Phloem loading in cucumber: combined symplastic and apoplastic strategies

Abstract

These authors contributed equally to this work. SUMMARYPhloem loading, as the first step of transporting photoassimilates from mesophyll cells to sieve element-companion cell complex, creates a driving force for long-distance nutrient transport. Three loading strategies have been proposed: passive symplastic loading, apoplastic loading and symplastic transfer followed by polymer-trapping of stachyose and raffinose. Although individual species are generally referred to as using a single phloem loading mechanism, it has been suggested that some plants may use more than one, i.e. 'mixed loading'. Here, by using a combination of electron microscopy, reverse genetics and 14 C labeling, loading strategies were studied in cucumber, a polymer-trapping loading species. The results indicate that intermediary cells (ICs), which mediate polymer-trapping, and ordinary companion cells, which mediate apoplastic loading, were mainly found in the fifth and third order veins, respectively. Accordingly, a cucumber galactinol synthase gene (CsGolS1) and a sucrose transporter gene (CsSUT2) were expressed mainly in the fifth/third and the third order veins, respectively. Immunolocalization analysis indicated that CsGolS1 was localized in companion cells (CCs) while CsSUT2 was in CCs and sieve elements (SEs). Suppressing CsGolS1 significantly decreased the stachyose level and increased sucrose content, while suppressing CsSUT2 decreased the sucrose level and increased the stachyose content in leaves. After 14 CO 2 labeling, [ 14 C]sucrose export increased and [ 14 C]stachyose export reduced from petioles in CsGolS1i plants, but [ 14 C]sucrose export decreased and [ 14 C]stachyose export increased into petioles in CsSUT2i plants. Similar results were also observed after pre-treating the CsGolS1i leaves with PCMBS (transporter inhibitor). These results demonstrate that cucumber phloem loading depends on both polymer-trapping and apoplastic loading strategies.

Down-regulation of the Sucrose Transporter CsSUT1 Causes Male Sterility by Altering Carbohydrate Supply

“…Various SUT genes are also expressed in pollen grains and have been reported to affect pollen germination and/or tube elongation (Hackel et al, 2006;Sivitz et al, 2008). It is worth mentioning that another cucumber Suc transporter gene, CsSUT2, is expressed in mature leaves and participates in the phloem loading (Ma et al, 2019).…”

Continuous Light Does Not Compromise Growth and Yield in Mini-Cucumber Greenhouse Production with Supplemental LED Light

“…The major difference between cucumber and tomato are their carbohydrate metabolism, specifically their carbon export process. In tomatoes, sucrose is the primary phloem mobile carbohydrate, whereas, in cucumbers, raffinose and stachyose are the main carbohydrates exported [46,47]. Moreover, tomatoes use an apoplastic phloem loading mechanism, whereas cucumbers use a symplastic polymer trap mechanism.…”

“…Namely, apoplastic phloem loading is a complicated pathway involving multiple cell lines, enzymes, and transporters, which all act as potential points of regulation [47,48]. Symplastic phloem loading is much more rudimentary, with minimal points of enzymatic regulation [46]. Due to the form of phloem loading and the production of auxiliary sugars such as raffinose and stachyose, cucumbers are known to be rapid exporters of recently fixed carbon, minimizing carbohydrate accumulation (i.e., starch) in the leaf [49].…”

Complexity untwined: The structure and function of cucumber (Cucumis sativus L.) shoot phloem

“…However, transport phloem has both collection and release functions: it unloads sugars and nutrients to supply the metabolic needs of flanking tissues and to stock transient and long‐term storage reserves, meanwhile retrieving and loading leaked sugars and those from lateral reserves (van Bel, 2003). Although phloem loading in the minor veins of cucumber is driven by the polymer trap mechanism (Turgeon et al ., 1993), sucrose retrieval from the apoplast in other tissues is mediated by Suc/H + symporters (Ma et al ., 2019). Accordingly, CsSUT2 is localized to the plasma membranes of SE/CC complexes mainly in the third order veins, functioning as a Suc/H + symporter and contributing to apoplastic phloem loading and export.…”