A sugar transporter takes up both hexose and sucrose for sorbitol-modulated in vitro pollen tube growth in apple

Authors: LI, CHUNLONG - Cornell University; MENG, DONG - Cornell University; Pineros, Miguel; MAO, YUAN - Cornell University; DANDEKAR, ABHAYA - University Of California, Davis; CHENG, LAILIANG - Cornell University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/3/2019
Publication Date: 2/1/2020
Citation: Li, C., Meng, D., Pineros, M., Mao, Y., Dandekar, A.M., Cheng, L. 2020. A sugar transporter takes up both hexose and sucrose for sorbitol-modulated in vitro pollen tube growth in apple. The Plant Cell. 32:449-469. https://doi.org/10.1105/tpc.19.00638.
DOI: https://doi.org/10.1105/tpc.19.00638

Interpretive Summary: The lack of understanding in the cellular mechanisms determining fertilization makes genetic improvement of tree fertility challenging for apple breeders. The successful germination and rapid growth of pollen tubes is a key step in the reproductive cycle of flowering plants. Although in the early stages of these processes, the pollen can rely energetically on nutrient storage in the grain, at later growth stages it requires to acquire a variety of sugar resources from its surroundings. It is unknown if plants require to regulate a suite of various sugar transport proteins to achieve this process, or if they have sugar transporters that can take up both simple (hexose monosaccharides) and disaccharides (sucrose) sugar substrates. A multidisciplinary approach was used to characterized an apple sugar transport protein (STP13) in the pollen grain. This protein can mediate the uptake of sucrose and hexose in a dynamic process, which is essential for the modulated pollen tube growth. Sorbitol, a significant product of photosynthesis and transport carbohydrate in apple, modulates pollen tube growth via known transcription factors (MYBs). The mechanistic findings in this work should assist in selection in apple breeding programs targeting fertility traits.

Technical Abstract: Rapid pollen tube growth requires uptake of Suc or its hydrolytic products, hexoses, from the apoplast of surrounding tissues in the style. Due to species-specific sugar requirements, reliance of pollen germination and tube growth on cell wall invertase and Suc or hexose transporters varies between species, but it is not known if plants have a sugar transporter that mediates the uptake of both hexose and Suc for pollen tube growth. Here, we show that a sugar transporter protein in apple (Malus domestica), MdSTP13a, takes up both hexose and Suc when expressed in yeast, and is essential for pollen tube growth on Glc and Suc but not on maltose. MdSTP13a-mediated direct uptake of Suc is primarily responsible for apple pollen tube growth on Suc medium. Sorbitol, a major photosynthate and transport carbohydrate in apple, modulates pollen tube growth via the MYB transcription factor MdMYB39L, which binds to the promoter of MdSTP13a to activate its expression. Antisense repression of MdSTP13a blocks sorbitol-modulated pollen tube growth. These findings demonstrate that MdSTP13a takes up both hexose and Suc for sorbitol-modulated pollen tube growth in apple, revealing a situation where acquisition of sugars for pollen tube growth is regulated by a sugar alcohol.