Abstract
Background: It is well known that cassava (Manihot esculenta Crantz) highly efficiently accumulates starch in its storage roots, but how photosynthates are transported from the leaves to the phloem (especially how they are unloaded into parenchymal cells of storage roots) remains unclear. Methods: Here, we investigated the phloem unloading pattern of sucrose and its impact on the development of cassava storage roots through microstructural and physiological analyses and carboxyfluorescein (CF) and isotope C14 tracing. Expression profiling of genes involved in symplastic and apoplastic transport was performed, and their correlations with storage root yield were determined in populations according to enzyme activity, Western blotting analysis and transcriptome sequencing. Results: Carbohydrates are transported mainly in the form of sucrose, with more than 54.6% present in the stem phloem at any time. Sucrose was predominantly unloaded symplastically from the phloem into storage roots, but there was a shift from apoplastic to symplastic unloading accompanied by the onset of root swelling. Statistical data concerning the microstructure revealed an enrichment of plasmodesmata within sieve, companion and parenchyma cells in the developing storage roots of a cultivar but not in a wild ancestor. Tracing tests with CF verified the existence of a coplastid channel, and [14C]Suc demonstrated that the marked sucrose could rapidly diffuse into root parenchyma cells from phloem cells. The relatively high expression of genes encoding SuSy and associated proteins in the storage roots at the middle and late stages but not in the early stage of storage roots, primary fibrous roots or secondary fibrous roots and the inverse expression pattern of SUTs, CWI and SAI in these corresponding organs supported the presence of a symplastic sucrose unloading pathway. The transcriptome pattern of genes involved in symplastic unloading and their significantly positive correction with starch yield at the population level confirmed that symplastic sucrose transport is vitally important in the development of cassava storage roots. Conclusions: In this study, we revealed a predominantly symplastic phloem unloading pattern of sucrose in cassava storage roots. This pattern is essential for the efficient starch accumulation for sucrose transport between high-yielding varieties and low-yielding wild ancestors.
Symplasmic phloem unloading and radial post-phloem transport via vascular rays in tuberous roots of Manihot esculenta