Sucrose feeding reverses shade-induced kernel losses in maize

Abstract

Background and aims: Water limitations can inhibit photosynthesis and change gene expression in ways that diminish or prevent reproductive development in plants. Sucrose fed to the plants can reverse the effects. To test whether the reversal acts generally by replacing the losses from photosynthesis, sucrose was fed to the stems of shaded maize plants (Zea mays) during reproductive development.

Methods: Shading was adjusted to mimic the inhibition of photosynthesis around the time of pollination in water-limited plants. Glucose and starch were imaged and quantified in the female florets. Sucrose was infused into the stems to vary the sugar flux to the ovaries.

Key results: Ovaries normally grew rapidly and contained large amounts of glucose and starch, with a glucose gradient favouring glucose movement into the developing ovary. Shade inhibited photosynthesis and diminished ovary and kernel size, weight, and glucose and starch contents compared with controls. The glucose gradient became small. Sucrose fed to the stem reversed these losses, and kernels were as large as the controls.

Conclusions: Despite similar inhibition of photosynthesis, the depletion of ovary glucose and starch was not as severe in shade as during a comparable water deficit. Ovary abortion prevalent during water deficits did not occur in the shade. It is suggested that this difference may have been caused by more translocation in shade than during the water deficit, which prevented low sugar contents necessary to trigger an up-regulation of senescence genes known to be involved in abortion. Nevertheless, sucrose feeding reversed kernel size losses and it is concluded that feeding acted generally to replace diminished photosynthetic activity.

Fig. 1.

Schedule of shading and stem infusion of sucrose. To reproduce the photosynthesis rates at low water potential observed by Zinselmeier et al. (1995a) and McLaughlin and Boyer (2004a), plants were shaded, as shown in (A). To overcome the loss in photosynthetic products because of shading, stems of some of the shaded plants were infused with photosynthetic quantities of sucrose each day, as shown in (B). The black bar on the x-axis indicates the duration of shading. Data in (B) are means ± s.e. for 4–13 plants.

Fig. 2.

(A) Net photosynthesis, (B) leaf water potential, (C) water usage and (D) ovary dry mass at various times when shade was imposed around pollination, as in Fig. 1A. Large open triangles (▵) in (A) show net photosynthesis observed by McLaughlin and Boyer (2004a) in controls and at low leaf water potentials. Open circles (○) indicate the control at high irradiance in the present study; closed circles (•) indicate shade; closed squares (▪) indicate shade plus sucrose infused into stems, as in Fig. 1B. Data are means ± s.e. for 4–8 plants. The s.e. is sometimes small enough to be obscured by data points.

Fig. 3.

In vivo starch location (A–K) and amount (L) in maize florets at various times when shade was imposed around pollination, as in Fig. 1A. Control: (A–D) Ovary on days –5, –2, 0 and 2, respectively. Starch is abundant in pedicel below spherical nucellus in ovary. Shade + sucrose infusion: (E–G) same as (B–D) except shade was started on day –2 and removed on day 2 while stems were fed sucrose solution as in Fig. 1B. Starch is partially maintained. Shade: (H–K) same as (E–G) but without sucrose feeding. Starch becomes depleted. Scale bar (applies to all micrographs) = 1 mm. (L) Starch contents of ovaries in micrographs. Open circles (○) are control at high irradiance; closed squares (▪), shade plus sucrose infused into stems; closed circles (•), shade. The black bar on the x-axis shows time when shade was present and sucrose was fed. Data are means ± s.e. for 4–6 plants.

Fig. 4.

In vivo glucose location (A–K) and amount of reducing sugars (L) in maize florets at various times when shade was imposed around pollination, as in Fig. 1A. Epi-fluorescence micrographs of ovary glucose (upper-case letters) are paired with UV autofluorescence images underneath to show ovary anatomy (lower-case letters). Control: (A–D) ovary on days –5, –2, 0 and 2, respectively. Note the autofluorescing vascular tissue in (a–d) below the nucellus. Glucose (red) is abundant around the vascular termini below the nucellus and increases as the ovary develops. Shade + Sucrose infusion: (E–G) same as (B–D) except shade was started on day –2 and removed on day 2 while stems were fed sucrose solution as in Fig. 1B. Glucose appears nearly as abundant as in controls. Shade: (H–K) same as (E–G) but without sucrose feeding. Less glucose accumulates than in controls. Scale bar (applies to all micrographs) = 1 mm. (L) Reducing sugar contents of ovaries in the micrographs. Open circles (○) = control at high irradiance; closed squares (▪), shade plus sucrose infused into stems; closed circles (•), shade. The black bar on the x-axis shows the time when shade was present and sucrose was fed. Data are means ± s.e. for 4–6 plants.

Fig. 5.

Ovary development (A–C) and dry mass (D) 10 d after pollination, when shade was imposed around pollination in maize plants as in Fig. 1A. (A) Unshaded controls, (B) shade plus sucrose infused into the stems, as in Fig. 1B, and (C) shade. Scale bar (applies to all micrographs) = 1 mm. Data in (D) are means ± s.e. for 4–7 plants.

Fig. 6.

(A) Ear development, (B) kernel weight and (C) kernel number at maturity when shade was imposed around pollination in maize plants as in Fig. 1A. Unshaded controls, shade plus sucrose infused into the stems, and shade treatments as indicated. Data are means ± s.e. for 4 plants. Scale bar = 5 cm.

Fig. 7.

Comparison of starch content of maize ovaries when plants were shaded (A) or unwatered (B, low Ψ_w) to cause the same inhibition of net photosynthesis around the time of pollination, as shown in Fig. 2A. Data in (A) are from the present study and in (B) from Zinselmeier et al. (1999). Open circles (○) = control at high irradiance or adequate water; closed squares (▪), shade or water deficit plus sucrose infused into stems; closed circles (•), shade or water deficit. The black bar on the x-axis in (A) shows time when shade was present and sucrose was fed. The black bar on the x-axis in (B) shows the time water was withheld, and the white bar shows the time sucrose was fed. Data are means ± s.e. for 4–6 plants.

Fig. 8.

Comparison of sugar contents of maize ovaries when plants were shaded (A) or unwatered (B, low Ψ_w) to cause the same inhibition of net photosynthesis around the time of pollination, as shown in Fig. 2A. Data in (A) are for reducing sugars from the present study and in (B) are for glucose from McLaughlin and Boyer (2004a). Open circles (○) = control at high irradiance or adequate water; closed squares (▪), shade or water deficit plus sucrose infused into stems; closed circles (•), shade or water deficit. The black bar on the x-axis in (A) shows time when shade was present and sucrose was fed. The black bar on the x-axis in (B) shows the time water was withheld, and the white bar shows the time sucrose was fed. Data are means ± s.e. for 4–6 plants in (A) and 3 plants in (B).

Fig. 9.

Translocation in maize during a prolonged water deficit beginning 10 d after pollination. (A) Translocation 7 d later and (B) 21 d later in the same plants. Open circles (○) = controls supplied with water; closed circles (•), water withheld. The experiment exposed an upper leaf to ¹⁴CO₂ and detected percentage of applied label arriving in the grain 24 h later. Plants were grown in the field at leaf water potentials similar to those in the present work. Data are from Jurgens et al. (1978) and were significantly different at the 5 % level for water deficit and at the 1 % level for harvest date.