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CsHT11 encodes a pollen-specific hexose transporter and is induced under high level sucrose in pollen tubes of cucumber (Cucumis sativus)

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Abstract

Pollen tubes require a high amount of sugars to sustain high growth rate. Sucrose, the main transport form of sugars, can serve as energy supply and as signaling molecules for pollen tube growth. We report the functional characterization of CsHT11, which is a sugar transporter protein/hexose transport protein (STP/HT). CsHT11 shares high homology with the characterized cucumber hexose transporter CsHT1, a pollen-specific gene. Analysis of CsHT11 mRNA and CsHT11 promoter-reporter gene studies revealed CsHT11 specifically expressed in pollen and pollen tubes. Subcellular localization indicated that CsHT11 is a plasma membrane transporter. Heterologous expression in yeast suggests that CsHT11 is an energy-dependent hexose/H+ symporter, with a wide variety of substrate specificity, including glucose, fructose, galactose, and mannose. In vitro pollen germination of different sugars shows that the expression of CsHT11 is significantly increased with higher sucrose content, but not with higher glucose or fructose content, thereby implying that CsHT11 may be involved in sucrose signal transduction. Thus, CsHT11 might have an essential effect on pollen development and pollen tube growth in cucumber.

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Abbreviations

HT:

Hexose transport protein

STP:

Sucrose transport protein

SWEETs:

Sugars will eventually be exported transports

SUC/SUT:

Sucrose transport protein

CWINV:

Cell wall invertases

VIN:

Vacuolar invertase

SuSy:

Sucrose synthase

Glc:

Glucose

Fru:

Fructose

Suc:

Sucrose

Man:

Mannose

Mat:

Mannitol

HXK:

Hexokinase

Gal:

Galactose

Man:

Mannose

GUS:

β-Glucuronidase

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Acknowledgements

We thank Fareeha Shireen for helpful discussions. This work was supported by the National Key Research and Development Program of China (2019YFD1000300) to Jintao Cheng, the National Natural Science Foundation of China (31972435 and 31601774) to Jintao Cheng and the Fundamental Research Funds for the Central Universities (2662018QD062) to Jintao Cheng.

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  1. College of Horticulture and Forestry Sciences, Huazhong Agricultural University and Key Laboratory of Horticultural Plant Biology, Ministry of Education, Wuhan, 430070, People’s Republic of China

    Suying Wen, Tianyang Bao, Xiangwei Zeng, Zhilong Bie & Jintao Cheng

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  1. Suying Wen
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  2. Tianyang Bao
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  3. Xiangwei Zeng
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JTC designed research. JTC and ZLB found the experiments. SYW, TYB and XWZ conducted experiments. SYW analyzed data and wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Jintao Cheng.

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Supplementary Fig. S1. Membrane-spanning model of CsHT11 by TMHMM. (TIF 1653 kb)

10725_2020_573_MOESM2_ESM.tif

Supplementary Fig. S2 Comparison of CsHT11 amino acid sequences. The protein sequence of CsHT11 is compared with protein sequences of previously-characterized pollen-specific monosaccharide transporters CsHT1, AtSTP2, 4, 6, 9 ,10, and AtSTP11 from Arabidopsis. Black boxes indicate identical amino acid residues. Dark gray boxes represent amino acid residues with identity of more than 50%. Light gray boxes represent similarity of more than 50%. Black bars indicate transmembrane domains of CsHT11 predicted by SOAP program in PCgene. The sequence alignment was performed using DNAMAN software package. The GenBank accession numbers of the sequences used for the analyses, as shown in Supplementary Table S1. (TIF 6536 kb)

10725_2020_573_MOESM3_ESM.tif

Supplementary Fig. S3. Spatiotemporal expression analysis of CsHT11 in different cucumber tissues. RPKM: normalized reads per million sequences. Project: PRINA80169. Data from the database of cucurbitgenomics (http://cucurbitgenomics.org/) (TIF 370 kb)

Supplementary Table S1. The GenBank accession numbers of the sequences used for the analysis in Fig. 1. (PDF 369 kb)

10725_2020_573_MOESM5_ESM.pdf

Supplementary Table S2. Primers used in the paper. The restriction enzyme sites or recombination connector sequence are underlined. (PDF 459 kb)

10725_2020_573_MOESM6_ESM.pdf

Supplementary Table S3. Potential cis-acting regulatory elements identified in promoter regions of CsHT11 genes. (PDF 544 kb)

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Wen, S., Bao, T., Zeng, X. et al. CsHT11 encodes a pollen-specific hexose transporter and is induced under high level sucrose in pollen tubes of cucumber (Cucumis sativus). Plant Growth Regul 90, 237–248 (2020). https://doi.org/10.1007/s10725-020-00573-9

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