The Tonoplast-Localized Sucrose Transporter in Populus (PtaSUT4) Regulates Whole-Plant Water Relations, Responses to Water Stress, and Photosynthesis

Abstract

The Populus sucrose (Suc) transporter 4 (PtaSUT4), like its orthologs in other plant taxa, is tonoplast localized and thought to mediate Suc export from the vacuole into the cytosol. In source leaves of Populus, SUT4 is the predominantly expressed gene family member, with transcript levels several times higher than those of plasma membrane SUTs. A hypothesis is advanced that SUT4-mediated tonoplast sucrose fluxes contribute to the regulation of osmotic gradients between cellular compartments, with the potential to mediate both sink provisioning and drought tolerance in Populus. Here, we describe the effects of PtaSUT4-RNA interference (RNAi) on sucrose levels and raffinose family oligosaccharides (RFO) induction, photosynthesis, and water uptake, retention and loss during acute and chronic drought stresses. Under normal water-replete growing conditions, SUT4-RNAi plants had generally higher shoot water contents than wild-type plants. In response to soil drying during a short-term, acute drought, RNAi plants exhibited reduced rates of water uptake and delayed wilting relative to wild-type plants. SUT4-RNAi plants had larger leaf areas and lower photosynthesis rates than wild-type plants under well-watered, but not under chronic water-limiting conditions. Moreover, the magnitude of shoot water content, height growth, and photosynthesis responses to contrasting soil moisture regimes was greater in RNAi than wild-type plants. The concentrations of stress-responsive RFOs increased in wild-type plants but were unaffected in SUT4-RNAi plants under chronically dry conditions. We discuss a model in which the subcellular compartmentalization of sucrose mediated by PtaSUT4 is regulated in response to both sink demand and plant water status in Populus.

Regulation of Sucrose Transporters and Phloem Loading in Response to Environmental Cues

“…In the passive symplasmic loader poplar, PtSUT4 is down-regulated (Fig. 4E), confirming its involvement in the drought response indicated by the study of knock-out plants (Frost et al, 2012;Xue et al, 2016). Also notable is the strong reduction in expression of Arabidopsis AtSUC1 ( Figure 4A), a type I SUT not directly involved in phloem loading, which was also down-regulated in response to drought stress.…”

“…There is increasing evidence that different types of SUTs are involved in the response to abiotic stress (Sivitz et al, 2008;Frost et al, 2012;Gong et al, 2015;Jia et al, 2015). Based on the extensive transcriptomics data available for drought, salt, and heat stress, these data are extended here by the identification of patterns in the response of SUT expression.…”

“…Since this is not the case, mechanisms that either modulate the cytosolic Suc concentration or the capacity for transport into the phloem must exist . In poplar, down-regulation of the vacuolar Suc transporter PtaSUT4 via RNAi decreases source strength and leads to Suc accumulation in the leaf as well as lower photosynthetic activity (Payyavula et al, 2011;Frost et al, 2012). It can be hypothesized that PtaSUT4 activity regulates the cytosolic concentration of Suc in leaf mesophyll cells by controlling the exchange with the vacuole, thereby influencing the Suc gradient along the prephloem pathway that determines the rate of phloem loading (Liesche, 2017).…”

Constitutively Elevated Salicylic Acid Levels Alter Photosynthesis and Oxidative State but Not Growth in Transgenic Populus

“…Primary transformants were transplanted to soil and maintained in a greenhouse for initial characterization. Selected transgenic lines along with the wild type were vegetatively propagated by rooted cuttings as described (Frost et al, 2012) for subsequent experiments.…”

“…Net photosynthesis, stomatal conductance, and transpiration rates were measured three times during the 10-d HT period and once after 1-week recovery. Two leaves (LPI-5 and LPI-10) were measured independently on each plant using a LiCor LI-6400XS at a saturating light intensity of 1500 µmol/m 2 /s as described (Frost et al, 2012). To test the effects of HT treatment, genotype, and their interaction on photosynthesis, data were analyzed by repeated measures ANOVA, using a linear mixed effect model with the lme function in R. Significant genotypic differences were further analyzed by pairwise comparisons between the wild type and each transgenic line.…”