Arabidopsis sucrose synthase localization indicates a primary role in sucrose translocation in phloem.

Shawn D Mansfield,Danyu Yao,Eliana Gonzales-Vigil,Christine Foyer

doi:10.1093/jxb/erz539

Abstract

Sucrose synthase (SuSy) is one of two enzyme families capable of catalyzing the first degradative step in sucrose utilization. Several earlier studies examining SuSy mutants in Arabidopsis failed to identify obvious phenotypic abnormalities compared with wild-type plants in normal growth environments, and as such a functional role for SuSy in the previously proposed cellulose biosynthetic process remains unclear. Our study systematically evaluated the precise subcellular localization of all six isoforms of Arabidopsis SuSy via live-cell imaging. We showed that yellow fluorescent protein (YFP)-labeled SuSy1 and SuSy4 were expressed exclusively in phloem companion cells, and the sus1/sus4 double mutant accumulated sucrose under hypoxic conditions. SuSy5 and SuSy6 were found to be parietally localized in sieve elements and restricted only to the cytoplasm. SuSy2 was present in the endosperm and embryo of developing seeds, and SuSy3 was localized to the embryo and leaf stomata. No single isoform of SuSy was detected in developing xylem tissue of elongating stem, the primary site of cellulose deposition in plants. SuSy1 and SuSy4 were also undetectable in the protoxylem tracheary elements, which were induced by the vascular-related transcription factor VND7 during secondary cell wall formation. These findings implicate SuSy in the biological events related to sucrose translocation in phloem.

Highlights

In the vast majority of terrestrial plants, assimilated carbon from photosynthesis is primarily transported as sucrose to nonphotosynthetic tissues, where it serves an integral role as a carbon and energy source
The Arabidopsis stem is considered a model system to study cell wall synthesis and, cellulose biosynthesis, as it is largely composed of xylem vessels and fiber cells, which in turn are dominated by the cellulose polymer
The Sucrose synthase (SuSy) pathway has been generally considered the dominant route of sucrose catabolism in many plants, its essential role in Arabidopsis growth and development has been questioned by several studies (Bieniawska et al, 2007; Barratt et al, 2009)

Summary

Introduction

In the vast majority of terrestrial plants, assimilated carbon from photosynthesis is primarily transported as sucrose to nonphotosynthetic tissues, where it serves an integral role as a carbon and energy source. Sucrose synthases have been shown to play an important role in modulating sink strength (D’Aoust et al, 1999). Phloem loading and sucrose breakdown efficiency in sink organs are thought to be important for defining sink strength. SuSy localization in phloem tissue has been observed through β-glucuronidase (GUS) histochemical staining or immunolabeling in many plant species, including maize (Nolte and Koch, 1993; Regmi et al, 2016), potato (Fu and Park, 1995), rice (Shi et al, 1994), citrus (Nolte and Koch, 1993), and Arabidopsis (Martin et al, 1993; Fallahi et al, 2008).

Methods

Results

Conclusion