Thermal imaging and carbon isotope composition indicate variation amongst strawberry (Fragaria × ananassa) cultivars in stomatal conductance and water use efficiency
Highlights
► Thermal imaging variables differed significantly between strawberry cultivars, indicating low gs in ‘Elsanta’ and ‘Totem’ and relatively high gs in well watered ‘Elvira’, ‘Florence’ and ‘Cambridge Favourite’. ► Optimisation of thermal imaging is important for effective screening. ► Validated thermal imaging for estimating stomatal conductance. ► Carbon isotope composition differed significantly between strawberry cultivars: in one experiment leaf δ13C indicated lowest WUE in ‘Elvira’ and highest WUE in ‘Totem’. ► Significant physiological variation in strawberry. ► But similar response to drought: lowering gs and hence increasing WUE.
Introduction
Worldwide, crop production is limited by drought more than by any other environmental stress (Cattivelli et al., 2008). For long-term sustainability, crops with greater water use efficiency (WUE) are required. Water use efficiency can be defined agronomically as the ratio between crop yield and water use, or physiologically as the ratio between photosynthesis and transpiration (Blum, 2005). High WUE, however, can be associated with reduced stomatal conductance (gs) and therefore reduced vigour and ultimately yield (Blum, 2005). The optimal cultivar for a particular environment might therefore show both high WUE and relatively high gs.
Stomatal conductance largely determines leaf transpirational water loss, and also influences photosynthetic assimilation and hence yields. It is therefore useful to screen genotypes for gs in programmes to improve yield or WUE (e.g. Gutierrez-Rodriguez et al., 2000). Infrared thermometry (and more particularly infrared thermal imaging) has opened up the possibility of remotely assessing the temperature of individual leaves (e.g. Tartachnyk and Blanke, 2008) or whole crop canopies (e.g. Berni et al., 2009). When stomata are open, transpiration cools a leaf, but when stomata are closed, transpirational cooling is no longer possible. On account of the relationship between canopy temperature and gs (Jones, 1992), infrared thermometry may be a useful tool for early-generation selection of physiologically superior lines in breeding programmes aiming to increase yield or reduce the impact of stressful environments (Reynolds et al., 1999, Lopes and Reynolds, 2010). The depression of canopy temperature compared to air temperature at solar noon, for example, has been correlated with yield and with gs of spring wheat (Amani et al., 1996). The use of indices relating the temperature of the canopy to that of reference surfaces (Jones, 1999), or estimation of gs from leaf energy balance equations (Leinonen et al., 2006, Guilioni et al., 2008), which take into account a range of environmental conditions other than air temperature, could greatly improve the application of thermometry in breeding programmes. To our knowledge these approaches have been confined to irrigation scheduling (e.g. Jones et al., 2002, Grant et al., 2007). Thermal imaging, as opposed to thermometry, allows the temperature of several plants to be compared within single images, which has the potential to dramatically increase the speed at which large numbers of genotypes are screened (Chaerle and Van Der Straeten, 2000). As a result, thermal imaging has been applied to screening for Arabidopsis mutants with altered transpiration in response to specific CO2 concentrations, relative humidity, and radiation (Merlot et al., 2002, Wang et al., 2004), but its potential in exploring the different phenotypes of diverse crop cultivars has not yet been fully exploited.
Photosynthesis is one of the primary processes to be affected by water stress (Chaves et al., 2009). During photosynthesis, the extent of discrimination against the naturally abundant and heaver isotope of carbon, 13C, is related to the ratio of internal to external partial pressure of CO2 (pi/pa), which is controlled by both stomatal conductance and photosynthetic capacity, and therefore is indirectly related to water use efficiency (Farquhar and Richards, 1984), with greater enrichment being associated with greater photosynthetic water use efficiency. The level of enrichment can be measured by determining the ratio of 13C and 12C and comparing the ratio to that of a standard, to determine the carbon isotope composition, δ13C. δ13C integrates the ratio of assimilation to transpiration over the duration in which dry matter is assimilated. Genetic differences in δ13C have been found within several species (Lambrides et al., 2004, de Souza et al., 2005, Peuke et al., 2006).
Despite the substantial interest in the use of δ13C for differentiating between genotypes, there is still uncertainty as to the best sampling strategy in terms of what plant tissue to sample, and under which environmental conditions. Internal partitioning and metabolism of primary assimilates may lead to different δ13C signatures for different plant organs (Farquhar et al., 1982), and notable differences between different tissues have been found in various species (de Souza et al., 2005, Hemming et al., 2005). δ13C is often increased when water availability is limited, as a result of stomatal closure and hence reduced transpiration, but this effect can depend on the plant tissue sampled (Peuke et al., 2006).
The shallow root system, large leaf area, and high water content of fruits of the commercial strawberry, Fragaria × ananassa Duch. mean that it uses large quantities of water (Klamkowski and Treder, 2006). Soil moisture deficits result in reduced gs and hence transpiration of strawberry plants (Klamkowski and Treder, 2006, Grant et al., 2010), but also in reduced vegetative growth, and for many cultivars in reduced yields (Savé et al., 1993, Grant et al., 2010, Li et al., 2010), even when the drought stress is relatively mild. Klamkowski and Treder (2008) and Grant et al. (2010) have shown substantial variation between cultivars in response to substrate water deficits. Given the increasing pressure on agriculture to optimise use of water, it is also of interest to determine variation amongst strawberry cultivars in water use efficiency. In strawberry, improving water use efficiency ultimately means increasing the ratio of saleable-quality fresh berries produced to unit of water consumed during production. Several factors impact on this ratio, one of them being the ratio between carbon fixed in photosynthesis and water lost via transpiration.
We hypothesised that variation exists amongst strawberry cultivars in leaf physiology, which could lead to improved water use efficiency or tolerance of water deficit. This hypothesis was tested using thermal imaging and δ13C analysis to assess stomatal conductance and water use efficiency of a range of F. × ananassa cultivars, both under well watered and water deficit conditions.
Section snippets
Plant material, experimental design, and irrigation scheduling
Bare root plants were acquired for ten June-bearing (short-day) cultivars of F. × ananassa Duch., as described previously (Grant et al., 2010): ‘Cambridge Favourite’, ‘Delia’, ‘Elsanta’, ‘Elvira’, ‘Emily’, ‘Florence’, ‘Hapil’, ‘Idea’, ‘Symphony’, and ‘Totem’. Two experiments were undertaken, one with plants growing in a polythene tunnel (‘polytunnel’) with no supplementary light or heating, and the other with plants growing in a controlled glasshouse containment facility (GroDome, Unigro,
Thermal imaging
No significant effect of irrigation was found on Tleaf when plants were left in situ, although there was a significant effect of cultivar (data not shown). In addition, when plants were grouped together, but no attempt was made to keep the selected leaves horizontal, there was no significant effect either of irrigation or cultivar on Tleaf, IG, CWSI, or gs estimated from leaf temperature. When the leaves were kept horizontal using a grid, however, Tleaf was significantly higher in water limited
Thermal imaging of strawberry cultivars
Leaf temperature is affected by the angle of the leaf towards light, i.e. how much energy to which it is exposed, as well as by stomatal conductance. When images were taken of plants in their ‘natural’ habit, either variation between individual plants in leaf angle had more influence than gs on the average leaf temperature in a treatment (Grant et al., 2006), or water limitation led to altered leaf angle, as has been noted for field-grown strawberry (Savé et al., 1993). Therefore it appears
Conclusions
Thermal imaging and δ13C analysis revealed substantial variation between strawberry cultivars in both gs and WUE. Thus the hypothesis that variation in leaf physiology exists between strawberry F. × ananassa cultivars, leading to variation in water use efficiency, can be accepted. On the other hand, results of the experiments reported here do not support the hypothesis that differences in leaf physiology lead to variation in tolerance of water deficit: water limitation reduced gs and thus
Acknowledgements
We gratefully acknowledge the assistance of the facilities team in EMR in crop husbandry. This research was funded by the Department for Environment, Food and Rural Affairs (Defra), UK, project WU0107, ‘Determination of the response of strawberry to water limited conditions, identification of quantitative trait loci (QTL) associated with water use efficiency (WUE) and development of molecular markers for use in a genetic improvement programme’.
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