Hexose translocation mediated by SlSWEET5b is required for pollen maturation in Solanum lycopersicum

Abstract

Pollen fertility is critical for successful fertilization and, accordingly, for crop yield. While sugar unloading affects growth and development of all types of sink organs, the molecular nature for sugar import to tomato pollen is poorly understood. However, SWEET transporters have been proposed to function in pollen development. Here, qRT-PCR revealed that SlSWEET5b was markedly expressed in flowers when compared to the remaining tomato SlSWEETs; particularly, in the stamens of maturing flower buds undergoing mitosis. Distinct accumulation of SlSWEET5b-GUS fusion proteins was present in mature flower buds, especially in anther vascular and inner cells, symplasmic isolated pollen cells and styles. The demonstration that GFP fusion proteins located to the plasma membrane support the idea that the SlSWEET5b carrier functions in apoplasmic sugar translocation during pollen maturation. Such function is in line with data from yeast complementation experiments and radiotracer uptakes, showing that SlSWEET5b operates as a low affinity hexose-specific passive facilitator, with a KM of ~36 mM. Most importantly, RNAi-mediated suppression of SlSWEET5b expression resulted in shrunken nucleus-less pollen cells, impaired germination and low seed yield. Interestingly, stamens from SlSWEET5b-silenced tomato mutants contained significantly lower amounts of sucrose and increased invertase activity, pointing to reduced carbon supply and perturbed sucrose homeostasis in this tissue. Taken together, our findings reveal an essential role of SlSWEET5b in mediating apoplasmic hexose import into phloem unloading cells and into developing pollen cells to support pollen mitosis and maturation in tomato flowers.

Sucrose rather than GA transported by AtSWEET13 and AtSWEET14 supports pollen fitness at late anther development stages

“…The released sucrose exported by AtSWEET13 and AtSWEET14 probably is partially cleaved into glucose and fructose by cell wall invertase 2 (AtcwINV2) or other AtcwINVs, because the AtcwINV2 antisense mutant displays defective pollen and reduced fertility phenotypes similar to atsweet13;14 (Hirsche et al ., 2009). The resulting hexoses and sucrose may be taken up by pollen grain‐accumulated AtSWEET5 (Ko et al ., 2022; Wang et al ., 2022b), AtSWEET8 (Zhang et al ., 2022), AtSUC1 (Stadler et al ., 1999; Sivitz et al ., 2008; Mergner et al ., 2020) and AtSWEET11/12 (Mergner et al ., 2020).…”

“…Sucrose Uptake Transporters (SUTs/SUCs), mainly transporting sucrose, often are paired with SWEETs in many processes (Braun, 2022). In tomato plants, SlSWEET5b mediates hexose export into the locules; unsurprisingly, the SlSWEET5b silencing mutant exhibits reduced pollen germination and seed production (Ko et al ., 2022). In rice, OsSUC1 is highly expressed in the wall of the anther, and the ossuc1 mutant shows impaired pollen function without affecting pollen maturation (Hirose et al ., 2010).…”

Sucrose rather than GA transported by AtSWEET13 and AtSWEET14 supports pollen fitness at late anther development stages

“…The released sucrose exported by AtSWEET13 and AtSWEET14 is likely to be partially cleaved into glucose and fructose by cell-wall invertase 2 (AtcwINV2) or other AtcwINVs, because the AtcwINV2 antisense mutant displays a defective pollen and reduced fertility phenotype similar to atsweet13;14 (Hirsche et al ., 2009). The resulting hexoses and sucrose may be taken up by pollen grain-accumulated AtSWEET5 (Ko et al ., 2022; Wang et al ., 2022b), AtSWEET8 (Zhang et al ., 2022) and AtSUC1 (Stadler et al ., 1999; Sivitz et al ., 2008), respectively.…”

“…Sucrose Uptake Transporters (SUTs/SUCs), mainly transporting sucrose, are often paired with SWEETs in many processes (Braun, 2022). In tomato, SlSWEET5b mediates hexose export into the locules; unsurprisingly, the SlSWEET5b silencing mutant exhibits reduced pollen germination and seed production (Ko et al ., 2022). In rice, OsSUC1 is highly expressed in the wall of anther, and the ossucl mutant shows impaired pollen function without affecting pollen maturation (Hirose et al ., 2010).…”