thiemt, K. Tokarz, and M. Wedzony Physiological and Biochemical Tools Useful in Drought-Tolerance Detection in Genotypes of Winter Triticale: Accumulation of Ferulic Acid Correlates with Drought Tolerance Ann. Bot., October 1, 2007; 100(4): 767 - 775. [Abstract] [Full Text] [PDF]
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 H. M. Poulos, U. M. Goodale, and G. P. Berlyn Drought response of two Mexican oak species, Quercus laceyi and Q. sideroxyla (Fagaceae), in relation to elevational position Am. J. Botany, May 1, 2007; 94(5): 809 - 818. [Abstract] [Full Text] [PDF]
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 P. M. O'Neill, J. F. Shanahan, and J. S. Schepers Use of Chlorophyll Fluorescence Assessments to Differentiate Corn Hybrid Response To Variable Water Conditions Crop Sci., February 1, 2006; 46(2): 681 - 687. [Abstract] [Full Text] [PDF]
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 S. Lefebvre, T. Lawson, M. Fryer, O. V. Zakhleniuk, J. C. Lloyd, and C. A. Raines Increased Sedoheptulose-1,7-Bisphosphatase Activity in Transgenic Tobacco Plants Stimulates Photosynthesis and Growth from an Early Stage in Development Plant Physiology, May 1, 2005; 138(1): 451 - 460. [Abstract] [Full Text] [PDF]
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