Cellular export of sugars and amino acids: role in feeding other cells and organisms

Abstract

Sucrose, hexoses and raffinose play key roles in plant metabolism. Sucrose and raffinose, produced by photosynthesis, are translocated from leaves to flowers, developing seeds and roots. Translocation occurs in the sieve elements or sieve tubes of angiosperms. But how is sucrose loaded into and unloaded from the sieve elements? There seem to be two principal routes: one through plasmodesmata and one via the apoplasm. The best-studied transporters are the H+/SUCROSE TRANSPORTERs (SUTs) in the sieve element-companion cell complex. Sucrose is delivered to SUTs by SWEET sugar uniporters that release these key metabolites into the apoplasmic space. The H+/amino acid permeases (AAPs) and the UmamiT amino acid transporters are hypothesized to play analogous roles as the SUT-SWEET pair to transport amino acids. SWEETs and UmamiTs also act in many other important processes – for example, seed filling, nectar secretion, and pollen nutrition. We present information on cell type specific enrichment of SWEET and UmamiT family members and propose several members to play redundant roles in the efflux of sucrose and amino acids across different cell types in the leaf. Pathogens hijack SWEETs and thus represent a major susceptibility of the plant. Here, we provide an update on the status of research on intercellular and long-distance translocation of key metabolites such as sucrose and amino acids, communication of the plants with the root microbiota via root exudates, discuss the existence of transporters for other important metabolites and provide potential perspectives that may direct future research activities.

Overexpression of the Potato Monosaccharide Transporter StSWEET7a Promotes Root Colonization by Symbiotic and Pathogenic Fungi by Increasing Root Sink Strength

“…However, the specificity of SWEET transporters for mono- or disaccharides is sometimes controversial in the literature. Thus, while most SWEET transporters are specific for only one type of sugar, for some others it is not totally clear, and some have been shown to transport both, mono- and disaccharides ( Kim et al, 2021 ). Furthermore, some SWEETs have been demonstrated to transport even sugar unrelated substrates, such as GA ( Kanno et al, 2016 ; Morii et al, 2020 ).…”

“…Increased resistance was mediated by activation of the salicylic acid-mediated defense response ( Gebauer et al, 2017 ). Although there are several other examples of sugar transporter activation by microbes that potentially implicate changes in susceptibility toward those microbes, perhaps the most prominent example is the activation of rice SWEET transporters by bacteria of the genus Xanthomonas by transcriptional activator like (TAL) effectors (reviewed in Eom et al, 2015 ; Kim et al, 2021 ). Because even before knowing which genes were involved, mutations in SWEET genes were shown to be susceptibility targets toward those bacteria ( Yang et al, 2006 ; Antony et al, 2010 ; Liu et al, 2011 ).…”

Mobile forms of carbon in trees: metabolism and transport

“…Apoplasmic phloem loading requires the presence of sugar/polyol exporters and importers in leaves. In herbaceous species, SWEET (sugar will be eventually exported) and SUT (sucrose/proton symport) transporters have been shown to be involved in the sucrose export and import, respectively, driving sucrose movement toward the SE/CCC (sieve element-companion cell complexes) in leaves ( Table 1 ) ( Riesmeier et al 1993 , Bürkle et al 1998 , Slewinski et al 2009 , Chen et al 2012 , Bezrutczyk et al 2018 , Kim et al 2021 ). Most of them remain to be functionally characterized in trees.…”

“…This implies the presence of sucrose transporters in both ray cells and fibers. Several SWEET transporters have been described in herbaceous plants as involved in sucrose transport in sink tissues ( Table 1 ) ( Le Hir et al 2015 , Sosso et al 2015 , Ma et al 2017 , Shammai et al 2018 , Yang et al 2018 , Kim et al 2021 ). The identification of SWEETs in several tree species, such as rubber tree ( Hevea brasiliensis (Willd.…”

Primary metabolism: It’s more than what's for dinner

“…Pathogens want them. Sugars, amino acids, and organic acids are continuously being exported from source cells to supply both other plant cells and potentially beneficial microorganisms (Kim et al, 2021). Logically, plants attempt to restrict access to pathogens by withholding these nutrients upon infection; and successful pathogens have evolved strategies to restore nutrient availability (Kim et al, 2021).…”