JXB Advance Access published online on December 22, 2006
Journal of Experimental Botany, doi:10.1093/jxb/erl257
Imaging Stress Responses in Plants Special Issue |
Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging
1Unit of Plant Hormone Signalling and Bio-imaging, Ghent University, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium
2Plant Research Unit, Division of Environmental and Applied Biology, University of Dundee at SCRI, Invergowrie, Dundee DD2 5DA, UK
* To whom correspondence should be addressed. E-mail: laury.chaerle{at}ugent.be; dominique.vanderstraeten{at}ugent.be
Received 8 May 2006; Revised 19 October 2006 Accepted 24 October 2006
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Abstract |
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 Top Abstract IntroductionStress detection and...Screening of crop growth...Plant rhythms and time-lapse...Future developmentsReferences |
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Thermal and chlorophyll fluorescence imaging are powerful tools for the study of spatial and temporal heterogeneity of leaf transpiration and photosynthetic performance. The relative advantages and disadvantages of these techniques are discussed. When combined, they can highlight pre-symptomatic responses not yet apparent in visual spectrum images and provide specific signatures for diagnosis of distinct diseases and abiotic stresses. In addition, their use for diagnosis and for selection for stomatal or photosynthetic mutants, these techniques can be applied for stress tolerance screening. For example, rapid screening for stomatal responses can be achieved by thermal imaging, while, combined with fluorescence imaging to study photosynthesis, they can potentially be used to derive leaf water use efficiency as a screening parameter. A particular advantage of imaging is that it allows continuous automated monitoring of dynamic spatial variation. Examples of applications include the study of growth and development of plant lines differing in stress resistance, yield, circadian clock-controlled responses, and the possible interactions between these parameters. In the future, such dual-imaging systems could be extended with complementary techniques such as hyperspectral and blue-green fluorescence imaging. This would result in an increased number of quantified parameters which will increase the power of stress diagnosis and the potential for screening of stress-tolerant genotypes.
Key words: Chlorophyll fluorescence imaging, hypersensitive reaction, rhythm, screening, stress, thermography
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Introduction |
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TopAbstractIntroductionStress detection and...Screening of crop growth...Plant rhythms and time-lapse...Future developmentsReferences |
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Abiotic and, to a lesser extent, biotic stresses cause considerable crop yield losses (Chrispeels and Sadava, 2003; Oerke and Dehne, 2004). A plethora of imaging techniques has been applied to study plant growth and health with the aim of speeding up stress detection and allowing timely treatment (Nilsson, 1995). One approach to non-contact detection of physiological parameters has been provided by chlorophyll fluorescence imaging from the microscopic to the remote sensing scale (Chaerle and Van Der Straeten, 2000, 2001; Baker et al., 2001). Fluorescence emission increases at an early stage under most stress conditions, its intensity generally being inversely correlated with photosynthetic efficiency (Krause and Weis, 1991; Rolfe and Scholes, 1995; Lichtenthaler and Miehe, 1997), although the share of thermal dissipation in the use of captured light energy possibly changes upon stress (Buschmann, 1999). A complementary technique is thermography which visualizes leaf surface temperature, and is a proxy to transpiration and thus stomatal conductance (Jones, 1999). Stomatal conductance is controlled by a complex regulatory network, which integrates environmental and developmental factors (Fan et al., 2004; Chaerle et al., 2005; Li et al., 2006). Thermography has been successfully used at the laboratory scale to reveal stress situations that affect stomatal conductance (Jones, 2004), but extrapolation of the approach for field use is not straightforward, given the fluctuations in environmental conditions (Grant et al., 2007; Leinonen et al., 2006). The field application of chlorophyll fluorescence imaging also poses some challenges due to the mostly high and varying light levels (Buschmann and Lichtenthaler, 1998; Cerovic et al., 1999; Chaerle et al., 2003b). Laboratory-based screening can avoid the fluctuating environmental factors inherent in field conditions, but field trials remain essential for the studies relating to growth and yield assessment for which imaging solutions are being developed (Corp et al., 2003; Kaukoranta et al., 2005; Rodriguez et al., 2005; Leinonen et al., 2006).
This review provides an overview of imaging approaches to stress detection and quantification, especially those involving combinations of thermal and fluorescence or reflectance imaging techniques, and their potential application to genetic screening and the monitoring of growth dynamics. Possible applications of combined imaging as a screening tool for crop yield improvement are discussed, in particular by engineering the efficiency of plant responses to the fluctuating diel and environmental conditions.
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Stress detection and identification |
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TopAbstractIntroductionStress detection and...Screening of crop growth...Plant rhythms and time-lapse...Future developmentsReferences |
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Chlorophyll fluorescence and thermal imaging are well established as non-destructive methods for detecting and diagnosing plant stresses. Thermal and chlorophyll fluorescence imaging techniques can be complementary in providing information on the effect of treatments on both stomatal and photosynthesis-related parameters, two of the key factors that determine plant yield (Omasa and Takayama, 2003; West et al., 2005). This section gives an overview of stress-monitoring approaches with an emphasis on the complementarity and respective benefits of thermal and fluorescence imaging techniques that make them particularly suitable for use in combination.
Chlorophyll fluorescence imaging has been shown to be capable of revealing spatial and temporal changes during plant stress development (Chaerle and Van Der Straeten, 2000, 2001; Soukupova et al., 2003; Berger et al., 2007) as well as environmental effects on several aspects of whole plant physiology (Gielen et al., 2005). Current chlorophyll fluorescence imaging systems can monitor the photosynthetic characteristics of several plants in parallel, and have been applied in screens for herbicide resistance and pathogen toxin responses (Barbagallo et al., 2003; Soukupova et al., 2003; Oxborough, 2004). All current chlorophyll fluorescence imaging systems need a dedicated illumination system.
Thermography, in contrast, is generally used as a passive technique, relying on imaging the long-wave (thermal) radiation emitted by the subject as an indicator of leaf temperature, which itself is indicative of changes in leaf transpiration (Jones, 2004). It is also possible, however, to use thermography in an active mode by following temperature kinetics after changes of incident radiation. Such dynamic thermal imaging (active thermography) can be used, for example, to estimate heat capacity per unit area (and thus water content) distribution in leaves (Kümmerlen et al., 1999; Chaerle and Van Der Straeten, 2000), or to study boundary layer transfer properties or even stomatal conductance (Jones, 2004; Bajons et al., 2005). Analogous, dynamic thermal imaging approaches are also used in remote sensing to estimate surface soil moisture content based on the apparent thermal inertia (I; J m–2 K–1 s–1/2) of the surface (Verhoef, 2004; Verstraeten et al., 2006). The time lag of the response of the surface temperature of a solid (related to thermal inertia) depends on both the heat capacity of the material and its thermal conductivity according to
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is the density (kg m–3), cp is the specific heat capacity (J kg–1 K–1), and k is the thermal conductivity of the surface soil (W m–1 K–1). When applied to leaves, rather than soils, the time constant depends only on the first two of these terms, since heat conduction over the thickness of a leaf is very fast. When a leaf is monitored by active thermography, leaf veins may be expected to lag behind the rest of the leaf surface in their adjustment to altered incident energy as a result of their higher mass and water content per unit area. Dynamic imaging of leaves is currently feasible only in controlled environments as constant environmental conditions are necessary (Kümmerlen et al., 1999).
An important difference between chlorophyll fluorescence imaging and thermography is their differing spatial resolution. Fluorescence imaging is capable of resolving subcellular effects, such as at a chloroplast scale (Oxborough, 2004), while thermography can only effectively resolve patches of the order of mm2, and therefore is unsuitable for the study of individual stomatal guard cells. Indeed, Jones (1999) pointed out that the maximum thermal gradient that could be detected in a typical leaf is likely to be no more than 
0.3 K mm–1. At the other end of the spatial scale, chlorophyll fluorescence is not easy to apply to plant canopies outdoors because of the need for adequate energizing radiation, although utilization of Fraunhofer lines in the solar spectrum to extend fluorescence measurement to a canopy level (Moya et al., 2004; Meroni and Colombo, 2006) is, in principle, applicable to imaging, In contrast, thermal imaging is particularly suited to outdoor measurements and to larger spatial scales including airborne and satellite.
As an example of the complementary information available at a subleaf scale, leaf veins often show a higher temperature in comparison with the rest of the leaf lamina, due to their lack of stomata, when viewed by passive thermography under constant temperature conditions, Hence, the first stages of stomatal closure induced by, for example, a xylem-transported compound, starting from the vein cannot be visualized by thermography. However, chlorophyll fluorescence imaging can be successfully applied since the higher intensity chlorophyll fluorescence of the tissue immediately adjacent to the veins (indirectly caused by the above-mentioned stomatal closure) can be visualized with high contrast against the dark (less chlorophyll-containing than the leaf lamina) leaf veins (Chaerle et al., 2003a).
Biotic stresses
The most appropriate imaging techniques for any particular stress need to be selected on the basis of laboratory studies of the specific ‘signature’ physiological responses, although both chlorophyll fluorescence and thermography have been used to reveal bacterial, viral, fungal, and oömycete infections (Balachandran et al., 1997; Chaerle et al., 1999; Chou et al., 2000; Boccara et al., 2001; Berger et al., 2004; Lindenthal et al., 2005; Scharte et al., 2005). The thermal signal generally depends on differences in evaporation rate, with areas of high temperature reflecting stomatal closure, and low temperature reflecting stomatal opening or tissue damage. Although changes in respiration rate (potentially thermogenic) should affect temperatures, the effect is generally small in comparison with the result of changing rates of water loss (Jones, 2004). Pathogens can influence stomatal behaviour by releasing specific compounds inducing plant resistance responses, or by interfering with water transport (Chaerle et al., 2004; Jones, 2004; Melotto et al., 2006; Prats et al., 2006). As an illustration of the sequence of events upon plant resistance-induced cell death [hypersensitive response (HR)] revealed by thermography, the hypersensitive reaction of tobacco to tobacco mosaic virus (TMV) is summarized below. First, a leaf temperature increase is apparent; this is caused by stomatal closure resulting from accumulation of salicylic acid (Chaerle et al., 1999). Typically, the thermal effect expands rapidly from its initial detection site one and a half days post-infection, and gradually declines thereafter. The final visual damage (necrotic lesions) observed 8 d after infection corresponded in area to the maximum extension of the thermal effect at 2 d after infection (Fig. 1). Hence, the area of the thermal effect upon HR cell death could be used as a quantification measure in screening approaches, anticipating disease progression.
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In practice, however, the thermal effect during plant–pathogen interactions is not necessarily associated with hot spots. As an example of a biotrophic interaction without HR, Cercospora infection in sugar beet led, in its early stages, to pronounced and rapidly spreading cold spots (Fig. 2A) (Chaerle et al., 2004). Infection is not synchronized and the progression of the disease is characterized by the appearance of multiple initiation sites on the leaf (Fig. 2B).
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Pathogens, in general, also affect the photosynthetic electron transport or the downstream metabolic reactions, resulting in an increase of chlorophyll fluorescence at the early stages of infection. For both the tobacco–TMV and beet–Cercospora plant–pathogen interactions, spots of higher chlorophyll fluorescence intensity co-located with the thermal symptoms (and with the subsequently spreading visual damage). These symptoms, which expand beyond the visible symptoms in the co-localized visible spectrum reflectance images (hereafter referred to as visible images), indicate an inhibition of photosynthetic electron transport. Photosynthetic inhibition in visually unaffected tissue was also observed in the bean–Cercospora interaction, as imaged with high-resolution chlorophyll fluorescence imaging, indicating the possibility of predicting final yield loss in screening applications (Meyer et al., 2001). The effect a pathogen can exert on the tissue surrounding the visible damage was further highlighted by studies on fungal (Botrytis cinerea) and bacterial (Pseudomonas syringae) infection of tomato, where an increase in photosynthesis was demonstrated, not being limited to the actually infected tissue (Berger et al., 2004). For infection with another class of plant pathogens, the oömycete powdery mildews, a pre-symptomatic decrease in leaf temperature was observed in cucumber (Lindenthal et al., 2005). Likewise, a bacterial toxin-induced cell death was revealed as low-temperature spots at an early stage (Boccara et al., 2001).
Developing cell death, resulting from a multitude of biotic or abiotic influences, can be readily visualized with chlorophyll fluorescence and thermal imaging. The contrast between unaffected and lesioned areas is markedly higher than in visible images, facilitating automated quantification. The typically finer spatial resolution of chlorophyll fluorescence imaging compared with thermal imaging is advantageous to reveal and quantify the earliest stress-induced symptoms (appearing as minute pin-point spots). Using chlorophyll fluorescence images, cell death and tissue survival can be quantified by defining a limit of intensity which divides background from plant information, and saving to a binary image (thresholding). White (1 values) correspond to healthy tissue, whereas black (0 values) correspond to background and cell death areas. In spontaneous disease-like lesion-forming Arabidopsis mutants and tobacco transgenics, the process of cell death was visualized with high contrast (Chaerle et al., 2001). A similar correlation between loss of chlorophyll fluorescence and the first stages of cell death was demonstrated during the HR of potato to Phytophthora (Scharte et al., 2005).
Autoluminescence imaging or biophoton imaging, which captures the spontaneous ultra weak emission of photons typically associated with oxidative stress reactions (Havaux et al., 2006), has been shown to discriminate the hypersensitive disease reaction (indicating plant resistance) from a lesion caused by attack of a virulent pathogen (Al-Daoude et al., 2005; Bennett et al., 2005). A drawback is that this technique needs to be carried out in a dark cabinet to allow the amplification of the weak signal, the origin of which still needs confirmation (Bennett et al., 2005; Mansfield, 2005). However, biophoton imaging will be likely to be useful in stress monitoring, for example, to discriminate the HR from cell death induced by other stress factors.
In addition to pathogen damage, insect herbivory also leads to considerable yield losses. Importantly, in addition to the loss of the consumed leaf tissue, insect feeding can also decrease the photosynthetic yield of tissues adjacent to the feeding sites. By using both chlorophyll fluorescence and thermal imaging, this systemic effect was shown to be mainly due to local water stress induced by the feeding damage (Tang et al., 2006). The combined use of thermal and chlorophyll fluorescence imaging thus can aid in accurately quantifying the damage caused by insect pests. As a possible complementary technique, near infrared reflectance (NIR) imaging is particularly suitable for field applications to differentiate vegetation from background (soil), and has been applied in a machine vision system to detect insect infestations in maize, based on the inhibition of leaf growth (reduced leaf area) (Zandonadi et al., 2005).
Abiotic stress
Imaging techniques including chlorophyll fluorescence imaging and thermography (Chaerle and Van Der Straeten, 2000), as well as reflectance imagery (Nilsson, 1995), multispectral fluorescence imaging (Lichtenthaler et al., 2005), and autoluminescence imaging (Havaux et al., 2006), have been extensively used for monitoring of the effects of abiotic stresses. Indeed most applications of thermal imaging have related to monitoring plant responses to water deficit stress (Jones, 2004). Changes in chlorophyll emission or leaf temperature associated with water stress usually affect the whole plant (Luquet et al., 2003; Blom-Zandstra and Metselaar, 2006). Wounding and, to a certain extent, nutrient stresses cause more localized responses (Chaerle et al., 2002; Corp et al., 2003; Quilliam et al., 2006). Low nitrogen stress has been revealed with multispectral fluorescence imaging (Lichtenthaler et al., 2005). Alternatively, nitrogen stress can also be detected by quantifying the decrease in chlorophyll content (as caused by N deficiency), with multispectral reflectance imaging (Borhan et al., 2004; Noh et al., 2006). Application of these techniques in precision agriculture will help to avoid excess fertilizer application while assuring optimal productivity. Toxicity effects exerted by soil contaminants such as heavy metals and persistent herbicides have also been revealed with chlorophyll fluorescence imaging (Ciscato and Valcke, 1998; Chaerle et al., 2003a). Combined approaches using both thermal and chlorophyll fluorescence imaging would have the added benefit of potentially monitoring (and identifying) different stresses simultaneously.
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Screening of crop growth performance |
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TopAbstractIntroductionStress detection and...Screening of crop growth...Plant rhythms and time-lapse...Future developmentsReferences |
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The major limitations to plant growth and development are water shortage and suboptimal light conditions. Under such conditions, growth slows down and plant leaf area is visibly reduced. Thermal and chlorophyll fluorescence imaging can reveal the early signs of the imposed stress, thus making it possible to visualize the most stress-tolerant plant lines in a screening set up. The efficient use of water in crop production, given the increasing reliance on irrigation (www.unesco.org/water), will be a key point in the coming years (Chaves and Oliveira, 2004; Chaerle et al., 2005; Valliyodan and Nguyen, 2006). For the successful engineering of stress-resistant food crops, a detailed knowledge of the interacting stress signalling pathways will be a prerequisite (Valliyodan and Nguyen, 2006). This also implies screening for plant lines, cultivars or mutants with increased tolerance to particular stresses. Subsequent characterization of metabolic and molecular mechanisms underlying this tolerance can be applied to engineer crop performance under stress conditions.
Water usage can be determined from weight loss and gas exchange measurements (Weyers and Meidner, 1990; Tocquin and Perilleux, 2004; Chaerle et al., 2005; Helmer et al., 2005). Unfortunately, these approaches are time-consuming and only suitable for experiments with small numbers of lines so cannot be readily used for crop phenotyping, although an automated weighing approach was proven to be successful (Granier et al., 2006). A major advantage of imaging techniques is that they can be used to screen large numbers of plants simultaneously, with thermography being particularly valuable for screening for stomatal behaviour and water use (Kümmerlen et al., 1999; Jones, 2004; Horie et al., 2006). Thermography has been successfully used to isolate Arabidopsis and barley mutants with the inability to close stomata, based on their cool signature (Raskin and Ladyman, 1988; Merlot et al., 2001, 2002; Mustilli et al., 2002; Riera et al., 2005). Conversely, screening for high leaf temperature has led to the identification of novel mutants that allowed further insight into the molecular characterization of stomatal regulation (Wang et al., 2004; Liang et al., 2005). Knowledge of the molecular mechanisms involved in water use efficiency (Masle et al., 2005) will be enhanced by the application of imaging techniques. In addition, the regulation of stomatal conductance by CO2 availability can also be revealed efficiently by thermography (Hashimoto et al., 2006; Messinger et al., 2006). This ability could aid in screening for yield-enhancing cultivars under the globally increasing CO2 levels.
In the case of water stress, it has been proposed that limitation of gas exchange by stomatal closure is the main inhibitory effect on assimilation, with increased mesophyll resistance to CO2 diffusion playing a secondary role (Flexas et al., 2006), although this conclusion probably does not hold in all cases. Efficient simultaneous visualization of leaf conductance (thermography) and photosynthesis (chlorophyll fluorescence) might allow ready resolution of such questions and will further increase throughput and detecting power in drought stress screening programmes (Granier et al., 2006). At the field scale, direct feedback of thermal imaging-derived water status information on water management shows great promise (Cohen et al., 2005; Grant et al., 2007; Leinonen et al., 2006), with some studies showing an association with crop yield (Horie et al., 2006). Also, in greenhouse environments, thermography can reveal water shortage at early stages, although care is needed (as in the field) to account for variability of leaf angles and irradiance (Kaukoranta et al., 2005; Grant et al., 2006). With further improvements, effective screening under the conditions for crop production would become possible. In summary, imaging techniques have the clear benefit of quantification and repeatability for parallel testing of crop performance of multiple transformed lines.
Under field conditions, plants have to adapt to weather-dependent changes in irradiance. This adaptability ensures optimal assimilation rates and avoids damage under high light. Chlorophyll fluorescence imaging-based screening has been exploited to isolate mutants defective in acclimation to changing irradiance (Walters et al., 2003). Identification of genotypes with an optimal adaptability to varying irradiance should contribute to improved yields under appropriate situations.
In addition, there have been suggestions that efficient lateral diffusion of CO2 in leaves might alleviate the effects of excess light, especially under water-limited conditions. In this context, chlorophyll fluorescence imaging has been used to visualize differences in lateral diffusion kinetics upon shading, depending on internal leaf architecture (Pieruschka et al., 2006). On the other hand, chlorophyll fluorescence imaging has also been used to show that lateral diffusion was spatially limited in some species (Morison et al., 2005). Further imaging studies will help to elucidate whether differences between species can explain these discrepancies (Lawson and Morison, 2006).
Chlorophyll fluorescence emission spectra have been exploited for yield prediction from measurements before crop maturation (Anderson et al., 2004). This non-imaging method, which relies on the measurement of the two peaks of chlorophyll fluorescence, at 690 nm (F690; red) and 740 nm (F740; far red) (Krause and Weis, 1991; Lichtenthaler and Miehe, 1997), could be converted to a powerful imaging tool. The ratio of fluorescence F690 to F740 is indicative of (active) chlorophyll content, determining photosynthetic activity and thus assimilative yield (Buschmann and Lichtenthaler, 1998). This and other imaging approaches might well complement the successful use of carbon isotope discrimination as a measure of water use efficiency in a breeding programme for drier areas (Condon et al., 2004). A problem with this latter approach is that it measures the intercellular CO2 concentration, as a measure of water use efficiency, but it does not discriminate between stomatal closure and improved photosynthetic activity as causes of enhanced water use efficiency. A combination of thermal imaging to study the stomatal conductance, and fluorescence imaging to study the photosynthetic activity, might, in principle, allow an improved discrimination of the preferred high photosynthetic activity lines rather than those lines which simply close stomata and therefore lose yield potential (Chaerle et al., 2005; Masle et al., 2005).
Imaging technology based on conventional RGB (red, green, blue) reflectance provides a powerful tool for continuous monitoring of growth (Walter and Schurr, 2005). However, taking the third dimension of the crop canopy into account will be needed to facilitate quantification of canopy growth and should permit predictive modelling of yield (Kaminuma et al., 2004). The approach can be extended to the study of kinetics of plant development and the changes of plant physiological parameters over time, based on leaf area extracted from time-lapse images, although diurnal (circadian) leaf movements have to be taken into account. Circadian and growth movements result in leaf overlap, which is difficult to estimate based on 2D images, wherein the projected leaf area apparently changes. Nevertheless, using visible 2D images of Arabidopsis plants, the detected leaf area was found to be proportional to the growth performance of different ecotypes (Leister et al., 1999). Information from several images captured in parallel with different imaging techniques can be combined to obtain periodical information on thermal, chlorophyll fluorescence and leaf area parameters (Fig. 3). Such data sets captured from a population of plants will allow the identification of individuals with an optimal growth performance under the chosen conditions, and to determine the mechanism of the selective advantage.
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Related machine vision technologies have been described where leaf movement is correlated with drought stress and applied for crop management in both controlled environments and greenhouses (Kacira and Ling, 2001; Kacira et al., 2002a). Such systems can also incorporate thermal sensing (Kacira et al., 2002b). It is considered that precision agriculture should be able to benefit from improved integration of a wide range of imaging sensors to help adjust crop demands to necessary inputs for profitable and sustainable food production (Rodriguez et al., 2005) and their incorporation into yield-mapping technologies. The combination of thermal and visual images to extract canopy-specific temperatures will open the road to field-based assessment of crop performance as a function of time (Leinonen and Jones, 2004; Rodriguez et al., 2005). The key step in this development will be the improvement of automated algorithms to discriminate between leaves and background in a wide range of field situations.
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Plant rhythms and time-lapse imaging |
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TopAbstractIntroductionStress detection and...Screening of crop growth...Plant rhythms and time-lapse...Future developmentsReferences |
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Imaging can contribute to improving our understanding of the regulation of circadian rhythms and the mechanisms of co-ordinated stomatal responses to changes in environmental conditions; indeed it is really only imaging that can be used to study spatial variation over time. For example, to achieve maximal growth efficiency, plant physiological processes need to be synchronized to the changing environment imposed by the natural day/night cycle and variable weather conditions. There are indications that an efficiently integrated circadian clock helps to optimize plant yield by a time-efficient and predictive (anticipatory) control of stomatal opening (Green et al., 2002; Dodd et al., 2005; Dunford et al., 2005). Long-term parallel monitoring of gas exchange on several individuals or plant lines is possible in cuvette systems (Dodd et al., 2004); however, when operated under strict environmental control, thermal and chlorophyll fluorescence imaging also enable high-throughput screening of large numbers of plant cultivars for their response to changes in environmental factors. Imaging can contribute to improving our understanding of the regulation of circadian rhythms and the mechanisms of co-ordinated stomatal responses to changes in environmental conditions.
The research field of chronobiology (representing biological clock-related studies) has made extensive use of luciferase imaging (which needs genetic transformation of the plants to be studied) for revealing cyclic and circadian patterns of gene expression (McClung, 2006). In addition, chlorophyll fluorescence and visible spectrum reflectance time-lapse growth monitoring reveal the dynamic patterns of metabolism that underlie the adaptability of plant development to the changing environment (Walters et al., 2003; Schurr et al., 2006), while rhythms in stomatal behaviour have been characterized using direct microscopical visualization or gas exchange measurements (Meidner and Mansfield, 1968; Weyers and Meidner, 1990).
Specific mutations in genes involved in stomatal control can reveal not only the obvious changes in control of stomatal aperture, but also alterations in the speed of responses to environmental stimuli (Hosy et al., 2003). Although this type of mutant can be characterized using gas exchange measurements, combined thermal and chlorophyll fluorescence imaging would be particularly suited for such studies, and for the follow-up screening of plant lines engineered for increased (drought) stress resistance.
Changes in environmental factors can induce both stomatal oscillations and stomatal patchiness. The study of both of these responses is ideally suited to analysis using imaging approaches. The phenomenon of stomatal patchiness, the heterogeneous response of groups of stomata on the same leaf surface, is thought to result from a mechanism co-ordinating optimal adjustment of stomatal aperture to changing environmental factors on the plant scale (Peak et al., 2004). Stomatal patchiness, or at least its consequences for photosynthesis, is commonly visualized with chlorophyll fluorescence imaging, although in some cases simultaneous chlorophyll fluorescence and thermal imaging have been used to demonstrate stomatal patchiness induced by a decrease in humidity (West et al., 2005). In this study, the changes in chlorophyll fluorescence were unequivocally proven to be caused by changes in stomatal conductance, which appeared to behave in an oscillatory way with periods of several minutes. In plants with CAM photosynthesis, which allows survival under arid conditions (Bohn et al., 2001), chlorophyll fluorescence imaging in combination with gas exchange revealed circadian rhythms in plant assimilative metabolism and stomatal conductance (Rascher and Luttge, 2002). This strict regulation is key to the increased assimilation efficiency under adverse conditions. Oscillatory patterns of transpiration in oats, induced by increased illumination or exposure to low air humidity, have also been visualized with thermography, again in parallel with gas exchange measurements (Prytz et al., 2003a, b). In this case, the oscillations were synchronized across the leaf surface with periods of 20 min, in contrast to the observed dynamics of stomatal patchiness. These contrasting spatial dynamics are likely to be due to the differences in anatomy between monocotyledonous plants and dicots. There is some evidence that circadian regulation of leaf hydraulic conductance is involved in oscillatory stomatal conductance (Nardini and Salleo, 2005; Nardini et al., 2005).
Thermography and chlorophyll fluorescence imaging can be advantageously used for continuous circadian plant monitoring, both to visualize whole plant responses and to follow the responses of individual leaves (see also Fig. 3). The effect of step changes in growth conditions has a clear potential to be exploited for screening. For example, the effect of a rapid decrease in relative humidity on a population of mutated Arabidopsis plants was studied by thermal imaging, and used to characterize genes involved in the stomatal response to air humidity (Xie et al., 2006), a factor which also fluctuates during a natural day. Likewise, the response to a day–night transition or step change in light level or temperature can be used to provide information applicable to the improvement of crop adaptability and yield performance. Application of NIR imaging and illumination, assumed not to induce phototropic responses in plants (Whippo and Hangarter, 2005) is the method of choice for studies of diurnal plant movements, information that can be complementary to thermal and chlorophyll fluorescence data.
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Future developments |
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TopAbstractIntroductionStress detection and...Screening of crop growth...Plant rhythms and time-lapse...Future developmentsReferences |
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Thermal and chlorophyll fluorescence imaging can reduce the time needed for screening-based estimation of growth performance. These techniques can be further complemented by UV-induced blue-green fluorescence, which directly visualizes inherently fluorescing compounds that accumulate under stress conditions (Buschmann and Lichtenthaler, 1998; Cerovic et al., 1999; Chaerle et al., 2007; Lenk et al., 2007). To obtain increased monitoring and stress-discriminating capability, multicolour fluorescence set-ups could be used. The advantage of this combined method is that it delivers data from different spectral regions, integrating red and far-red chlorophyll fluorescence in addition to blue and green fluorescence (Chaerle et al., 2007).
Combination of UV-induced fluorescence and hyperspectral imaging has already shown promise for in-field detection of plant diseases (Moshou et al., 2005). Hyperspectral reflectance imaging provides information from multiple narrow wavelength zones [typically of a few (tens) of nanometres], the combination of which can be indicative of specific stresses (e.g. revealing the accumulation of particular compounds; West et al., 2003; Muhammed, 2005). Based on the above-mentioned multisensor monitoring approaches, it is suggested that it should be possible to establish a robust ‘stress-catalogue’ that might be used to diagnose and quantify different stress responses on the basis of their characteristic stress-specific signatures. This could evolve towards an early warning expert system. Screening programmes will benefit from this catalogued information, and data on the temporal characteristics of plant physiological parameters will provide additional leads for crop improvement.
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Acknowledgements |
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DVDS and HGJ are grateful to the European Community for financial support provided through the Human Potential Programme under contract HPRN-CT-2002-00254, STRESSIMAGING. IL is a research fellow in this European network. LC is a post-doctoral fellow of the Research Foundation-Flanders.
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Abbreviations |
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HR, hypersensitive reaction; NIR, near infrared; TMV, tobacco mosaic virus.
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References |
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TopAbstractIntroductionStress detection and...Screening of crop growth...Plant rhythms and time-lapse...Future developmentsReferences |
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