A vacuolar hexose transport is required for xylem development in the inflorescence stem

Abstract

In Angiosperms, the development of the vascular system is controlled by a complex network of transcription factors. However, how nutrient availability in the vascular cells affects their development remains to be addressed. At the cellular level, cytosolic sugar availability is regulated mainly by sugar exchanges at the tonoplast through active and/or facilitated transport. In Arabidopsis (Arabidopsis thaliana), among the genes encoding tonoplastic transporters, SUGAR WILL EVENTUALLY BE EXPORTED TRANSPORTER 16 (SWEET16) and SWEET17 expression has been previously detected in the vascular system. Here, using a reverse genetics approach, we propose that sugar exchanges at the tonoplast, regulated by SWEET16, are important for xylem cell division as revealed in particular by the decreased number of xylem cells in the swt16 mutant and the accumulation of SWEET16 at the procambium–xylem boundary. In addition, we demonstrate that transport of hexoses mediated by SWEET16 and/or SWEET17 is required to sustain the formation of the xylem secondary cell wall. This result is in line with a defect in the xylem cell wall composition as measured by Fourier-transformed infrared spectroscopy in the swt16swt17 double mutant and by upregulation of several genes involved in secondary cell wall synthesis. Our work therefore supports a model in which xylem development partially depends on the exchange of hexoses at the tonoplast of xylem-forming cells.

Delving deeper into the link between sugar transport, sugar signaling, and vascular system development

“…Further, our study highlights the need for new approaches to discriminate the metabolic role of sugars from their signaling role in the vascular tissues in which sugars are abundant. It should be emphasized that we did not analyze the role of other sugars, such as fructose, which emerges as an additional signal molecule in the regulation of plant development (Aubry et al, 2022; Stein & Granot, 2018; Valifard et al, 2021).…”

“…Especially, the symplasmic transport plays a key role in delivering phloem-mobile sugars to root/SAM and developing leaves (Gisel et al, 1999(Gisel et al, , 2002Ross-Elliott et al, 2017;Schulz, 2005). It emerges as an additional signal molecule in the regulation of plant development (Aubry et al, 2022;Stein & Granot, 2018;Valifard et al, 2021).…”

“…(2) modification of sucrose and fructose metabolism alter the development of vascular tissues (Granot et al, 2013), (3) effects of tree girdling on carbon allocation, i.e. alteration of wood formation (Winkler & Oberhuber, 2017), (4) induction of phloem and xylem elements by sucrose in callus during in vitro culture (Wetmore & Rier, 1963;Jeffs & Northcote, 1966, 1967Wilson et al Warren et al, 1994), and (5) modification of sugar homeostasis in the vascular tissue alter xylem development (Aubry et al, 2022;Gerber et al, 2014;Mahboubi et al, 2013;Unda et al, 2017). These obser- S1 of sugars is also transported to the adjacent tissues (Gould et al, 2012), in particular for cambial activity and xylem cell development, which are large energy sinks and depend on a continuous supply of soluble sugars (Hansen & Beck, 1994;Muller et al, 2011;Oribe et al, 2003;Spicer, 2014).…”

“…Several lines of evidence support such a role: (1) concentration gradients of soluble sugars in the vascular tissues (Abreu et al, 2020; Roach et al, 2017; Uggla et al, 2001; Verscht et al, 2006) (Figure 1), (2) modification of sucrose and fructose metabolism alter the development of vascular tissues (Granot et al, 2013), (3) effects of tree girdling on carbon allocation, i.e. alteration of wood formation (Winkler & Oberhuber, 2017), (4) induction of phloem and xylem elements by sucrose in callus during in vitro culture (Wetmore & Rier, 1963; Jeffs & Northcote, 1966, 1967; Wilson et al Warren et al, 1994), and (5) modification of sugar homeostasis in the vascular tissue alter xylem development (Aubry et al, 2022; Gerber et al, 2014; Mahboubi et al, 2013; Unda et al, 2017). These observations raise the question of how the development of the vascular tissues can adjust to carbon availability and whether sugar signaling pathways are acting upstream of master genes involved in the vascular development.…”

Impairment of sugar transport in the vascular system acts on nitrogen remobilisation and nitrogen use efficiency in Arabidopsis

“…In this work, we proposed to fill this gap by evaluating consequences of a deregulation of members of the SWEET sugar transporter family on biomass production, seed yield and N allocation in Arabidopsis. Based on our previous work, we focused on the concurrent downregulation of SWEET11 , SWEET12 , SWEET16 and SWEET17 genes shown to be expressed in the inflorescence stem (Le Hir et al , 2015; Aubry et al , 2022). Indeed, this organ constitutes an obligatory step for nutrients to be transported from leaves to seeds and is therefore of interest when studying whole plant C and N allocation.…”