Source-sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum

Abstract

Spring geophytes produce larger storage organs and present delayed leaf senescence under lower growth temperature. Bulb and leaf carbon metabolism were investigated in Erythronium americanum to identify some of the mechanisms that permit this improved growth at low temperature. Plants were grown under three day/night temperature regimes: 18/14 °C, 12/8 °C, and 8/6 °C. Starch accumulated more slowly in the bulb at lower temperatures probably due to the combination of lower net photosynthetic rate and activation of a 'futile cycle' of sucrose synthesis and degradation. Furthermore, bulb cell maturation was delayed at lower temperatures, potentially due to the delayed activation of sucrose synthase leading to a greater sink capacity. Faster starch accumulation and the smaller sink capacity that developed at higher temperatures led to early starch saturation of the bulb. Thereafter, soluble sugars started to accumulate in both leaf and bulb, most probably inducing decreases in fructose-1,6-bisphosphatase activity, triose-phosphate utilization in the leaf, and the induction of leaf senescence. Longer leaf life span and larger bulbs at lower temperature appear to be due to an improved equilibrium between carbon fixation capacity and sink strength, thereby allowing the plant to sustain growth for a longer period of time before feedback inhibition induces leaf senescence.

Fig. 1.

Representative illustration of Erythronium americanum plants during the different phenological stages of epigeous growth. (This figure is available in colour at JXB online.)

Fig. 2.

Evolution of bulb mass (A), root mass (B), leaf mass (C), and leaf area (D) throughout the epigeous growth period in E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). The first data points correspond to the time when leaves were completely unfolded. The penultimate data points correspond to the first visual signs of leaf senescence and the last data points correspond to complete leaf senescence. The data points identified 1, 2, and 3 on each curve are the lower and upper thresholds used to estimate two different growth rates (see Table 1) during bulb growth. The means ±SE (n=2; six plants per growing season) are presented.

Fig. 3.

Evolution of net photosynthetic rate (A, D), stomatal conductance (B, E), and intercellular CO₂ concentration (C, F) in E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). Gas exchange data (mean ±SE) were recorded at both 400 μmol m⁻² s⁻¹ (A, B, C) and at 1000 μmol m⁻² s⁻¹ (D, E, F) (n=2; five plants per growing season). Triangles indicate, for each temperature, the date to which A–Ci curves were carried out.

Fig. 4.

Evolution of leaf respiratory (A) and photorespiratory rate (B) over time in E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). Photorespiratory rates were estimated from measures taken at 400 μmol m⁻² s⁻¹. The means ±SE (n=2; five plants per growing season) are presented.

Fig. 5.

Evolution of photochemical quenching (A), non-photochemical quenching (B), PSII maximum efficiency (C), and electron flux across PSII (D) over time in E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). Fluorescence data (mean ±SE) were recorded at 400 μmol m⁻² s⁻¹ (n=2; five plants per growing season).

Fig. 6.

Evolution of starch (A), sucrose (B, E, G), reducing sugar concentrations (C, F, H), and fraction of amylose (D) over time in the bulb (A–F) and leaf (G, H) of E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). Concentration of sucrose and reducing sugars are presented as a function of total bulb biomass (mg g⁻¹; B, C) and as a function of bulb biomass other than starch (mg g⁻¹ DW-Starch; E, F). The means ±SE of three plants are presented.

Fig. 7.

Evolution of leaf (A) and bulb (B) protein concentration over time in E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). The means ±SE of three plants are presented.

Fig. 8.

Activities of fructose-1,6-bisphosphatase (A) in the leaf and of ADP-glucose pyrophosphorylase (B), sucrose synthase (C), cell wall invertase (D), neutral invertase (E), vacuolar invertase (F), and sucrose phosphate synthase (G) throughout the growth period in the bulb of E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). The means ±SE of three plants are presented.

Fig. 9.

Evolution of bulb cell size in E. americanum plants grown at 18/14 °C (black), 12/8 °C (grey), and 8/6 °C (white). The means ±SE of three plants are presented.