Sugar import mediated by sugar transporters and cell wall invertases for seed development in Camellia oleifera

Abstract

Seed development and yield depend on the transport and supply of sugar. However, an insufficient supply of nutrients from maternal tissues to embryos results in seed abortion and yield reduction in Camellia oleifera. In this study, we systematically examined the route and regulatory mechanisms of sugar import into developing C. oleifera seeds using a combination of histological observations, transcriptome profiling, and functional analysis. Labelling with the tracer carboxyfluorescein revealed a symplasmic route in the integument and an apoplasmic route for postphloem transport at the maternal-filial interface. Enzymatic activity and histological observation showed that at early stages [180-220 days after pollination (DAP)] of embryo differentiation, the high hexose/sucrose ratio was primarily mediated by acid invertases, and the micropylar endosperm/suspensor provides a channel for sugar import. Through Camellia genomic profiling, we identified three plasma membrane-localized proteins including CoSWEET1b, CoSWEET15, and CoSUT2 and one tonoplast-localized protein CoSWEET2a in seeds and verified their ability to transport various sugars via transformation in yeast mutants and calli. In situ hybridization and profiling of glycometabolism-related enzymes further demonstrated that CoSWEET15 functions as a micropylar endosperm-specific gene, together with the cell wall acid invertase CoCWIN9, to support early embryo development, while CoSWEET1b, CoSWEET2a, and CoSUT2 function at transfer cells and chalazal nucellus coupled with CoCWIN9 and CoCWIN11 responsible for sugar entry in bulk into the filial tissue. Collectively, our findings provide the first comprehensive evidence of the molecular regulation of sugar import into and within C. oleifera seeds and provide a new target for manipulating seed development.

Acknowledgements

We are grateful to Dr. Si Ma from the College of Horticulture, China Agricultural University for her guidance in the experiment of in situ hybridization. We also thank professor Jinxing Lin from Beijing Forestry University for his valuable advice in this paper and Dr. Qinsong Yang for his guidance on the experiments. This work was supported by the National Natural Science Foundation of China (grant number 32071798 to L.Z.).

Date availability

All relevant data in this study can be found in the article and its supporting files.

Conflict of interest statement

There are no competing interests in this paper, and the authors do not have any possible conflict of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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