Resource partitioning to male and female flowers of Spinacia oleracea L. in relation to whole-plant monocarpic senescence

Abstract

Male plants of spinach (Spinacea oleracea L.) senesce following flowering. It has been suggested that nutrient drain by male flowers is insufficient to trigger senescence. The partitioning of radiolabelled photosynthate between vegetative and reproductive tissue was compared in male (staminate) versus female (pistillate) plants. After the start of flowering staminate plants senesce 3 weeks earlier than pistillate plants. Soon after the start of flowering, staminate plants allocated several times as much photosynthate to flowering structures as did pistillate plants. The buds of staminate flowers with developing pollen had the greatest draw of photosynthate. When the staminate plants begin to show senescence 68% of fixed C was allocated to the staminate reproductive structures. In the pistillate plants, export to the developing fruits and young flowers remained near 10% until mid-reproductive development, when it increased to 40%, declining to 27% as the plants started to senesce. These differences were also present on a sink-mass corrected basis. Flowers on staminate spinach plants develop faster than pistillate flowers and have a greater draw of photosynthate than do pistillate flowers and fruits, although for a shorter period. Pistillate plants also produce more leaf area within the inflorescence to sustain the developing fruits. The (14)C in the staminate flowers declined due to respiration, especially during pollen maturation; no such loss occurred in pistillate reproductive structures. The partitioning to the reproductive structures correlates with the greater production of floral versus vegetative tissue in staminate plants and their more rapid senescence. As at senescence the leaves still had adequate carbohydrate, the resources are clearly phloem-transported compounds other than carbohydrates. The extent of the resource redistribution to reproductive structures and away from the development of new vegetative sinks, starting very early in the reproductive phase, is sufficient to account for the triggering of senescence in the rest of the plant.

Fig. 1.

Photographs of male (staminate, right) and female (pistillate left) spinach plants. The lower photograph shows spinach plants in the second week of the flowering period. The upper photograph shows the upper part of the inflorescence of plants in the fourth week of the flowering period.

Fig. 2.

Area of leaves of staminate (black bars) and pistillate plants (grey bars). (A) Area of leaves below the inflorescence; (B) area of leaves within the inflorescence. After week 5, the staminate plants have senesced. Bars represent ±SE.

Fig. 3.

Allocation of radiolabelled photosynthate to different structures from the leaf just below the inflorescence (L-1) to each importing structure at the onset of flowering, within a few days of flowers becoming visible on the plants. (A) As a percentage of total export; (B) relative specific activity (RSA), calculated on a per gram basis. The dpm g⁻¹ for each organ was divided by the average dpm g⁻¹ of all the importing organs in that plant. Labelling was for 1 h followed by a 3 h chase. Bars represent ±SE.

Fig. 4.

Allocation of radiolabelled photosynthate from the leaf just below the inflorescence (L–1), over time, from the start of flowering: (A, B) to the flowers or fruits; (C, D) to the leaves and stem below the inflorescence; (E, F) to the apical bud region. Week 1 represents the time 1 week after flowers were first visible on the plant, with subsequent samples occurring weekly afterwards. (A, C, E) As a percentage of total export; (B, D, F) relative specific activity (RSA), calculated on a per gram basis. The dpm g⁻¹ for each organ was divided by the average dpm g⁻¹ of all the importing organs in that plant. Labelling was for 1 h followed by a 3 h chase. Bars represent ±SE. By week 5, the staminate plants have senesced.

Fig. 5.

Allocation of radioactivity to various parts of staminate and pistillate plants at 3 weeks after the start of flowering and at various times following a 1 h exposure of L–1 to ¹⁴CO₂ followed by long chase times. (A) The flowers and fruits; (B) the leaves of the inflorescence region; C) the stem of the inflorescence. Bars represent ±SE.

Fig. 6.

Mass corrected (RSA) measure of radiolabelled photosynthate allocated to the reproductive structures of staminate and pistillate plants at 3 weeks after the start of flowering and at various times following a 1 h exposure of L–1 to ¹⁴CO₂ followed by long chase times. Bars represent ±SE.

Fig. 7.

Allocation of radiolabelled photosynthate from L–1 to different parts of staminate plants with the reproductive organs separated into flowers of different ages, 2 weeks after the start of flowering. (A) As a percentage of total export; (B) RSA. Labelling was for 1 h followed by a 3 h chase. Bars represent ±SE.

Fig. 8.

Allocation to organs of staminate and pistillate plants when the entire inflorescence was exposed to ¹⁴CO₂ for 1 h with a 4 h chase period. (A) 1 week after the start of flowering. (B) Plants two weeks after the start of flowering. Bars represent ±SE.

Fig. 9.

Photosynthetic rates of leaves of staminate and pistillate spinach plants measured at various times following the start of flowering. Measurements occurred at mid-morning with 175 μE m⁻² of light. (A) Leaves of staminate plants; (B) Leaves of pistillate plants. Bars represent ±SE.

Fig. 10.

Rates of respiration per segment (A, B) of 3.5 cm segments of the inflorescence, without leaves, and rates of respiration, per unit fresh weight, of the reproductive structures (C, D) from 3.5 cm segments within the inflorescence, both numbered downwards from the apex of the plant. (A, C) 2 weeks; (B, D) 4 weeks after the start of flowering. Respiration was determined by CO₂ evolution in darkness. Values in (C) and (D) were obtained by subtraction of the CO₂ evolution of stems alone from that of stems with reproductive structures, divided by the fresh weight of the reproductive structures. Bars represent ±SE.

Fig. 11.

Changes over time in the total non-structural carbohydrate content of staminate and pistillate plants. (A) Reproductive structures 15–18.5 cm below the tip of the inflorescence; (B) leaf L3 (third leaf, counting from the base, within the inflorescence). Bars represent ±SE.