Carbohydrate distribution via SWEET17 is critical for Arabidopsis inflorescence branching under drought.

Sugars Will Eventually be Exported Transporters (SWEETs) are the most recently discovered family of plant sugar transporters. By acting as uniporters, SWEETs facilitate the diffusion of sugars across cell membranes and play an important role in various physiological processes such as abiotic stress adaptation. AtSWEET17, a vacuolar fructose facilitator, was shown to be involved in the modulation of the root system during drought. In addition, previous studies have shown that overexpression of an apple homolog leads to increased drought tolerance in tomato plants. Therefore, SWEET17 might be a molecular element involved in plant responses to drought. However, the role and function of SWEET17 in above-ground tissues of Arabidopsis under drought stress remain elusive. By combining gene expression analysis and stem architecture with the sugar profiles of different above-ground tissues, we uncovered a putative role for SWEET17 in carbohydrate supply and thus cauline branch elongation, especially during periods of carbon limitation, as occurs under drought stress. Thus, SWEET17 seems to be involved in maintaining efficient plant reproduction under drought stress conditions.

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

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.

Vacuolar fructose transporter SWEET17 is critical for root development and drought tolerance.

Root growth and architecture are markedly influenced by both developmental and environmental cues. Sugars integrate different stimuli and are essential building blocks and signaling molecules for modulating the root system. Members from the SUGAR WILL EVENTUALLY BE EXPORTED TRANSPORTER (SWEET) family facilitate the transport of different sugars over cellular membranes and steer both inter and intracellular distribution of sugars. SWEET17 represents a fructose-specific sugar porter localized to the vacuolar membrane, the tonoplast. Here, we analyzed how SWEET17-dependent fructose released from vacuoles affects root growth during drought stress in Arabidopsis (Arabidopsis thaliana). We found that the SWEET17 gene was predominantly expressed in the root vasculature and in meristematic cells of the root tip. SWEET17 expression appeared markedly induced during lateral root (LR) outgrowth and under drought. Moreover, fructose repressed primary root growth but induced density and length of first order LRs. Consistently, sweet17 knock-out mutants exhibited reduced LR growth and a diminished expression of LR-development-related transcription factors during drought stress, resulting in impaired drought tolerance of sweet17 mutants. We discuss how SWEET17 activity integrates drought-induced cellular responses into fructose signaling necessary for modulation of the root system and maximal drought tolerance.

The nucellus: between cell elimination and sugar transport.

The architecture of the seed is shaped by the processes of tissue partitioning, which determines the volume ratio of maternal and zygotic tissues, and nutrient partitioning, which regulates nutrient distribution among tissues. In angiosperms, early seed development is characterized by antagonistic development of the nucellus maternal tissue and the endosperm fertilization product to become the main sugar sink. This process marked the evolution of angiosperms and outlines the most ancient seed architectures. In Arabidopsis, the endosperm partially eliminates the nucellus and imports sugars from the seed coat. Here, we show that the nucellus is symplasmically connected to the chalaza, the seed nutrient unloading zone, and works as both a sugar sink and source alongside the seed coat. After fertilization, the transient nucellus accumulates starch early on and releases it in the apoplasmic space during its elimination. By contrast, the persistent nucellus exports sugars toward the endosperm through the SWEET4 hexose facilitator. Finally, we analyzed sugar metabolism and transport in the transparent testa 16 mutant, which fails to undergo nucellus cell elimination, which shed light on the coordination between tissue and nutrient partitioning. Overall, this study identifies a path of sugar transport in the Arabidopsis seed and describes a link between sugar redistribution and the nucellus cell-elimination program.

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

Plant growth and development rely on the transport and use of sugars produced during photosynthesis. Sugars have a dual function as nutrients and signal molecules in the cell. Many factors maintaining sugar homeostasis and signaling are now identified, but our understanding of the mechanisms involved in coordinating intracellular and intercellular sugar translocation is still limited. We also know little about the interplay between sugar transport and signaling and the formation of the vascular system, which controls long-distance sugar translocation. Sugar signaling has been proposed to play a role; however, evidence to support this hypothesis is still limited. Here, we exploited recent transcriptomics datasets produced in aerial organs of Arabidopsis to identify genes coding for sugar transporters or signaling components expressed in the vascular cells. We identified genes belonging to sugar transport and signaling for which no information is available regarding a role in vasculature development. In addition, the transcriptomics datasets obtained from sugar-treated Arabidopsis seedlings were used to assess the sugar-responsiveness of known genes involved in vascular differentiation. Interestingly, several key regulators of vascular development were found to be regulated by either sucrose or glucose. Especially CLE41, which controls the procambial cell fate, was oppositely regulated by sucrose or glucose in these datasets. Even if more experimental data are necessary to confirm these findings, this survey supports a link between sugar transport/signaling and vascular system development.

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

Carbon (C) and nitrogen (N) metabolisms have long been known to be coupled, and this is required for adjusting nitrogen use efficiency (NUE). Despite this intricate relationship, it is still unclear how deregulation of sugar transport impacts N allocation. Here, we investigated in Arabidopsis the consequences of the simultaneous downregulation of the genes coding for the sugar transporters SWEET11, SWEET12, SWEET16, and SWEET17 on various anatomical and physiological traits ranging from the stem's vascular system development to plant biomass production, seed yield, and N remobilization and use efficiency. Our results show that intracellular sugar exchanges mediated by SWEET16 and SWEET17 proteins specifically impact vascular development but do not play a significant role in the distribution of N. Most importantly, we showed that the double mutant swt11 swt12, which has an impacted vascular development, displays an improved NUE and nitrogen remobilization to the seeds. In addition, a significant negative correlation between sugar and amino acids contents and the inflorescence stem radial growth exists, highlighting the complex interaction between the maintenance of C/N homeostasis and the inflorescence stem development. Our results thus deepen the link between sugar transport, C/N allocation, and vascular system development.

DspA/E-Triggered Non-Host Resistance against E. amylovora Depends on the Arabidopsis GLYCOLATE OXIDASE 2 Gene.

DspA/E is a type three effector injected by the pathogenic bacterium Erwinia amylovora inside plant cells. In non-host Arabidopsis thaliana, DspA/E inhibits seed germination, root growth, de novo protein synthesis and triggers localized cell death. To better understand the mechanisms involved, we performed EMS mutagenesis on a transgenic line, 13-1-2, containing an inducible dspA/E gene. We identified three suppressor mutants, two of which belonged to the same complementation group. Both were resistant to the toxic effects of DspA/E. Metabolome analysis showed that the 13-1-2 line was depleted in metabolites of the TCA cycle and accumulated metabolites associated with cell death and defense. TCA cycle and cell-death associated metabolite levels were respectively increased and reduced in both suppressor mutants compared to the 13-1-2 line. Whole genome sequencing indicated that both suppressor mutants displayed missense mutations in conserved residues of Glycolate oxidase 2 (GOX2), a photorespiratory enzyme that we confirmed to be localized in the peroxisome. Leaf GOX activity increased in leaves infected with E. amylovora in a DspA/E-dependent manner. Moreover, the gox2-2 KO mutant was more sensitive to E. amylovora infection and displayed reduced JA-signaling. Our results point to a role for glycolate oxidase in type II non-host resistance and to the importance of central metabolic functions in controlling growth/defense balance.

Involvement of SUT1 and SUT2 Sugar Transporters in the Impairment of Sugar Transport and Changes in Phloem Exudate Contents in Phytoplasma-Infected Plants.

Phytoplasmas inhabit phloem sieve elements and cause abnormal growth and altered sugar partitioning. However, how they interact with phloem functions is not clearly known. The phloem responses were investigated in tomatoes infected by "Candidatus Phytoplasma solani" at the beginning of the symptomatic stage, the first symptoms appearing in the newly emerged leaf at the stem apex. Antisense lines impaired in the phloem sucrose transporters SUT1 and SUT2 were included. In symptomatic sink leaves, leaf curling was associated with higher starch accumulation and the expression of defense genes. The analysis of leaf midribs of symptomatic leaves indicated that transcript levels for genes acting in the glycolysis and peroxisome metabolism differed from these in noninfected plants. The phytoplasma also multiplied in the three lower source leaves, even if it was not associated with the symptoms. In these leaves, the rate of phloem sucrose exudation was lower for infected plants. Metabolite profiling of phloem sap-enriched exudates revealed that glycolate and aspartate levels were affected by the infection. Their levels were also affected in the noninfected SUT1- and SUT2-antisense lines. The findings suggest the role of sugar transporters in the responses to infection and describe the consequences of impaired sugar transport on the primary metabolism.

Beneficial rhizobacteria Pseudomonas simiae WCS417 induce major transcriptional changes in plant sugar transport.

Plants live in close relationships with complex populations of microorganisms, including rhizobacterial species commonly referred to as plant growth-promoting rhizobacteria (PGPR). PGPR are able to improve plant productivity, but the molecular mechanisms involved in this process remain largely unknown. Using an in vitro experimental system, the model plant Arabidopsis thaliana, and the well-characterized PGPR strain Pseudomonas simiae WCS417r (PsWCS417r), we carried out a comprehensive set of phenotypic and gene expression analyses. Our results show that PsWCS417r induces major transcriptional changes in sugar transport and in other key biological processes linked to plant growth, development, and defense. Notably, we identified a set of 13 genes of the SWEET and ERD6-like sugar transporter gene families whose expression is up- or down-regulated in response to seedling root inoculation with the PGPR or exposure to their volatile compounds. Using a reverse genetic approach, we demonstrate that SWEET11 and SWEET12 are functionally involved in the interaction and its plant growth-promoting effects, possibly by controlling the amount of sugar transported from the shoot to the root and to the PGPR. Altogether, our study reveals that PGPR-induced beneficial effects on plant growth and development are associated with changes in plant sugar transport.

Salinity Effects on Sugar Homeostasis and Vascular Anatomy in the Stem of the Arabidopsis Thaliana Inflorescence.

The regulation of sugar metabolism and partitioning plays an essential role for a plant's acclimation to its environment, with specific responses in autotrophic and heterotrophic organs. In this work, we analyzed the effects of high salinity on sugar partitioning and vascular anatomy within the floral stem. Stem sucrose and fructose content increased, while starch reduced, in contrast to the response observed in rosette leaves of the same plants. In the stem, the effects were associated with changes in the expression of SWEET and TMT2 genes encoding sugar transporters, SUSY1 encoding a sucrose synthase and several FRK encoding fructokinases. By contrast, the expression of SUC2, SWEET11 and SWEET12, encoding sugar transporters for phloem loading, remained unchanged in the stem. Both the anatomy of vascular tissues and the composition of xylem secondary cell walls were altered, suggesting that high salinity triggered major readjustments of sugar partitioning in this heterotrophic organ. There were changes in the composition of xylem cell walls, associated with the collapse and deformation of xylem vessels. The data are discussed regarding sugar partitioning and homeostasis of sugars in the vascular tissues of the stem.