Compartmentation of sucrose during radial transfer in mature sorghum culm

Abstract

Background: The sucrose that accumulates in the culm of sorghum (Sorghum bicolor (L.) Moench) and other large tropical andropogonoid grasses can be of commercial value, and can buffer assimilate supply during development. Previous study conducted with intact plants showed that sucrose can be radially transferred to the intracellular compartment of mature ripening sorghum internode without being hydrolysed. In this study, culm-infused radiolabelled sucrose was traced between cellular compartments and among related metabolites to determine if the compartmental path of sucrose during radial transfer in culm tissue was symplasmic or included an apoplasmic step. This transfer path was evaluated for elongating and ripening culm tissue of intact plants of two semidwarf grain sorghums. The metabolic path in elongating internode tissue was also evaluated.

Results: On the day after culm infusion of the tracer sucrose, the specific radioactivity of sucrose recovered from the intracellular compartment of growing axillary-branch tissue was greater (nearly twice) than that in the free space, indicating that sucrose was preferentially transferred through symplasmic routes. In contrast, the sucrose specific radioactivity in the intracellular compartment of the mature (ripening) culm tissue was probably less (about 3/4's) than that in free space indicating that sucrose was preferentially transferred through routes that included an apoplasmic step. In growing internodes of the axillary branch of sorghum, the tritium label initially provided in the fructose moiety of sucrose molecules was largely (81%) recovered in the fructose moiety, indicating that a large portion of sucrose molecules is not hydrolysed and resynthesized during radial transfer.

Conclusion: During radial transfer of sucrose in ripening internodes of intact sorghum plants, much of the sucrose is transferred intact (without hydrolysis and resynthesis) and primarily through a path that includes an apoplasmic step. In contrast, much of the sucrose is transferred through a symplasmic path in growing internode (axillary branch) tissue. These results contrast with the probable symplasmic path in mature culm of the closely related species, sugarcane. Phylogenetic variability exists in the compartmental path of radial transfer of sucrose in culms of the andropogonoid grasses.

Figure 1

Soluble sugars of free-space and intracellular compartment in elongating and ripening internode of sorghum. The contents of glucose (G), fructose (F) and sucrose (S), expressed on a weight per tissue weight basis, of the free space (left subpanel) and the intracellular compartment (right subpanel) of elongating internode tissue from axillary branches at or before anthesis (left panel) and of mature ripening internode tissue of the main culm (right panel) of sorghum. The results from two cultivars of sorghum are combined. The error bars are 95% confidence intervals.

Figure 2

Ratio of the ¹⁴C-sucrose specific radioactivity of the intracellular compartment relative to free space. The ratio of the ¹⁴C-sucrose specific radioactivity of the intracellular compartment relative to the free space of elongating internode tissue from axillary branches at or before anthesis (left panel) and of ripening internode tissue of the main culm (right panel) of sorghum. Radiolabeled sucrose had been introduced into intact plants via culm infusion about 24 h previously. The reference line is at a ratio of 1.0. The results from two sorghum cultivars are combined. The error bars are 95% confidence intervals.

Figure 3

Proportion of radioactivity in fructose moiety of sucrose recovered from intracellular compartment of internode tissue. The proportion of ¹⁴C (left panel) and ³H (right panel) in the fructose moiety relative to the combined fructose and glucose moieties of sucrose recovered from the intracellular compartment of internode tissue. Tissue was sampled from unperturbed internode tissue of sorghum plants into which uniformly labelled ¹⁴C-sucrose and asymmetrically labelled (all of the label in the fructose moiety) ³H-sucrose had been simultaneously infused about 24 h before. The proportions are provided for tissue from axillary branches at or before anthesis and for mature ripening tissue from the main culm. The results for the main culm are from a previous study [1]. In each case, the results from two sorghum cultivars are combined. The reference line is at a proportion of 0.5, which was the proportion of the ¹⁴C-sucrose at the time of introduction into the plant. The error bars are 95% confidence intervals.