Effects of Light Quality and Intensity on Diurnal Patterns and Rates of Photo-Assimilate Translocation and Transpiration in Tomato Leaves

Abstract

Translocation of assimilates is a fundamental process involving carbon and water balance affecting source/sink relationships. Diurnal patterns of CO₂ exchange, translocation (carbon export), and transpiration of an intact tomato source leaf were determined during ¹⁴CO₂ steady-state labeling under different wavelengths at three pre-set photosynthetic rates. Daily patterns showed that photosynthesis and export were supported by all wavelengths of light tested including orange and green. Export in the light, under all wavelengths was always higher than that at night. Export in the light varied from 65-83% of the total daily carbon fixed, depending on light intensity. Photosynthesis and export were highly correlated under all wavelengths (r = 0.90-0.96). Export as a percentage of photosynthesis (relative export) decreased as photosynthesis increased by increasing light intensity under all wavelengths. These data indicate an upper limit for export under all spectral conditions. Interestingly, only at the medium photosynthetic rate, relative export under the blue and the orange light-emitting diodes (LEDs) were higher than under white and red-white LEDs. Stomatal conductance, transpiration rates, and water-use-efficiency showed similar daily patterns under all wavelengths. Illuminating tomato leaves with different spectral quality resulted in similar carbon export rates, but stomatal conductance and transpiration rates varied due to wavelength specific control of stomatal function. Thus, we caution that the link between transpiration and C-export may be more complex than previously thought. In summary, these data indicate that orange and green LEDs, not simply the traditionally used red and blue LEDs, should be considered and tested when designing lighting systems for optimizing source leaf strength during plant production in controlled environment systems. In addition, knowledge related to the interplay between water and C-movement within a plant and how they are affected by environmental stimuli, is needed to develop a better understanding of source/sink relationships.

Keywords: carbon export; light quality; light-emitting diode (LED); photosynthesis; tomato; translocation; transpiration; water-use-efficiency (WUE).

FIGURE 1

Daily patterns of leaf net carbon exchange rate (NCER) and export at an initial high photosynthetic rate of ∼12 μmol m^-2 s^-1 as affected by different spectral qualities. The NCER (A–C), export (D–F), and relative export (export as a percentage of photosynthesis; G–I) exposed to mixed light-emitting diodes (LEDs), red-blue (RB), white (W), and red-white (RW) are shown in A,D,G. The NCER, export, and relative export from R and B are shown in B,E,H while O and G are shown in C,F,I respectively.

FIGURE 2

Daily patterns of leaf NCER and export at an initial medium photosynthetic rate of ∼8 μmol m^-2 s^-1 as affected by different spectral qualities. The NCER (A–C), export (D–F), and relative export (export as a percentage of photosynthesis; G–I) exposed to mixed LEDs system, RB, W, and RW are shown in A,D,G. The NCER, export, and relative export from R and B are shown in B,E,H while O and G are shown in C,F,I respectively.

FIGURE 3

Daily patterns of leaf NCER and export at an initial low photosynthetic rate of ∼4 μmol m^-2 s^-1 as affected by different spectral qualities. The NCER (A–C), export (D–F), and relative export (export as a percentage of photosynthesis; G–I) exposed to mixed LEDs system, RB, W, and RW are shown in A,D,G. The NCER, export, and relative export from R and B are shown in B,E,H while O and G are shown in C,F,I respectively.

FIGURE 4

A summary of carbon allocation at high (A), medium (B), and low (C) photosynthetic rates to day-time export, storage in the leaf at the end of the photoperiod, night-time export, night-time respiration, and storage in the leaf after 23 h pulse and chase experiment. Carbon allocation is expressed as a percentage of total carbon fixed during the photoperiod. A statistical difference (p < 0.05) in the percentage of day-time export between an LED treatment and the W LED control is indicated with an asterisk (^∗).

FIGURE 5

Total carbon fixed and exported during the photoperiod under low, medium, and high photosynthetic rates from leaves that were illuminated by various LED systems (A). B illustrates the relationship between export and photosynthesis during the day-time under different LED treatments. Relative export during the day-time was expressed as the percentage of the total fixed carbon.

FIGURE 6

Correlation analysis between hourly averages of carbon fixation and export under illumination with LEDs of different spectral qualities and intensities (A). B displays the correlation between the average export during the last hour of illumination and the soluble sugar in the leaf at the end of the illumination period. The solid black line (–) indicates the linear regression line within each dataset.

FIGURE 7

Diurnal patterns of stomatal conductance (A–C), transpiration rate (D–F), and WUE (G–I) of leaves during the light period under various wavelength specific LEDs. A,D,G show these values from export experiments done at an initial high photosynthetic level of ∼12 μmol m^-2 s^-1. Panels B,E,H show these values from export experiments done at an initial medium photosynthetic level of ∼8 μmol m^-2 s^-1. C,F,I show these values from export experiments done at an initial low photosynthetic level of ∼4 μmol m^-2 s^-1.

FIGURE 8

Potential sites of carbon and water regulation which can be affected by light intensity and quality within a tomato source leaf. ATP is produced via the light reactions through the movement of electrons between photosystem II (yellow triangle) and photosystem I (red triangle) allows for the conversion of CO₂ to triose phosphate via the Calvin cycle (1). Triose phosphate is then moved out of the chloroplast into the mesophyll cell (MC) via the anti-port mechanism of the triose phosphate/phosphate translocator (TPT; blue oval) where it is converted to sucrose (2; Stitt et al., 1987; Huber and Huber, 1990a; Walters et al., 2004). Triose phosphate can also be made into starch in a multiple step process. Starch, which is a storage molecule in tomatoes, can be broken down into either maltose or glucose and transported into the MC via a maltose excess1 transporter (MEXI; red circle) or glucose transporter (GUT; orange circle) respectively (3; Schleucher et al., 1998; Niittylä et al., 2004). Both maltose and glucose can then be converted to sucrose in the MC. Sucrose is then able to proceed via multiple pathways. Sucrose can enter the vacuole via an anti-port tonoplast membrane located H⁺/sucrose transporter (black oval) and conversely leave the vacuole via a tonoplast membrane located H⁺/sucrose symport (black rectangle) (4; Schulz et al., 2011; Etxeberria et al., 2012). Sucrose can also move into the apoplast via the ‘sugars will eventually be exported transporter’ (SWEET; red rectangle) directly from the MC or by first symplastically diffusing into the phloem parenchyma cell (PPC) (5; Chen et al., 2012; Feng et al., 2015). The mechanism of sucrose efflux via SWEET is currently speculated to be bidirectional uniport, however lacks concrete evidence (Chen et al., 2015). Once in the apoplast, sucrose enters the phloem directly or the transfer cell (TC) then enters the phloem symplastically. Entering the phloem directly or the TC is catalyzed by a co-transport H⁺/sucrose transporter (SUT; orange oval) (6; Riesmeier et al., 1992). ATPase enzymes (dark blue circle) are responsible for maintaining H⁺ gradients across membranes and are usually found close to enzymes using H⁺ symport or anti-port mechanism (7). The movement of water between the xylem and phloem has also been proposed to affect carbon export rates (8; Smith and Milburn, 1980; Windt et al., 2006; De Swaef et al., 2013; Nikinmaa et al., 2013).