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Sugar transport played a more important role than sugar biosynthesis in fruit sugar accumulation during Chinese jujube domestication

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Abstract

Main conclusion

Sugar transport, including the symplasmic pathway in plasmodesmata and apoplasmic pathway mediated by sugar transporters, accelerated sugar accumulation in cultivated jujube, while sugar metabolism-related genes played weak roles in jujube domestication.

The fruit of Chinese jujube (Ziziphus jujuba Mill.) is high in sugar concentration. By contrast, wild type-sour jujube (Z. jujuba Mill. var. spinosa Hu) contains markedly less sugar. It is unknown whether sugar transport or sugar metabolism drove sugar accumulation during jujube domestication. Using a combination of ultrastructural observations, phylogenetic analysis, testing for soluble sugars, and transcriptional analysis, the sugar accumulation mechanism was studied in the developmental stages of cultivated jujube and sour jujube. Our results indicate that the symplasmic transport pathway in plasmodesmata is present in cultivated jujube, but not in sour jujube. Sugar transporter genes have higher frequencies of duplication than sugar metabolism-related genes. Gene expression patterns indicate that sugar transporter genes, especially ZjSUT2, ZjSWEET1, ZjSWEET7, ZjSWEET11, ZjSTP3, and ZjSTP13a, rather than sugar metabolism-related genes showed higher expression levels in cultivated jujube versus sour jujube during fruit sugar accumulation. These findings suggest that sugar transport, including apoplasmic and symplasmic transport, rather than sugar biosynthesis, is associated with the difference in sugar accumulation between jujube and sour jujube, and that it may drive jujube domestication. This study provides valuable genetic information for jujube improvement, and offers new insights into fruit tree domestication related to sugar accumulation.

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Abbreviations

SUT:

Sucrose transporter

STP:

Sugar transporter protein

ERD6:

Early response to dehydration 6

INT:

Inositol transporter

pGlcT:

Plastidic glucose transporter

PLT:

Polyol monosaccharide transporter

TMT:

Tonoplast monosaccharide transporter

VGT:

Vacuolar glucose transporter

SPS:

Sucrose phosphate synthases

SUSY:

Sucrose synthases

(cw, n, v) INV:

(cell wall, neutral, vacuolar) invertase

SE:

Sieve element

CC:

Companion cell

PP:

Phloem parenchyma cell

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Acknowledgements

This work was supported by grants from the National Science and Technology (Grant no. 2013BAD20B03). We thank Zhang Jun and the staff of the Center for Jujube Engineering and Technology of the State Forestry Administration, College of Forestry, Northwest A&F University, for their assistance with sample collection.

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Correspondence to Xingang Li.

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Zhang, C., Bian, Y., Hou, S. et al. Sugar transport played a more important role than sugar biosynthesis in fruit sugar accumulation during Chinese jujube domestication. Planta 248, 1187–1199 (2018). https://doi.org/10.1007/s00425-018-2971-1

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  • DOI: https://doi.org/10.1007/s00425-018-2971-1

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