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Sucrose accumulation in sweet sorghum stems occurs by apoplasmic phloem unloading and does not involve differential Sucrose transporter expression.

Bihmidine S, Baker RF, Hoffner C, Braun DM - BMC Plant Biol. (2015)

Bottom Line: Once in the phloem apoplasm, a soluble tracer diffused from the vein to stem parenchyma cell walls, indicating the lignified mestome sheath encompassing the vein did not prevent apoplasmic flux outside of the vein.Contrary to previous findings, we detected no significant differences in SbSUTs gene expression within stem tissues.Additionally, no changes in SbSUTs gene expression were detected in sweet vs. grain sorghum stems, suggesting alterations in SbSUT transcript levels do not account for the carbohydrate partitioning differences between cultivars.

View Article: PubMed Central - PubMed

Affiliation: Division of Biological Sciences, Interdisciplinary Plant Group, and Missouri Maize Center, University of Missouri, 110 Tucker Hall, Columbia, MO, 65211, USA. bihmidines@missouri.edu.

ABSTRACT

Background: Sorghum (Sorghum bicolor L. Moench) cultivars store non-structural carbohydrates predominantly as either starch in seeds (grain sorghums) or sugars in stems (sweet sorghums). Previous research determined that sucrose accumulation in sweet sorghum stems was not correlated with the activities of enzymes functioning in sucrose metabolism, and that an apoplasmic transport step may be involved in stem sucrose accumulation. However, the sucrose unloading pathway from stem phloem to storage parenchyma cells remains unelucidated. Sucrose transporters (SUTs) transport sucrose across membranes, and have been proposed to function in sucrose partitioning differences between sweet and grain sorghums. The purpose of this study was to characterize the key differences in carbohydrate accumulation between a sweet and a grain sorghum, to define the path sucrose may follow for accumulation in sorghum stems, and to determine the roles played by sorghum SUTs in stem sucrose accumulation.

Results: Dye tracer studies to determine the sucrose transport route revealed that, for both the sweet sorghum cultivar Wray and grain sorghum cultivar Macia, the phloem in the stem veins was symplasmically isolated from surrounding cells, suggesting sucrose was apoplasmically unloaded. Once in the phloem apoplasm, a soluble tracer diffused from the vein to stem parenchyma cell walls, indicating the lignified mestome sheath encompassing the vein did not prevent apoplasmic flux outside of the vein. To characterize carbohydrate partitioning differences between Wray and Macia, we compared the growth, stem juice volume, solute contents, SbSUTs gene expression, and additional traits. Contrary to previous findings, we detected no significant differences in SbSUTs gene expression within stem tissues.

Conclusions: Phloem sieve tubes within sweet and grain sorghum stems are symplasmically isolated from surrounding cells; hence, unloading from the phloem likely occurs apoplasmically, thereby defining the location of the previously postulated step for sucrose transport. Additionally, no changes in SbSUTs gene expression were detected in sweet vs. grain sorghum stems, suggesting alterations in SbSUT transcript levels do not account for the carbohydrate partitioning differences between cultivars. A model illustrating sucrose phloem unloading and movement to stem storage parenchyma, and highlighting roles for sucrose transport proteins in sorghum stems is discussed.

No MeSH data available.


Comparison of the growth of grain (cv. Macia) and sweet (cv. Wray) sorghum plants. A side-by-side comparison of plants collected from the field at the early vegetative stage (a). Plants at maturity (b). A graph of the height of Macia and Wray plants measured in cm at different days after planting (c). Values are means ± SE of N = 10 plants, an asterisk indicates significantly different means between the two lines at p ≤ 0.05, and the arrows indicate the anthesis time for each line. Macia = black squares, and Wray = white squares
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Fig1: Comparison of the growth of grain (cv. Macia) and sweet (cv. Wray) sorghum plants. A side-by-side comparison of plants collected from the field at the early vegetative stage (a). Plants at maturity (b). A graph of the height of Macia and Wray plants measured in cm at different days after planting (c). Values are means ± SE of N = 10 plants, an asterisk indicates significantly different means between the two lines at p ≤ 0.05, and the arrows indicate the anthesis time for each line. Macia = black squares, and Wray = white squares

Mentions: To understand how and when Macia and Wray differ in terms of growth, yield, and carbohydrate allocation, we characterized plant growth, anthesis, biomass accumulation, and the total solutes in the stem juice, which is composed primarily of apoplasmic fluid, cytoplasm, and vacuolar sap, at multiple stages throughout their lifecycle. The early seedling growth of Macia and Wray appeared very similar (Fig. 1a). However, a number of morphological differences between the two cultivars emerged over time (Fig. 1b, c, and Additional file 1: Table S1). Beginning in the late vegetative stage (after 43 days after planting (DAP)), Wray developed taller stems as compared to Macia, with the difference in plant height increasing and being maintained throughout the season (Fig. 1b, c). In association with the increased stem height, Wray flowered an average of five days later than Macia (Fig. 1c). Additionally, Wray produced higher stem biomass compared to Macia (Fig. 2). Specifically, the total fresh and dry weight of the main stem collected at harvest was significantly higher in Wray than Macia (Fig. 2d). With the exception of the top one to two internodes, this difference was also reflected for each individual internode (Fig. 2b, c). Internode weights from Macia and Wray showed about a two-fold and nine-fold variation, respectively. Although Wray showed a significant increase in stem biomass, Macia displayed shorter but thicker stems (Fig. 2a, e, f). However, apart from the top two internodes, the significantly greater length of most of the internodes in Wray contributed more to the mass per internode than the greatly increased stem thickness in Macia (Fig. 2a-c, e, f). Therefore, Wray outperformed Macia at the level of biomass accumulation, as would be predicted for a sweet sorghum cultivar.Fig. 1


Sucrose accumulation in sweet sorghum stems occurs by apoplasmic phloem unloading and does not involve differential Sucrose transporter expression.

Bihmidine S, Baker RF, Hoffner C, Braun DM - BMC Plant Biol. (2015)

Comparison of the growth of grain (cv. Macia) and sweet (cv. Wray) sorghum plants. A side-by-side comparison of plants collected from the field at the early vegetative stage (a). Plants at maturity (b). A graph of the height of Macia and Wray plants measured in cm at different days after planting (c). Values are means ± SE of N = 10 plants, an asterisk indicates significantly different means between the two lines at p ≤ 0.05, and the arrows indicate the anthesis time for each line. Macia = black squares, and Wray = white squares
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4518677&req=5

Fig1: Comparison of the growth of grain (cv. Macia) and sweet (cv. Wray) sorghum plants. A side-by-side comparison of plants collected from the field at the early vegetative stage (a). Plants at maturity (b). A graph of the height of Macia and Wray plants measured in cm at different days after planting (c). Values are means ± SE of N = 10 plants, an asterisk indicates significantly different means between the two lines at p ≤ 0.05, and the arrows indicate the anthesis time for each line. Macia = black squares, and Wray = white squares
Mentions: To understand how and when Macia and Wray differ in terms of growth, yield, and carbohydrate allocation, we characterized plant growth, anthesis, biomass accumulation, and the total solutes in the stem juice, which is composed primarily of apoplasmic fluid, cytoplasm, and vacuolar sap, at multiple stages throughout their lifecycle. The early seedling growth of Macia and Wray appeared very similar (Fig. 1a). However, a number of morphological differences between the two cultivars emerged over time (Fig. 1b, c, and Additional file 1: Table S1). Beginning in the late vegetative stage (after 43 days after planting (DAP)), Wray developed taller stems as compared to Macia, with the difference in plant height increasing and being maintained throughout the season (Fig. 1b, c). In association with the increased stem height, Wray flowered an average of five days later than Macia (Fig. 1c). Additionally, Wray produced higher stem biomass compared to Macia (Fig. 2). Specifically, the total fresh and dry weight of the main stem collected at harvest was significantly higher in Wray than Macia (Fig. 2d). With the exception of the top one to two internodes, this difference was also reflected for each individual internode (Fig. 2b, c). Internode weights from Macia and Wray showed about a two-fold and nine-fold variation, respectively. Although Wray showed a significant increase in stem biomass, Macia displayed shorter but thicker stems (Fig. 2a, e, f). However, apart from the top two internodes, the significantly greater length of most of the internodes in Wray contributed more to the mass per internode than the greatly increased stem thickness in Macia (Fig. 2a-c, e, f). Therefore, Wray outperformed Macia at the level of biomass accumulation, as would be predicted for a sweet sorghum cultivar.Fig. 1

Bottom Line: Once in the phloem apoplasm, a soluble tracer diffused from the vein to stem parenchyma cell walls, indicating the lignified mestome sheath encompassing the vein did not prevent apoplasmic flux outside of the vein.Contrary to previous findings, we detected no significant differences in SbSUTs gene expression within stem tissues.Additionally, no changes in SbSUTs gene expression were detected in sweet vs. grain sorghum stems, suggesting alterations in SbSUT transcript levels do not account for the carbohydrate partitioning differences between cultivars.

View Article: PubMed Central - PubMed

Affiliation: Division of Biological Sciences, Interdisciplinary Plant Group, and Missouri Maize Center, University of Missouri, 110 Tucker Hall, Columbia, MO, 65211, USA. bihmidines@missouri.edu.

ABSTRACT

Background: Sorghum (Sorghum bicolor L. Moench) cultivars store non-structural carbohydrates predominantly as either starch in seeds (grain sorghums) or sugars in stems (sweet sorghums). Previous research determined that sucrose accumulation in sweet sorghum stems was not correlated with the activities of enzymes functioning in sucrose metabolism, and that an apoplasmic transport step may be involved in stem sucrose accumulation. However, the sucrose unloading pathway from stem phloem to storage parenchyma cells remains unelucidated. Sucrose transporters (SUTs) transport sucrose across membranes, and have been proposed to function in sucrose partitioning differences between sweet and grain sorghums. The purpose of this study was to characterize the key differences in carbohydrate accumulation between a sweet and a grain sorghum, to define the path sucrose may follow for accumulation in sorghum stems, and to determine the roles played by sorghum SUTs in stem sucrose accumulation.

Results: Dye tracer studies to determine the sucrose transport route revealed that, for both the sweet sorghum cultivar Wray and grain sorghum cultivar Macia, the phloem in the stem veins was symplasmically isolated from surrounding cells, suggesting sucrose was apoplasmically unloaded. Once in the phloem apoplasm, a soluble tracer diffused from the vein to stem parenchyma cell walls, indicating the lignified mestome sheath encompassing the vein did not prevent apoplasmic flux outside of the vein. To characterize carbohydrate partitioning differences between Wray and Macia, we compared the growth, stem juice volume, solute contents, SbSUTs gene expression, and additional traits. Contrary to previous findings, we detected no significant differences in SbSUTs gene expression within stem tissues.

Conclusions: Phloem sieve tubes within sweet and grain sorghum stems are symplasmically isolated from surrounding cells; hence, unloading from the phloem likely occurs apoplasmically, thereby defining the location of the previously postulated step for sucrose transport. Additionally, no changes in SbSUTs gene expression were detected in sweet vs. grain sorghum stems, suggesting alterations in SbSUT transcript levels do not account for the carbohydrate partitioning differences between cultivars. A model illustrating sucrose phloem unloading and movement to stem storage parenchyma, and highlighting roles for sucrose transport proteins in sorghum stems is discussed.

No MeSH data available.