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Title: Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport

item SOSSO, DAVIDE - University Of Florida
item LUO, DANGPING - University Of Florida
item Li, Qin-Bao
item SASSE, JOELLE - University Of Florida
item YANG, JINLIANG - University Of Florida
item GENDROT, GHISLAINE - University Of Florida
item SUZUKI, MASAHARU - University Of Florida
item KOCH, KAREN - University Of Florida
item MCCARTY, DONALD - University Of Florida
item CHOUREY, PREM - Retired ARS Employee
item ROGOWSKY, PETER - University Of Florida
item ROSS-IBARRA, JEFFREY - University Of Florida
item YANG, BING - University Of Florida
item FROMMER, WOLF - University Of Florida

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/23/2015
Publication Date: 12/1/2015
Citation: Sosso, D., Luo, D., Li, Q., Sasse, J., Yang, J., Gendrot, G., Suzuki, M., Koch, K., Mccarty, D., Chourey, P., Rogowsky, P., Ross-Ibarra, J., Yang, B., Frommer, W. 2015. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nature Genetics. 47(12):1489-1496.

Interpretive Summary: Maize and rice SWEET4 genes encode hexose transporters likely acting downstream of a cell wall invertase which hydrolyzes phloem-derived sucrose. ZmSWEET4c and OsSWEET4 appear to be responsible for transferring hexoses across the BETL to sustain development of the large starch-storing endosperm of cereal grains and contribute to their sink strength. Reduced sequence variation at ZmSWEET4c and OsSWEET4 intimates that both loci were targets of selection during domestication. Engineering of SWEET hexose transporters may help generating new high-yield maize and rice varieties. We propose a model for glucose­ mediated feed-forward regulation that couples plasma membrane amplification to invertase and SWEET activity. Our work highlights processes analogous to trans-epithelial sugar import across cells with amplified membrane surface, mediated by SWEET4 in plants and GLUT2 in humans. Further work is required to determine whether SWEET4c localizes to both apical and basal BETL membranes and contributes to uptake and efflux.

Technical Abstract: Carbohydrate import into seeds directly determines seed size and must have been increased through domestication. However, evidence for domestication of sugar translocation and the identity of seed filling transporters remained elusive. Maize ZmSWEET4c, as opposed to its sucrose-transporting homologs, mediates trans-epithelial hexose transport across the basal endosperm transfer layer (BETL), the entry point of nutrients into the seed, and shows signatures indicative of selection during domestication. Mutants of both maize zmsweet4c and its rice ortholog ossweet4 are defective in seed filling, indicating that a lack of hexose transport at the BETL impairs further transfer of sugars imported from the maternal phloem. In both cases SWEET4 was likely recruited during domestication to enhance sugar import into the endosperm.