JXB Advance Access originally published online on April 8, 2004
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Journal of Experimental Botany, Vol. 55, No. 400, pp. 1187-1193, May 1, 2004
© 2004 Oxford University Press
Limitations to Photosynthetic Performance |
Seeing ‘cool’ and ‘hot’—infrared thermography as a tool for non-invasive, high-throughput screening of Arabidopsis guard cell signalling mutants
Received 15 September 2003; Accepted 24 February 2004
1 Department of Biological Sciences, Institute of Environmental and Natural Sciences, Lancaster University, Bailrigg, Lancaster LA1 4YQ, UK
2 Department of Botany, University College Dublin, Belfield, Dublin 4, Ireland
* Present address: Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK. To whom correspondence should be addressed. Fax: +353 1 716 1153. E-mail: carl.ng{at}ucd.ie
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Abstract |
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 Top Abstract IntroductionInfrared thermography: a non...Isolating novel mutants: Open...Isolating mutants using a...Concluding remarksReferences |
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The use of Arabidopsis mutants defective in abscisic acid (ABA) perception has been instrumental in the understanding of stomatal function, in particular, ABA signalling in guard cells. The considerable attention devoted to ABA signalling in guard cells is due in part to (1) the fundamental role of ABA in drought stress and (2) the use of a screening protocol based on the sensitivity of seed germination to ABA. Such a screen has facilitated the isolation of ABA signalling mutants with genetic lesions that exert pleiotropic effects at the whole plant level. As such, there is a requirement for new approaches to complement the seed germination screen. The recent advances made in the use of infrared thermography as a non-invasive, high-throughput tool are reviewed here and the versatility of this technique for screening Arabidopsis defective in stomatal regulation is highlighted.
Key words: Arabidopsis, drought, EMS mutants, infrared thermography, low humidity.
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Introduction |
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TopAbstractIntroductionInfrared thermography: a non...Isolating novel mutants: Open...Isolating mutants using a...Concluding remarksReferences |
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Stomata are pores on leaf surfaces that function as gateways linking the intracellular leaf spaces to the external environment. Two guard cells surround the stomatal pore and changes in turgor of the guard cells serve to regulate the size of the pore opening. An increase in guard cell turgor results in stomatal opening whereas a reduction in turgor leads to stomatal closure (Mansfield et al., 1990; Willmer and Fricker, 1996). Stomata can, therefore, be viewed as valves, controlling carbon dioxide assimilation for photosynthesis and loss of water via transpiration. The need to maximize carbon dioxide assimilation and to limit excessive water loss via transpiration requires the optimal functioning of a robust signalling network within individual guard cells for perceiving changes in the external environment, integrating and transducing these signals leading ultimately to regulated changes in guard cell turgor (Assmann, 1993; MacRobbie, 1998; Blatt, 2000; Assmann and Wang, 2001; Hetherington, 2001; Schroeder et al., 2001a, b; Hetherington and Woodward, 2003).
Identifying the individual components of this signalling network has been the subject of considerable attention. Although guard cells are competent to respond to a variety of external stimuli, for example, light, abscisic acid (ABA), carbon dioxide, auxin, and oxidative stress, the signalling network by which ABA brings about changes in guard cell turgor has been most intensively investigated (Assmann, 1993; MacRobbie, 1998; Blatt, 2000; Assmann and Wang, 2001; Hetherington, 2001; McAinsh et al., 2001; Ng et al., 2001; Schroeder et al., 2001a, b; Hetherington and Woodward, 2003). ABA has long been regarded as the key molecule in the response of plants to drought because it is synthesized in the roots and its concentration builds up in leaves during conditions of decreased water availability, leading to reductions in the aperture of the stomatal pore (Davies and Zhang, 1991). Decreasing transpirational loss by this mechanism enables the plant to conserve water and hence tolerate periods of drought. As adverse environmental conditions, including drought, can greatly compromise photosynthetic performance and hence plant productivity, an understanding of the organization and workings of the ABA signalling network has far-reaching implications, from the development of efficient agronomic practices to the engineering of drought-resistant crops (Schroeder et al., 2001b).
Much of the current understanding of ABA signalling in guard cells has relied on the combined application of cellular, molecular, and genetic approaches. The use of Arabidopsis thaliana mutants defective in ABA perception has been instrumental in the understanding of ABA signalling in guard cells. The ABA-insensitive mutants (abi1 and abi2) were first isolated by Koornneef et al. (1984) based on germination assays conducted in the presence of ABA. Two independent studies (Meyer et al., 1994; Leung et al., 1994) showed that the carboxy-terminal end of ABI1 is related to serine-threonine phosphatase 2C with a unique amino-terminal extension containing an EF hand Ca2+ binding site. Roelfsema and Prins (1995) used the abi1 and abi2 mutants to show the involvement of ABI1 and ABI2 in the ABA-signalling network, mediating changes in guard cell turgor. To date, numerous other ABA signalling mutants have also been isolated by this approach and these include era1 (Cutler et al., 1996; Pei et al., 1998; Allen et al., 2002), gca2 (Himmelbach et al., 1998; Pei et al., 2000), abh1 (Hugovieux et al., 2001), and rop10 (Zheng et al., 2002). In addition, other mutations, such as rcn1 (Kwak et al., 2002) and mrp5 (Klein et al., 2003) that attenuated stomatal responses to ABA, also affected other ABA-mediated responses such as seed germination and root elongation. While useful, this approach effectively rules out the isolation of mutants habouring genetic lesions that specifically affect ABA sensitivity in stomatal guard cells. Assmann and co-workers (Li and Assmann, 1996; Li et al., 2000) reported the isolation and cloning of a guard cell-specific ABA-activated, Ca2+-independent protein kinase (AAPK) that is involved in ABA regulation of slow anion channels. More recently, Zhu et al. (2002) showed that the syntaxin protein, OSM1/SYP61 mediates ABA sensitivity only in stomatal guard cells and not in seed germination or root elongation in Arabidopsis. It is noteworthy that OSM1 also affected responses to salt (NaCl) and osmotic stress. The work of Zhu et al. (2002) is in agreement with the observations of Blatt and co-workers (Leyman et al., 1999) who showed that the tobacco syntaxin, Nt-Syr1 is involved in ABA regulation of both guard cell potassium and chloride channels and hence stomatal function. In addition, both Nt-Syr1 and OSM1/SYP61 have been shown to be involved in root development (Leyman et al., 1999, 2000; Geelen et al., 2002; Zhu et al., 2002). Nevertheless, these observations suggest that certain components of the ABA signalling network may be limited to guard cells only. As such, there is a requirement for additional approaches for the screening and isolation of mutants that habour genetic lesions specifically affecting guard cell signalling.
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Infrared thermography: a non-invasive, high-throughput approach |
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TopAbstractIntroductionInfrared thermography: a non...Isolating novel mutants: Open...Isolating mutants using a...Concluding remarksReferences |
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Thermography is the use of specially designed infrared video or still cameras to ‘see’ thermal energy emitted from a surface. Infrared thermography cameras detect infrared radiation and converts it into an electronic signal that is subsequently processed to produce thermal images, allowing for non-contact temperature measurements (see Table 1 for some of the infrared cameras that have been used for thermography in plant systems). Infrared thermography has been used successfully to measure the spatio-temporal variations in stomatal conductance over leaves (Jones, 1999; Jones et al., 2002; Prytz et al., 2003). It is noteworthy that a strong correlation was observed between stomatal conductance calculated from infrared thermography and estimates obtained from diffusion porometry (Jones, 1999). It remains to be determined if such a strong correlation can be observed using the Arabidopsis. As pointed out by Jones (1999), there can be limitations to the accuracy of the measurements. For example, if the stomatal conductance of the lower and upper epidermes varies by less than 5-fold, the error in the estimation of total leaf conductance will be significant. For a comprehensive overview of the usefulness of infrared thermography for estimating stomatal conductances, the reader is referred to excellent papers from the Jones laboratory (Jones, 1999; Jones et al., 2002). The isolation of a ‘cool’ barley mutant with stomata that is insensitive to ABA provided the first indications that infrared thermography can be used for screening mutants with altered stomatal function (Raskin and Ladyman, 1988). More recently, Merlot et al. (2002) have used infrared thermography as a non-invasive, high throughput tool for screening large populations of Arabidopsis to identify mutants showing a different leaf temperature compared with wild-type plants. The approach adopted by Merlot et al. (2002) was aimed at visualizing leaf temperature profiles between plants in a population. This removes the laborious task of measuring the absolute leaf temperatures for individual plants in a population.
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As a first step towards establishing a robust protocol for the thermal screen, Merlot et al. (2002) spiked two abi1-1 mutants plants (whose stomata are insensitive to ABA) into a population of about 40 wild-type Arabidopsis plants. The plants were well-watered for 10 d before being subjected to drought stress for 3 d. After 3 d of drought stress, the two abi1-1 mutant plants were clearly visible in the pseudocoloured infrared image as having leaf temperatures approximately 1 °C cooler compared with the wild-type plants (Fig. 1).
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A similar approach to Merlot et al. (2002) has been used in the infrared thermography screen. An Inframetrics SC1000 infrared camera (FLIR Systems) equipped with a 16° lens and a 256x256 pixels platinum silicide (PtSi) focal plane array detector with variable integration was used. This camera has a spectral range of 3.5–5.0 µm and a sensitivity of 0.07 °C. The specifications of this camera were similar to the one used by Merlot et al. (2002) (Table 1). Post-acquisition analysis of acquired images were performed using Thermogram Pro (Thermometrix Systems). However, instead of using a 3 d drought-stress treatment, plants were subjected to a low-humidity treatment by removing the lids of the propagators in which the plants were growing. Figure 2A shows the pseudocoloured infrared image of abi1-1 mutants and wild-type Arabidopsis plants. The results show that a low-humidity treatment is sufficient to show differences in the leaf temperature profiles of the abi1-1 mutants and the wild-type plants, suggesting that there is a difference in the stomatal conductance between these plants. This is interesting as Assmann et al. (2000) showed, using gas exchange experiments, that the stomatal conductance of the abi1-1 mutants and wild-type Ler are identical, regardless of the vapour pressure difference (Fig. 2B). The discrepancy between these observations and those of Assmann et al. (2000) is puzzling because Jones (1999) has clearly demonstrated a strong correlation between stomatal conductance calculated from infrared thermography and estimates obtained from diffusion porometry in Phaseolus vulgaris. This raises the question of whether Arabidopsis exhibits such correlation and makes a compelling case for investigating the relationship between estimates obtained from diffusion porometry and stomatal conductance calculated from infrared thermography in Arabidopsis. The differences in the observations may also be attributed to differences in the prevailing experimental conditions. Clearly, more work, using a combined approach of gas exchange measurements and diffusion porometry coupled with infrared thermography, is needed to assess the humidity responses of the abi mutants relative to the wild-type plants.
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Isolating novel mutants: Open Stomata 1 |
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TopAbstractIntroductionInfrared thermography: a non...Isolating novel mutants: Open...Isolating mutants using a...Concluding remarksReferences |
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By screening an M2 population of about 85 000 plants derived from ethyl methane sulphonate (EMS)-mutagenized wild-type Arabidopsis, Merlot et al. (2002) identified 85 candidates displaying a ‘cool’ mutant phenotype of which 75 were fertile. Of these, 44 retained the ‘cool’ phenotype in the M3 generation. Further analysis revealed that 82% of these mutants (36 out of 44) were ABA biosynthesis mutants while the remaining 8 were ABA-insensitive mutants. Using a CAPS assay described by Leung et al. (1997), Merlot et al. (2002) showed that three of the remaining ABA-insensitive mutants are identical to abi1-1. By crossing the remaining five mutants to wild-type plants, Merlot et al. (2002) showed that four of the mutations conferring the ‘cool’ phenotype were recessive and belonged to a single complementation group designated OST1 (Open Stomata 1), whereas one was dominant and was designated OST2. Further analyses revealed that the four recessive mutations correspond to two independent mutant alleles and were named ost1-1 and ost1-2. Figure 3A shows the effect of a 3 d drought stress on leaf temperatures of wild-type, abi1-1, ost1, and ost2 plants. It is evident that the abi1, ost1, and ost2 mutants all show a ‘cool’ phenotype relative to the wild-type controls. This ‘cool’ phenotype could be tied to aberrant stomatal function as epidermal peel bioassays indicated that stomata from ost1 and ost2 are insensitive to ABA (Fig. 3B). Interestingly, germination assays conducted in the presence of ABA showed that both ost1 and ost2 mutants displayed wild-type sensitivity (Fig. 3C), suggesting that these two genetic lesions affect only guard cell responses to ABA (Merlot et al., 2002).
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More recently, Mustilli et al. (2002) cloned OST1 and showed that it is an ABA-activated, Ca2+-independent protein kinase bearing a high level of sequence identity (79%) to AAPK, a guard cell-specific protein kinase that was isolated by Assmann and co-workers (Li and Assmann, 1996; Li et al., 2000). On the basis of similarities of OST1 and AAPK in terms of expression in guard cells and not mesophyll cells, ABA-activation and Ca2+-independence of kinase activity, and sensitivity of stomatal closure to ABA, it has been suggested that OST1 and AAPK are orthologous protein kinases (Assmann, 2003). However, it should be noted that whereas the ost1 mutation affected both ABA inhibition of stomatal opening and promotion of stomatal closure in Arabidopsis, the over-expression of a dominant-negative form of AAPK attenuated only ABA promotion of stomatal closure and not ABA inhibition of stomatal opening in Vicia faba (Li et al., 2000; Mustilli et al., 2002; Assmann, 2003). As highlighted by Mustilli et al. (2002) and Assmann (2003), it is unclear whether such a difference is (1) due to species differences in kinase function or (2) a result of the over-expression of a dominant-negative mutant in the case of AAPK and loss-of-function mutation in the case of ost1. Mustilli et al. (2002) also showed that in the ost1 mutants, ABA-induced ROS (reactive oxygen species) production is impaired. In addition, they showed that ABA-activation of OST1-kinase activity is impaired in the abi1-1 mutant. Together, these data suggest that OST1 acts between ABI1 and ROS production (Fig. 4). Recently, Assmann and co-workers (Li et al., 2002) identified an AAPK-Interacting Protein (AKIP1), a heterogeneous nuclear ribonucleoprotein (hnRNP)-like single-strand RNA binding protein and showed that ABA activation of AAPK led to the phosphorylation of AKIP1, increasing (1) its affinity for binding dehydrin mRNA and (2) partitioning into subnuclear bodies resembling nuclear speckles (Fig. 4). It will be of interest to identify AKIP1-like Arabidopsis RNA binding proteins as more in-depth experiments can be carried out in this genetically tractable model species to ascertain the role of OST1 and these putative proteins in ABA-regulation of RNA metabolism.
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Isolating mutants using a low-humidity screen |
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TopAbstractIntroductionInfrared thermography: a non...Isolating novel mutants: Open...Isolating mutants using a...Concluding remarksReferences |
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A similar approach has been adopted to that used by Merlot et al. (2002) for screening an EMS mutagenized population of Arabidopsis of the Columbia ecotype (kindly provided by Professor Ottoline Leyser, University of York, UK). However, instead of using a 3 d drought-stress treatment, plants were subjected to a low-humidity treatment by removing the lids of the propagators in which the plants were grown. During the screen, plants were left in the light with a PPFD of 150 µmol m–2 s–1 at 23±2 °C. It was estimated that the removal of the propagator lids resulted in a reduction in relative humidity from 60–70% to 30–40%. Approximately 50 000 M2 Arabidopsis plants were screened and two ‘cool’ mutants were isolated by simply visualizing differences in leaf temperatures as seen in the infrared image (Fig. 5). Differences in leaf temperatures were evident as early as 10 min following a change in humidity. Currently, a caps-based mapping approach is being used to identify the genetic lesions that are responsible for the ‘cool’ phenotypes. It is possible that the genetic lesion may have resulted in altered stomatal function. In addition, the genetic lesions may also have impacted on developmental programmes that ultimately affected the ability of the plant to regulate leaf temperatures. With this in mind, it would therefore be interesting to see if mutants with alterations in epicuticular wax deposition, for example, the eceriferum (cer) mutants (Jenks et al., 1995) also display different leaf temperatures compared with wild-type plants.
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Concluding remarks |
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TopAbstractIntroductionInfrared thermography: a non...Isolating novel mutants: Open...Isolating mutants using a...Concluding remarksReferences |
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The use of mutants has greatly advanced current understanding of stomatal guard cell function, in particular, ABA and drought signalling. Screening of mutants using a seed germination assay in the presence of ABA has proved to be extremely successful in the isolation of mutants affecting ABA signalling. However, this limits the isolation of genetic lesions that exert a pleiotropic effect on ABA signal transduction, missing out genetic lesions that affect only ABA signalling in the guard cells. Recently, Merlot et al. (2002) successfully employed infrared thermography as a non-invasive, high throughput technique for screening large populations of Arabidopsis mutants for plants that show differences in leaf temperatures due to aberrations in stomatal function. This screening method, based on visualizing differences in evaporative cooling following a 3 d drought stress, has enabled the identification of two genetic loci, OST1 and OST2. The ‘cool’ phenotype associated with these two genetic loci takes the form of ABA-insensitivity at the level of the stomata as ost1 and ost2 seeds show a wild-type sensitivity to ABA. This is important as it is further evidence in support of (1) certain elements of the signalling network functioning in a guard cell-specific manner and (2) infrared thermography as a useful complementary approach for screening novel mutants. A combined approach based on seed germination assays and infrared thermography will be a very powerful approach for the identification and isolation of novel guard cell function mutants. The authors’ experience with using low humidity suggests that this technique is not limited to screening for drought/ABA signalling mutants. The potential exists for using infrared thermography to screen for novel genetic lesions through modification of the external environment, for example, varying components of the gaseous environment like carbon dioxide and pollutants.
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Acknowledgements |
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We would like to thank the Biotechnology and Biological Sciences Research Council, UK (AMH) and University College Dublin (CKYN) for research funding.
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