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Plasma membrane-localized hexose transporter OsSWEET1b, affects sugar metabolism and leaf senescence

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Abstract

Key message

OsSWEET1b is a hexose transporter protein, which localized in cell membranes and interacting with itself to form homodimer and knockout of OsSWEET1b resulted in reduced leaves sugar content and accelerating leaf senescence.

Abstract

In the rice genome, the SWEET gene family contains 21 homologous members, but the role of some of them in rice growth and development is still unknown. The function of the sugar transporter OsSWEET1b protein in rice was identified in this research. Expression analysis showed that the expression levels of OsSWEET1b in leaves were higher than that in other tissues. The hexose transport experiment confirmed that OsSWEET1b has glucose and galactose transporter activity in yeast. Subcellular localization indicates that OsSWEET1b protein was targeted to the plasma membrane and BiFC analysis showed that OsSWEET1b interacts with itself to form homodimers. Functional analysis demonstrated that the ossweet1b mutant plants were have reduced the sucrose, glucose, fructose, starch and galactose contents, and induced carbon starvation-related gene expression, which might lead to carbon starvation in leaves at filling stage. The ossweet1b knockout plants showed decreased chlorophyll content and antioxidant enzyme activity, and increased ROS accumulation in leaves, leading to leaf cell death and premature senescence phenotype at filling stage. In ossweet1b mutants, the leaf senescence-related gene expression levels were increased and the abundance of photosynthesis-related proteins was decreased. Loss of OsSWEET1b were affected the starch, sucrose metabolism and carbon fixation in photosynthetic organelles pathway by RNA-seq analysis. The destruction of OsSWEET1b function will cause sugar starvation, decreased photosynthesis and leaf senescence, which leading to reduced rice yield. Collectively, our results suggest that the OsSWEET1b plays a key role in rice leaves carbohydrate metabolism and leaf senescence.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

This work was supported by National Key R&D Program of China, Rice germplasm precisely evaluation for direct-breeding in east China (No. 2021YFD1200503). The Nanfan special project, CAAS (Grant No. ZDXM2315). The National Natural Science Foundation of China (Grant No. 32188102). Funded by Qian Qian Academician Workstation, and the specific research fund of the innovation platform for academicians of Hainan province (YSPTZX202303). The Key Research and Development Program of Zhejiang Province (2021C02056). The Agricultural Science and Technology Innovation Program (ASTIP). Central Public-interest Scientific Institution Basal Research Fund.

Funding

This work was funded by Zhejiang Provincial Natural Science Foundation of China under Grant (LQ24C130006). The National Key R&D Program of China, Rice germplasm precisely evaluation for direct-breeding in east China (No. 2021YFD1200503). The Qian Qian Academician Workstation, and the specific research fund of the innovation platform for academicians of Hainan province. The Agricultural Science and Technology Innovation Program (ASTIP). The Key Research and Development Program of Zhejiang Province (2021C02056). The Central Public-interest Scientific Institution Basal Research Fund.

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Author notes

  1. Qiang Zhang, Changzhao Chen, and Rui Guo have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou, 310006, Zhejiang, China

    Qiang Zhang, Changzhao Chen, Rui Guo, Xinyu Tao, Mengxing He, Zhiwen Li, Lan Shen, Qing Li, Deyong Ren, Jiang Hu, Li Zhu, Guangheng Zhang & Qian Qian

  2. National Nanfan Research Institute, Chinese Academy of Agricultural Sciences, Sanya, 572000, China

    Qiang Zhang & Qian Qian

  3. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Science, Nanjing, 210008, China

    Xiaofang Zhu & Zhiwen Li

  4. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 310006, Zhejiang, China

    Xinyu Tao

  5. College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, 321004, Zhejiang, China

    Mengxing He

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  1. Qiang Zhang
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Contributions

QZ and QQ: conceived and designed the research; QZ, CZC, RG and MXH: performing the experiments; ZWL, LS, and QL: investigation and data analysis; QZ and CZC: writing the article JH, LZ, GHZ, and DYR providing critical comments to the manuscript.

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Correspondence to Qian Qian.

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Communicated by Li Tian.

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Table S1

. Primers of sequences in this study. Figure S1. Transmembrane domain analysis of OsSWEET1b protein. Figure S2. Glucose and galactose transport capacity of ossweet1b-1 and ossweet1b-2. Figure S3. Phenotypic analysis of ossweet1b-1 and ossweet1b-2 mutant at seedling stage and heading stage. Figure S4. The relative green fluorescence intensity was measured at WT and ossweet1b-1, ossweet1b-2. Each value shows the mean ± SD of three replicates. Asterisks shows significant differences between WT and ossweet1b-1or ossweet1b-2 by Student’s t-test, * P < 0.05. Figure S5. GO and KEGG analysis of DEGs. Figure S6. Phylogenic analysis of SWEET1b proteins in different plants. (RAR 3938 KB)

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Zhang, Q., Chen, C., Guo, R. et al. Plasma membrane-localized hexose transporter OsSWEET1b, affects sugar metabolism and leaf senescence. Plant Cell Rep 43, 29 (2024). https://doi.org/10.1007/s00299-023-03125-3

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