Nighttime Stomatal Conductance and Transpiration in C3 and C4 Plants
Year: 2007
Type: review
Abstract: Histogram summarizing reported g night in species among different plant functional groups. For each species, g night was averaged from all reported values with units in mol m−2 s−1 presented in Supplemental Table S1 and thus represents a mixture of field and greenhouse studies. The black two-headed arrow at the top left of the graph represents the range for reported g cuticular taken from many species, and reported g night within this range may be largely due to g cuticular rather than g stomatal. A complete listing of species with references is provided in Supplemental Table S1. The magnitude of water loss occurring during the night depends on both g night and the vapor pressure difference (VPD) between leaves and the air, as well as canopy structure and atmospheric mixing. While g night has been recorded at up to 90% of daytime conductance, nighttime VPD is typically much lower than daytime. Thus, nighttime transpiration rates (E night) are typically 5% to 15% of daytime rates, although sometimes as high as 30%, based on gas exchange measurements of individual leaves, whole-plant sap flow, and field scale lysimetry (Benyon, 1999; Snyder et al., 2003; Bucci et al., 2004, 2005; Daley and Phillips, 2006; Scholz et al., 2007). While some methods are more accurate and/or have less uncertainty than others, a few studies have compared methods, generally finding agreement even across measurement scales (e.g. leaf versus whole plant; Green et al., 1989). Drawbacks for each method must be recognized, particularly when comparing species or environments. For example, leaf-level gas exchange typically includes cuticular as well as stomatal components of leaf conductance to water vapor, while sap flow methods typically have attendant uncertainties as to the proportion of the measured flux resulting in bole refilling rather than transpiration from the canopy. Nevertheless, there is broad agreement among the methods and scales that stomata of many species remain partially open during the night. Measurements of minimum leaf conductance induced by ABA application and by drying excised leaves to wilting have been used to separate stomatal (g stomatal) and cuticular (g cuticular) conductance (Rawson and Clarke, 1988; Howard and Donovan, 2007). Conductance measured at maximal stomatal closure can be functionally defined as g cuticular because it is not under guard cell regulation. For a few species, this would include the effect of dust or stomatal plugs that prevent complete closure (Feild et al., 1998). In general, g cuticular estimates range from 0.004 to 0.020 mol m−2 s−1 (Rawson and Clarke, 1988; Nobel, 1991; Kerstiens, 1995; Boyer et al., 1997; Burghardt and Riederer, 2003; Howard and Donovan, 2007), far lower than most estimates of g night (Fig. 1; Supplemental Table S1). Thus, most reported values of g night are largely influenced by g stomatal. Diagram summarizing sources of variation (internal and external) affecting g night and transpiration (E night), and consequences of g night and E night at the individual plant and larger scales. Species in which g night has been documented include a diverse range of genera and life forms (annuals and perennials; monocots, herbaceous dicots, shrubs, and trees; Fig. 1; Supplemental Table S1) native to a diversity of habitats: e.g. wetland (Loftfield, 1921), desert (Donovan et al., 2003; Snyder et al., 2003; Ludwig et al., 2006), neotropical savanna (Bucci et al., 2004, 2005; Domec et al., 2006; Scholz et al., 2007), temperate deciduous and evergreen forests (Benyon, 1999; Oren et al., 2001; Barbour et al., 2005; Daley and Phillips, 2006; Kavanagh et al., 2007), and subalpine forest (Herzog et al., 1998). Many horticultural and crop species have substantial g night and/or E night (England, 1963; Rosenberg, 1969; Rawson and Clarke, 1988; Green et al., 1989; Blom-Zandstra et al., 1995; Assaf and Zieslin, 1996; Musselman and Minnick, 2000). Although it has been suggested that sustained nocturnal stomatal opening is not a feature of grasses (Loftfield, 1921), substantial g night has been observed in Distichlis spicata (C4; Snyder et al., 2003) and wheat (Triticum aestivum; C3; Rawson and Clarke, 1988), among others. Substantial variation in magnitude of maximum g night has been observed among closely related species (Supplemental Table S1); however, differences among some species are minimal and not biologically significant (see Helianthus species, Supplemental Table S1; Howard and Donovan, 2007). Multiple surveys have shown that g night varies substantially among species within a particular environment or habitat type (Snyder et al., 2003; Bucci et al., 2004; Daley and Phillips, 2006; Kavanagh et al., 2007), and the relationship of species differences to source environment or habitat remains unclear. Additional studies investigating g night in a phylogenetic context in native and common garden locations will be required to determine whether species differences in g night are adaptive. Many studies have also demonstrated genetic variation in magnitude of g night among cultivars or accessions of single species (Supplemental Table S1). Arabidopsis (Arabidopsis thaliana) natural accessions had a 2.5-fold variation in magnitude of g night when grown in a common environment, and the variation was correlated to mean annual VPD of the accessions native environment (M. Caird, unpublished data). Although correlative, this relationship suggests the potential for natural selection to have operated on g night. In addition to genetic variation, there is also evidence for separate genetic control of g night from g day. Three near-isogenic lines of Arabidopsis differed from their parental lines in either g night or g day, but not both, providing evidence that these two traits can be regulated independently due to genetic factors alone (M. Caird, unpublished data). Future studies exploiting natural and mutant genotypes will likely play an important role in discovering the genetic factors that influence g night in plants. Although recent studies of nighttime water loss generally do not consider differences in stomatal density or adaxial and abaxial surface responses, these factors may contribute to within and among species variation in g night. Not only does stomatal density often differ between adaxial and abaxial leaf surfaces, but the stomata on these surfaces can respond differently to environmental cues such as light. Stomata on the abaxial leaf surface, but not the adaxial surface, remained open at night in cotton (Gossypium hirsutum; Sharpe, 1973) and fava bean (Vicia faba; Aben et al., 1989). Future studies need to consider how these factors may affect g night and E night, particularly with regard to between and within species variation in g night. For many species, g night is not stable throughout the night period. Endogenous, gradual increases in stomatal opening during predawn hours have been reported in many species under natural field conditions as well as in controlled environments (Schwabe, 1952; Muchow et al., 1980; Anderson, 1982; Lasceve et al., 1997; Leymarie et al., 1998, 1999; Donovan et al., 2003; Bucci et al., 2004; Dodd et al., 2005; Howard and Donovan, 2007). In Arabidopsis accession Columbia, a mean minimum g night of 0.117 mol m−2 s−1 slowly increased to a predawn mean of 0.161 mol m−2 s−1, amounting to a 38% increase in g stomatal during the night (Lasceve et al., 1997). Arabidopsis mutants with disrupted circadian rhythms do not have increased stomatal opening in predawn hours, indicating g night has some component of circadian regulation (Dodd et al., 2004, 2005). Lasceve et al. (1997) also found starch-deficient Arabidopsis mutants do not have the increased endogenous predawn opening observed in wild-type plants, implying that starch metabolism, possibly through the formation of an osmoticant necessary for guard cell osmoregulation, is an important factor affecting stomatal opening during predawn. Photoperiod length and light intensity can affect the speed and degree to which stomata close in the dark. Incomplete stomatal closure at night resulted from short-day as opposed to long-day photoperiods in Chrysanthemum (Schwabe, 1952). Higher light intensity during the day or longer supplementary lighting intervals (extending light period into the normal night) resulted in faster stomatal closure responses to lights turning off in roses, although closure was still incomplete (Blom-Zandstra et al., 1995). The spectrum of the low intensity supplementary light (25 μmol m−2 s−1) also affected g night, with orange and blue supplementary light preventing complete stomatal closure 2.5 h into the night, while white and no (control) supplementary light resulted in g night comparable to previously determined g cuticular (0.01 mol m−2 s−1; Blom-Zandstra et al., 1995). This evidence, together with evidence of starch-deficient Arabidopsis mutants having decreased nighttime stomatal opening (Lasceve et al., 1997), suggests that daytime conditions and photosynthetic rates can influence g night. Although the exact mechanism is unclear, it is possible that a byproduct of starch metabolism may affect guard cell osmoregulation at night (Lasceve et al., 1997), causing greater stomatal opening when starch levels are high. Positive correlations have been observed for g night and g day among species in Great Basin habitats (Snyder et al., 2003). Although only correlative data are available, the relationship may be the result of daytime conditions that allow high photosynthetic rates but also result in high g night. Alternatively, leaf development and stomatal anatomy that affect g day could be a cause for correlation with g night. Atmospheric conditions can be important in driving E night when stomata are open, as evidenced by canopy scale measurements of crop water loss on weighing lysimeters (England, 1963; Rosenberg, 1969). Advection was found to create sufficient evaporative demand to cause 20% to 30% of total daily transpiration to occur at night in alfalfa (Medicago sativa) in the field (Abdel-Aziz et al., 1964) and kiwifruit (Actinidia deliciosa) in orchards (Green et al., 1989). Seginer (1984) extended this concept to show energy requirements and conditions in greenhouses under which E night occurs in roses using a modified version of the Penman model. In natural systems, increased VPD has been correlated with greater E night at the scale of sap flux for many tree species (Herzog et al., 1998; Benyon, 1999; Oren et al., 2001; Daley and Phillips, 2006; Kavanagh et al., 2007). A trend for lower g night with increasing VPD has been observed in some species (Muchow et al., 1980; Oren et al., 2001; Bucci et al., 2004), yet some data indicate lack of any response (Barbour et al., 2005). However, correlative studies such as these do not control for possible variation due to inherent circadian regulated stomatal opening that might parallel decreasing VPD during the night. Nevertheless, similar correlations have been found when nighttime VPD around plants is experimentally manipulated, providing more direct evidence that some species do close stomata in response to higher VPD during the night just as during the daytime (Bakker, 1991). A more thorough understanding of whether VPD regulates g night in a manner parallel to that of g day will require more studies that manipulate VPD while controlling for other potentially confounding factors, including circadian rhythms. It is expected that at night stomata will be sensitive to decreased water availability, just as during the daytime, to conserve water. Lower g night has been associated with decreased plant water status in Hibiscus cannabinus (Muchow et al., 1980), Pseudostuga menziesii (Running, 1976; Blake and Ferrell, 1977), and Helianthus anomalus (Ludwig et al., 2006). In a field experiment, g night of unirrigated desert shrubs was lower than that of shrubs receiving surface irrigation (Donovan et al., 2003). In greenhouse studies, g night decreased in response to a water stress treatment in wheat (Rawson and Clarke, 1988) and in Helianthus species (Howard and Donovan, 2007). Similar to drought, increased salinity also reduced g night in desert shrubs (Donovan et al., 1999). The magnitude of g night can additionally vary seasonally. For Chrysothamnus nauseosus, g night was reduced at the end of growing season when soils were dry, while the cooccurring Sarcobatus vermiculatus had higher g night (relative to g day) by the end of the season (Donovan et al., 2003). The Sarcobatus response may be related to its capacity to accumulate high concentrations of leaf apoplastic solutes (James et al., 2006), which could in turn affect stomatal regulation. Seasonal changes in g night were also found for Pinus ponderosa, with stomata more open during the night in early summer, like Chrysothamnus (Grulke et al., 2004). ABA can induce stomatal closure during the dark (Rawson and Clarke, 1988; Howard and Donovan, 2007). Similar to responses observed during the daytime, increased concentrations of exogenous ABA resulted in greater stomatal closure at night in Arabidopsis, and stomatal closure in response to ABA was more prominent at higher CO2 (Leymarie et al., 1998, 1999). In P. menziesii seedlings, nighttime leaf resistance was sensitive to the ABA content of leaves (Blake and Ferrell, 1977), indicating ABA induced stomatal closure in response to water stress at night just as during the daytime. Typically, higher nutrient availability, particularly nitrogen (N), is correlated with higher daytime photosynthesis (Lambers et al., 1998). However, varying results have been found for correlations of nutrient supply and g day (Meinzer et al., 1988; Toft et al., 1989). Similarly, species show different responses of g night to limited nutrient supply. In two field studies with nutrient treatments, high nutrient plants had lower g night, but the experimental designs do not allow unambiguous separation of direct effects due to reduced plant demand for nutrient acquisition regulating g night from indirect effects of plant size or water status (Ludwig et al., 2006; Scholz et al., 2007). Other nutrient response experiments that controlled for plant water status have found differing effects of N supply on g night. For example, reduced g night was observed in N-limited Arabidopsis, but higher g night was found in N-limited D. spicata and Populus balsamifera subsp. trichocarpa (M. Caird and A. Howard, unpublished data). Still other species showed no g night response to soil nutrient limitations (Helianthus species; Howard and Donovan, 2007). The relationship between varying g night responses to nutrients and particular life forms or ecological strategies is unknown and may be related to the underlying causes of nutrient status effects on g day. The occurrence of high g night in many C3 and C4 plant species has important implications for air pollutant uptake (Goknur and Tibbitts, 1984; Segschneider et al., 1995; Musselman and Minnick, 2000; Takahashi et al., 2005). g stomatal is a major factor affecting ozone (O3) uptake in plants (Wieser and Havranek, 1993). Tree species in areas with high levels of O3 exposure can have stomata open at night (Wieser and Havranek, 1993; Matyssek et al., 1995), and nocturnal O3 uptake can be a significant proportion of daily O3 uptake (up to 9%; Grulke et al., 2004). Stomatal responsiveness may be reduced after exposure to O3 (Keller and Hasler, 1984; Skarby et al., 1987). Whole-plant production and carbon allocation in Betula pendula were also more sensitive to nighttime compared to daytime O3 exposure (Matyssek et al., 1995). Thus, O3 damage resulting from nighttime uptake may be an important factor for plants. However, g night may also prove to be useful in areas of high air pollution. For example, H. cannabinus may be useful as a phytoremediator of NO2 because this species has high g night and g day (Takahashi et al., 2005). Nighttime stomatal opening may influence oxygen isotope signatures of within-canopy CO2 (Barbour et al., 2005). This has important implications for models describing ecosystem respiratory CO2 flux and its partitioning into above- and below-ground components. 18O enrichment of leaves will also be affected by g night, complicating the use of such signatures in detecting genetic or environmental effects on transpiration rate. Variation in magnitude of g night among species and the regulation and responses of g night to environmental factors (i.e. VPD) are important considerations in determining how large an impact nighttime stomatal opening will have on oxygen isotope signatures. More research on these topics is required and will need to be incorporated into models. Plants may be able to increase their photosynthetic carbon gain by preopening stomata before dawn. This might be especially advantageous in water-limited environments because of a higher potential for early morning carbon gain when temperatures and VPD are lower. Although stomatal responses to light are typically fast, there is some evidence to support the hypothesis that maintaining open stomata at night affects daytime opening. In Xanthium pennsylvanicum, the rate of stomatal opening in light was greater when stomata were open during the night (Mansfield and Heath, 1961). However, there is no evidence for an effect of experimentally lowering g night on carbon gain or g day during the subsequent day. Additional research is necessary to directly test whether high g night influences early morning and total daily carbon gain, and if so how much and by what mechanism. Plant water potential is expected to equilibrate with the wettest soil layer in the rooting zone overnight. However, substantial E night can prevent equilibration from occurring, resulting in soil-plant predawn water potential disequilibrium, or predawn disequilibrium (Donovan et al., 2001), which complicates interpretation of soil moisture availability based on plant water potential measurements. E night has been observed to contribute to predawn disequilibrium in many species (Donovan et al., 1999, 2001, 2003; Sellin, 1999; Bucci et al., 2004, 2005; Kavanagh et al., 2007). Substantial E night may additionally reduce a plant's ability to conduct hydraulic redistribution (HR, also referred to as hydraulic lift; Richards and Caldwell, 1987). HR occurs when some roots are absorbing water from wet soil locations and other roots of the same plant are losing water to relatively dry soil locations. When stomata are open and the atmospheric conditions allow E night to occur, the water loss through the shoot should decrease the amount released to drier soil layers because of impacts on plant water potentials. Plants in natural populations can simultaneously have both HR and high E night, although these two processes may vary in magnitude through the growing season (Donovan et al., 2003; Domec et al., 2006). Significant water loss without simultaneous photosynthetic carbon gain could constitute a major cost to a plant. However, it is possible that E night may provide a benefit that outweighs this cost. Mobile mineral nutrients are moved into the immediate of plant roots (i.e. the by flow of the soil 1995). Thus, the of a water through the plant during both day and night could potentially result in nutrient availability to the plant. et al. showed that stomatal closure reduced transpiration and N acquisition by Populus the the effect of increased water flux on uptake and nutrient in the rooting zone can be and The result is that increasing water flux or the which in the by maintaining a supply of to the and 1995). However, under low or high length density the effect is reduced and total uptake is not affected are experimentally this In addition to supply of nutrients to the of nutrients within plants, particularly nutrients such as depends on the flow rate and of transpiration 1995). increase in the total amount of water through the may when are Daley and also that g night may nutrient within such as by providing oxygen to that in nutrient and for plant water and nutrient that E night may also impact plant and although experimental evidence on the is It is that E night to plants under conditions as evidenced by in g night in response to water However, more research is necessary to determine what if may either or these Although research to the stomata of many C3 and C4 plant species as during the night, is this have a growing of evidence that g night is in many similar to daytime stomatal and that nighttime stomatal opening and transpiration have implications for plant and Nevertheless, more research will be necessary to the of g night and E night. Future research on plant regulation of g night and the consequences of substantial E night for water and nutrient will be for understanding the ecological and consequences of g night and E night in C3 and C4 plants. The are in the version of this Supplemental Table S1. A of C3 and C4 plant species reported in the as having significant g night and/or nighttime water loss or incomplete stomatal closure at night.
Source: PLANT PHYSIOLOGY
Institutions: University of Georgia, University of California, Davis
Language: English
Subfield: Global and Planetary Change
Field: Environmental Science
Domain: Physical Sciences
Open Access status: green
OpenAlex ID: W2015633635