Mechanisms of phloem unloading: shaped by cellular pathways, their conductances and sink function.

Phloem unloading represents a series of cell-to-cell transport steps transferring phloem-mobile constituents from phloem to sink tissues/organs to fuel their development or resource storage. Our analysis focuses on unloading of two major phloem-mobile constituents, sugars and water. Their unloading can occur across phloem plasma membranes (apoplasmic unloading), through plasmodesmata interconnecting phloem and sink cells (symplasmic unloading) or predominately symplasmically with an intervening post-phloem apoplasmic step. In planta studies of phloem unloading encounter substantial technical challenges in accessing phloem within a meshwork of vascular/ground tissues. Thus, current understanding of phloem-unloading mechanisms largely has been deduced from indirect experimental measures or modelling. Here we highlight recent advances in understanding phloem unloading mechanisms and identify where important knowledge gaps remain.

• Publication year

  2018

• Venue

  Current opinion in plant biology

• Publication date

  2018-06-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1016/j.pbi.2017.11.003PMID 29248828
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  1985cited by this paper
• Long distance transport.

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  2018cites this paper