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

Abstract

Carbohydrate import into seeds directly determines seed size and must have been increased through domestication. However, evidence of the domestication of sugar translocation and the identities of seed-filling transporters have been elusive. Maize ZmSWEET4c, as opposed to its sucrose-transporting homologs, mediates transepithelial 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 maize and rice, SWEET4 was likely recruited during domestication to enhance sugar import into the endosperm.

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Figure 1: ZmSWEET4c molecular domestication and seed phenotype.
Figure 2: ZmSWEET4c localization in the BETL and hexose transport activity.
Figure 3: The zmsweet4c-umu1 mutant has altered BETL development.
Figure 4: The ZmSWEET4c ortholog in O. sativa (OsSWEET4) is essential for seed filling.

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Acknowledgements

We are grateful to D. Ehrhardt and H. Cartwright for confocal microscopy. For the rice experiments, we are grateful to T. Li for constructing the TALEN vector targeting OsSWEET4, B. Liu for rice transgenics, C. Ji for the isolation and transfection of rice protoplasts in the laboratory of B.Y. and X. Li for help with domestication analysis of OsSWEET4. We thank M. Greenfield, A. Grimault and K.M. Wong for plant care, Y. Gong for the yeast complementation assay, M. Evans for providing teosinte plant material and C. Stefan for renaming ZmSWEET4 with “c” for her initial. Work performed on maize in the laboratory of W.B.F. was made possible by support from the Office of Basic Energy Sciences of the US Department of Energy under grant DE-FG02-04ER15542, and work on rice was supported by the National Science Foundation under grant IOS-1258018 (B.Y. and W.B.F.); the other laboratories were supported by the National Science Foundation (IOS-1116561 to D.R.M. and K.E.K., IOS-1025976 to K.E.K. and IOS-1238014 to J.R.-I.), as well as USDA-NIFA 2010-04228 (K.E.K., D.R.M. and M.S.).

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D.S., P.S.C., P.M.R., J.R.-I., B.Y. and W.B.F. conceived and designed experiments. D.S., D.L., Q.-B.L., J.S., J.Y., G.G., M.S., K.E.K., D.R.M. and J.R.-I. performed experiments. D.S., P.S.C., J.R.-I., B.Y., K.E.K., J.Y., D.R.M. and W.B.F. analyzed the data. D.S. and W.B.F. wrote the manuscript, and J.S., M.S., K.E.K., D.R.M., P.S.C., P.M.R., J.R.-I. and B.Y. revised it.

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Correspondence to Davide Sosso.

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Patent applications regarding the use of SWEET genes have been filed.

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Sosso, D., Luo, D., Li, Q. et al. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet 47, 1489–1493 (2015). https://doi.org/10.1038/ng.3422

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