The SnRK2.3

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Soluble sugars are the core components of fruit quality, and the degree of sugar accumulation is largely determined by tonoplast-localized sugar transporters. We previously showed that two classes of tonoplast sugar transporters, MdERDL6 and MdTST1/2, coordinately regulate sugar accumulation in vacuoles. However, the mechanism underlying this coordination remains unknown. Here we discovered that two transcription factors, MdAREB1.1/1.2, regulate MdTST1/2 expression by binding their promoters in apple. The enhanced MdAREB1.1/1.2 expression in MdERDL6-1-overexpression plants resulted in an increase in MdTST1/2 expression and sugar concentration. Further studies established that MdSnRK2.3, whose expression could be regulated by expressing MdERDL6-1, could interact with and phosphorylate MdAREB1.1/1.2, thereby promoting the MdAREB1.1/1.2-mediated transcriptional activation of MdTST1/2. Finally, the orthologous SlAREB1.2 and SlSnRK2.3 exhibited similar functions in tomato fruit as in their apple counterparts. Together, our findings provide insights into the regulatory mechanism of tonoplast sugar transport exerted by SnRK2.3-AREB1-TST1/2 for fruit sugar accumulation.

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All data supporting the findings of this study are available in the main text or the Supplementary Information. Additional data related to this study are available from the corresponding author upon request. All biological materials used in this study are available from the corresponding author on reasonable request. Source data are provided with this paper.

Zhu, L. et al. MdERDL6-mediated glucose efflux to the cytosol promotes sugar accumulation in the vacuole through up-regulating TSTs in apple and tomato. Proc. Natl Acad. Sci. USA 118, e2022788118 (2021).

Article CAS PubMed Google Scholar

Ruan, Y. L. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu. Rev. Plant Biol. 65, 33–67 (2014).

Article CAS PubMed Google Scholar

Wan, H., Wu, L., Yang, Y., Zhou, G. & Ruan, Y. L. Evolution of sucrose metabolism: the dichotomy of invertases and beyond. Trends Plant Sci. 23, 163–177 (2018).

Article CAS PubMed Google Scholar

Braun, D. M. Phloem loading and unloading of sucrose: what a long, strange trip from source to sink. Annu. Rev. Plant Biol. 73, 553–584 (2022).

Article PubMed Google Scholar

Wen, S., Neuhaus, H. E., Cheng, J. & Bie, Z. Contributions of sugar transporters to crop yield and fruit quality. J. Exp. Bot. 73, 2275–2289 (2022).

Article CAS PubMed Google Scholar

Lecourieux, F. et al. An update on sugar transport and signalling in grapevine. J. Exp. Bot. 65, 821–832 (2014).

Article CAS PubMed Google Scholar

Wang, Z. et al. Heterologous expression of the apple hexose transporter MdHT2.2 altered sugar concentration with increasing cell wall invertase activity in tomato fruit. Plant Biotechnol. J. 18, 540–552 (2020).

Article CAS PubMed Google Scholar

Ren, Y. et al. Evolutionary gain of oligosaccharide hydrolysis and sugar transport enhanced carbohydrate partitioning in sweet watermelon fruits. Plant Cell 33, 1554–1573 (2021).

Article PubMed PubMed Central Google Scholar

Jung, B. et al. Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nat. Plants 1, 14001 (2015).

Article CAS PubMed Google Scholar

Deng, J. et al. The calcium sensor CBL2 and its interacting kinase CIPK6 are involved in plant sugar homeostasis via interacting with tonoplast sugar transporter TST2. Plant Physiol. 183, 236–249 (2020).

Article PubMed PubMed Central Google Scholar

Wingenter, K. et al. A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant J. 68, 890–900 (2011).

Article CAS PubMed Google Scholar

Vu, D. P. et al. Vacuolar sucrose homeostasis is critical for plant development, seed properties, and night-time survival in Arabidopsis. J. Exp. Bot. 71, 4930–4943 (2020).

Article CAS PubMed Google Scholar

Hedrich, R., Sauer, N. & Neuhaus, H. E. Sugar transport across the plant vacuolar membrane: nature and regulation of carrier proteins. Curr. Opin. Plant Biol. 25, 63–70 (2015).

Article CAS PubMed Google Scholar

Rodrigues, C. M. et al. Vernalization alters sink and source identities and reverses phloem translocation from taproots to shoots in sugar beet. Plant Cell 32, 3206–3223 (2020).

Article CAS PubMed PubMed Central Google Scholar

Zhang, Q. et al. Evolutionary expansion and functional divergence of sugar transporters in Saccharum (S. spontaneum and S. officinarum). Plant J. 105, 884–906 (2020).

Article PubMed Google Scholar

Aluri, S. & Büttner, M. Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc. Natl Acad. Sci. USA 104, 2537–2542 (2007).

Article CAS PubMed PubMed Central Google Scholar

Poschet, G. et al. A novel Arabidopsis vacuolar glucose exporter is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Physiol. 157, 1664–1676 (2011).

Article CAS PubMed PubMed Central Google Scholar

Schneider, S. et al. Vacuoles release sucrose via tonoplast-localised SUC4-type transporters. Plant Biol. 14, 325–336 (2012).

Article CAS PubMed Google Scholar

Klemens, P. A. et al. Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol. 163, 1338–1352 (2013).

Article CAS PubMed PubMed Central Google Scholar

Guo, W. J. et al. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol. 164, 777–789 (2014).

Article CAS PubMed Google Scholar

Peng, Q. et al. The sucrose transporter MdSUT4.1 participates in the regulation of fruit sugar accumulation in apple. BMC Plant Biol. 20, 191 (2020).

Article CAS PubMed PubMed Central Google Scholar

Furihata, T. et al. Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl Acad. Sci. USA 103, 1988–1993 (2006).

Article CAS PubMed PubMed Central Google Scholar

Li, M. et al. Proteomic analysis reveals dynamic regulation of fruit development and sugar and acid accumulation in apple. J. Exp. Bot. 67, 5145–5157 (2016).

Article CAS PubMed PubMed Central Google Scholar

Liu, Z. et al. Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signalling during cold response. Mol. Cell 66, 117–128 (2017).

Article CAS PubMed Google Scholar

Ruan, Y. L., Patrick, J. W. & Brady, C. Protoplast hexose carrier activity is a determinate of genotypic difference in hexose storage in tomato fruit. Plant Cell Environ. 20, 341–349 (1997).

Article CAS Google Scholar

Ren, Y. et al. A tonoplast sugar transporter underlies a sugar accumulation QTL in watermelon. Plant Physiol. 176, 836–850 (2018).

Article CAS PubMed Google Scholar

Wipf, D. et al. Identification of putative interactors of Arabidopsis sugar transporters. Trends Plant Sci. 26, 13–22 (2021).

Article CAS PubMed Google Scholar

Mou, W. et al. SlAREB1 transcriptional activation of NOR is involved in abscisic acid-modulated ethylene biosynthesis during tomato fruit ripening. Plant Sci. 276, 239–249 (2018).

Article CAS PubMed Google Scholar

Rook, F., Hadingham, S. A., Li, Y. & Bevan, M. W. Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ. 29, 426–434 (2006).

Article CAS PubMed Google Scholar

Ma, Q. J. et al. Transcription factor AREB2 is involved in soluble sugar accumulation by activating sugar transporter and amylase genes. Plant Physiol. 174, 2348–2362 (2017).

Article CAS PubMed PubMed Central Google Scholar

Yakir, E. et al. MaMADS2 repression in banana fruits modifies hormone synthesis and signalling pathways prior to climacteric stage. BMC Plant Biol. 18, 267 (2018).

Article CAS PubMed PubMed Central Google Scholar

Fujita, Y. et al. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50, 2123–2132 (2009).

Article CAS PubMed Google Scholar

Fujita, Y., Yoshida, T. & Yamaguchi-Shinozaki, K. Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol. Plant. 147, 15–27 (2013).

Article CAS PubMed Google Scholar

Yang, J. et al. Response of sugar metabolism in apple leaves subjected to short-term drought stress. Plant Physiol. Biochem. 141, 164–171 (2019).

Article CAS PubMed Google Scholar

Wang, Z. et al. Variation in the promoter of the sorbitol dehydrogenase gene MdSDH2 affects binding of the transcription factor MdABI3 and alters fructose content in apple fruit. Plant J. 109, 1183–1198 (2022).

Article CAS PubMed Google Scholar

Fürtauer, L., Weckwerth, W. & Nagele, T. A benchtop fractionation procedure for subcellular analysis of the plant metabolome. Front. Plant Sci. 7, 1912 (2016).

Article PubMed PubMed Central Google Scholar

Beshir, W. F. et al. Non-aqueous fractionation revealed changing subcellular metabolite distribution during apple fruit development. Hortic. Res. 6, 98 (2019).

Article PubMed PubMed Central Google Scholar

Zhang, L. et al. MdWRKY126 modulates malate accumulation in apple fruit by regulating cytosolic malate dehydrogenase (MdMDH5). Plant Physiol. 188, 2059–2072 (2022).

Article CAS PubMed PubMed Central Google Scholar

Ma, S. et al. F-box protein MdAMR1L1 regulates ascorbate biosynthesis in apple by modulating GDP-mannose pyrophosphorylase. Plant Physiol. 188, 653–669 (2022).

Article CAS PubMed Google Scholar

Jia, M. et al. SnRK2 subfamily I protein kinases regulate ethylene biosynthesis by phosphorylating HB transcription factors to induce ACO1 expression in apple. New Phytol. 234, 1262–1277 (2022).

Article CAS PubMed PubMed Central Google Scholar

Liu, C., Yu, H., Rao, X., Li, L. & Dixon, R. A. Abscisic acid regulates secondary cell-wall formation and lignin deposition in Arabidopsis thaliana through phosphorylation of NST1. Proc. Natl Acad. Sci. USA 118, e2106367118 (2021).

Article Google Scholar

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We thank J. Zhang and J. Zhao (Horticulture Science Research Center, Northwest A&F University, Yangling, China) for providing professional technical assistance with GC–MS analysis; H. Zhao and F. Yuan (State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, China) and Y. Yuan and R. Chen (Horticulture Science Research Center, Northwest A&F University, Yangling, China) for providing confocal microscopy experimental assistance. This work was supported by the Program for the National Natural Science Foundation of China (31872043) to M.L., the Shaanxi Science and Technology Innovation Team Project (2022TD-18) to M.L., the Australian Research Council (DP180103834) to Y.-L.R., and the Earmarked Fund for the China Agriculture Research System (CARS-27) to F.M.

These authors contributed equally: Lingcheng Zhu, Yanzhen Li.

State Key Laboratory of Crop Stress Biology in Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Xianyang, China

Lingcheng Zhu, Yanzhen Li, Chengcheng Wang, Zhiqi Wang, Wenjing Cao, Jing Su, Yunjing Peng, Baiyun Li, Baiquan Ma, Fengwang Ma, Yong-Ling Ruan & Mingjun Li

College of Life Science, Northwest A&F University, Xianyang, China

Lingcheng Zhu

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory, Australia

Yong-Ling Ruan

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L.Z., M.L., F.M. and Y.-L.R. designed this research. L.Z., Y.L., C.W., Z.W., J.S., Y.P., B.L., W.C. and B.M. performed the experiments. L.Z., J.S., Y.L., M.L. and Y.-L.R. analysed the data. L.Z., M.L. and Y.-L.R. wrote the paper. M.L. and F.M. supervised the study. All authors read and approved the final paper.

Correspondence to Fengwang Ma, Yong-Ling Ruan or Mingjun Li.

The authors declare no competing interests.

Nature Plants thanks Jintao Cheng, Li-Qing Chen and H. Ekkehard Neuhaus for their contribution to the peer review of this work.

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a, b, Relative distribution of compartment-specific markers in MdERDL6-1 overexpressed apple leaves (a) and tomato fruits (b). Tissues were fractionated using a NAF procedure and the activities of marker enzymes in the five fractions were determined. Data are expressed as percentage activities in each fraction. AGPase, UGPase, and ACP were used as plastidic, cytosolic, and vacuolar markers, respectively. c, d, Subcellular concentrations of Glc, Fru, and Suc in plastid, cytosol, and vacuole fractions of MdERDL6-1 overexpressed apple leaves (c) and tomato fruits (d). nd, no data. The bars represent the mean value ± SD (n = 3 independent biological replicates). The asterisks in (c,d) indicate significant differences as assessed by Student's t-test (two-sided). ***P < 0.001, **P < 0.01, *P < 0.05, ns, not significant.

Source data

a, Differentially expressed transcription factors in the RNA-seq of MdERDL6-1 transgenic apples. The threshold was set as: RPKM > 1, fold change > 1.5. b, c, Predicted active transcription factors regulate MdTST1 (b) and MdTST2 (c) expression based on ATAC-seq in apple fruit. d, The ABRE element analysis on MdTST1/2 promoters. e, qRT-PCR validation of three differential transcription factors in the RNA-seq of MdERDL6-1 transgenic apples. The transcript levels were normalized with those of MdActin in transgenic apple. Relative expression levels for each gene were obtained via ddCT method, with the expression in wild type (WT) set as ‘1’.The bars represent the mean value ± SD (n = 3 seedlings). The asterisks in (e) indicate significant differences as assessed by Student's t-test (two-sided). ***P < 0.001, **P < 0.01, ns, not significant.

Source data

a, b, The impacts of sugars feeding on MdSnRK2.3 and MdAREB1.1/1.2 expression levels. Apple calli was cultured on MS liquid medium with 2% different exogenous sugars (Water was used as control) and different concentrations of Glc for 24 h, and the gene expression levels were detected by qRT-PCR. The transcript levels were normalized with those of MdActin. Relative expression level was obtained via ddCT method, setting the expression level in water feeding as ‘1’. c, d, The impacts of sugars feeding on MdAREB1.1/1.2 promoter activities. Apple calli was cultured on MS liquid medium with different exogenous sugars and different concentrations of Glc for 24 h after infiltrating with Agrobacterium harboring MdAREB1.1/1.2pro-GUS plasmids. The treated and control apple calli were harvested for GUS activity assay after 24 h feeding. The 1924bp and 1937bp promoters of MdAREB1.1 and MdAREB1.2 were used in the GUS experiments. Man: mannose; Glc: glucose; Fru: fructose; Suc: sucrose; and Sor: sorbitol. Bars represent the mean value ± SD (n = 3 independent biological replicates). Different letters indicate significant differences as assessed by one-way ANOVA (Tukey's test), respectively (P < 0.05).

Source data

a, Phylogenetic tree of MdAREBs from apple and the orthologous genes from Arabidopsis and tomato. The AREB orthologous sequences were collected to build an un-rooted phylogenetic tree using the neighbour-joining method of the MEGA7 software. A 1000 trial of bootstrap analysis was used to provide confident estimates for phylogenetic tree topology. The colored circles are studied genes in this research. The scale bar corresponds to 0.05. b, Nuclear localization of MdAREB1.1/1.2. 35Spro:MdAREB1.1/1.2-GFP were transiently expressed in protoplasts of Arabidopsis leaves. DAPI served as a nuclear dye. The GFP signals of MdAREB1.1/1.2 overlapped with DAPI, indicating that MdAREB1.1/1.2 localized in the nuclear. Scale bars, 20 μm. c, The transcriptional self-activation assay of MdAREB1.1/1.2. The pGBKT7-MdAREB1.1/1.2 and empty pGBKT7 vector (negative control) were introduced into the yeast strain Y2H respectively, and the transformed cells were spotted on SD-Trp and SD-Trp-His-Leu+x-α-Gal medium. The plates were incubated at 30 °C for 3 d. d, The heat map of MdAREBs expression levels based on RNA-seq in mature leaves (ML) and five stages of developing fruits (S1-S5). Fold difference is designated as a log2 value, with the data in S1 set as 1. The experiments in (b, c) were repeated independently at least three times, with similar results.

Source data

a, The complete coding sequences of MdAREB1.1 or MdAREB1.2 were inserted into the pMDC83 vector for gene stable overexpression (OE-MdAREB1.1#1, #2; OE-MdAREB1.2#1, #2), while the specific cDNA fragments were cloned into pK7GWIWG2 vector for gene stable silencing (PK7-MdAREB1.1#1, #2; PK7-MdAREB1.2#1, #2). The empty vectors pMDC83 and PK7 served as controls respectively. b, The mRNA relative expression levels of MdAREB1.1/1.2 and MdTST1/2 in transgenic apple calli, setting that from pMDC83 as ‘1’. c, The sugar concentrations (Fru, fructose; Glc, glucose; Suc, sucrose) in transgenic apple calli. The bars represent the mean value ± SD (n = 3 independent biological replicates). Different letters indicate significant differences as assessed by one-way ANOVA (Tukey's test) (P < 0.05).

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a, Phylogenetic analysis of MdSnRK2s from apple and the orthologous genes from Arabidopsis and tomato. The SnRK2s orthologous sequences were collected to build an un-rooted phylogenetic tree using the neighbour-joining method of the MEGA7 software, which was obviously clustered into three subclasses. A 1000 trial of bootstrap analysis was used to provide confident estimates for phylogenetic tree topology. The colored circles are studied genes in this research. The scale bar corresponds to 0.05. b, The heat map of MdSnRK2s expression levels based on RNA-seq in MdERDL6-1 overexpressing apple lines. Fold difference is designated as a log2 value, with the data in WT set as 1. c, The protein abundances (quantified proteins) of MdSnRK2.1/2.3/2.5 are extracted from tandem mass tags (TMT) quantitative proteomics of five developing stages of apple fruits. The bars represent the mean value ± SD (n = 3 independent biological replicates). d, Subcellular localization of MdSnRK2.3-GFP fusion protein in the protoplasts from Arabidopsis leaves. GFP, green fluorescent protein. DAPI (4’,6-diamidino-2-phenylindole) was used to stain the nucleus. Auto, the red auto fluorescence of chloroplasts. Bar = 20 μm. The experiments in (d) were repeated independently at least three times, with similar results.

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a, b, Yeast one-hybrid assays showed that MdAREB1.1/1.2 and SlAREB1.2 bound to their own promoters containing ABRE cis-elements. Schematic diagram of P1 and P2 truncation promoters with or without ABRE cis-elements, the vertical lines represent ABRE cis-elements (a). The positive controls were pAbAi-P53 and pGADT7-53. The screening concentration of AbA were 150 ng/mL, 180 ng/mL, and 200 ng/mL of MdAREB1.1, MdAREB1.2, and SlAREB1.2 promoters respectively. Each colony was dissolved in 5 μL sterile NaCl and then diluted to 10−1 to 10−3. c, Dual-luciferase assays in tobacco (N. benthamiana) leaves revealed that MdAREB1.1/1.2 and SlAREB1.2 binding to their own promoters. The left are the dual-luciferase signal imagings, and the right are dual-luciferase activity assays. The 1924bp and 1937bp promoters of MdAREB1.1 and MdAREB1.2, 1911bp promoter of SlAREB1.2 were used in this assay. The positive controls are pGreenII 0800-LUC-P53 and pGreenII 62-SK-53. The experiments were repeated independently at least three times, with similar results.

a, The fruits of transgenic tomato lines (overexpression lines: OE#2, OE#5; silence lines: PK7#1, PK7#3). b, c, The relative expression levels of SlAREB1.2 and SlTST1/2 in the transgenic tomato measured using qRT-PCR and normalized to those of SlActin, setting that from WT as ‘1’. d, e, The soluble solids contents and carbohydrate levels in ripening fruits of transgenic tomato. Glc, glucose; Fru, fructose; Suc, sucrose. The bars represent the mean value ± SD (n = 3 independent biological replicates). The asterisks indicate significant differences as assessed by Student's t-test (two-sided). ***P < 0.001, **P < 0.01, *P < 0.05.

Source data

a, The Agrobacterium containing the resulting vectors pTRV2-SlAREB1.2 and pTRV1 were mixed in equal proportions, which were used for injection in two MdERDL6-1 overexpressing tomato lines (OE1-pTRV#SlAREB1.2 and OE2-pTRV#SlAREB1.2), with empty pTRV2 and pTRV1 mixture for injection as controls (WT, OE-1, and OE-2). The arrows indicate the injection sites in fruits. b, The mRNA relative expression levels of SlAREB1.2 and SlTST1/2 in transgenic tomato fruits of wild-type and MdERDL6-1 overexpressed background, setting that from WT as ‘1’. c, The sugar concentrations (Fru, fructose; Glc, glucose; Suc, sucrose) in transgenic tomato fruits of wild-type and MdERDL6-1 overexpressed background. The bars represent the mean value ± SD (n = 3 independent biological replicates). Different letters indicate significant differences as assessed by one-way ANOVA (Tukey's test) (P < 0.05).

Source data

a, The Agrobacterium containing the resulting vectors pTRV2-SlSnRK2.3 and pTRV1 were mixed in equal proportions, which were used for injection in two MdERDL6-1 overexpressing tomato lines (OE1-pTRV#SlSnRK2.3 and OE2-pTRV#SlSnRK2.3), with empty pTRV2 and pTRV1 mixture for injection as controls (WT, OE-1, and OE-2). The arrows indicate the injection sites in fruits. b, The mRNA relative expression levels of SlSnRK2.3, SlAREB1.2 and SlTST1/2 in transgenic tomato fruits of wild-type and MdERDL6-1 overexpressed background, setting that from WT as ‘1’. c, The sugar concentrations (Fru, fructose; Glc, glucose; Suc, sucrose) in transgenic tomato fruits of wild-type and MdERDL6-1 overexpressed background. The bars represent the mean value ± SD (n = 3 independent biological replicates). Different letters indicate significant differences as assessed by one-way ANOVA (Tukey's test) (P < 0.05).

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Zhu, L., Li, Y., Wang, C. et al. The SnRK2.3-AREB1-TST1/2 cascade activated by cytosolic glucose regulates sugar accumulation across tonoplasts in apple and tomato. Nat. Plants (2023). https://doi.org/10.1038/s41477-023-01443-8

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Received: 09 December 2022

Accepted: 12 May 2023

Published: 08 June 2023

DOI: https://doi.org/10.1038/s41477-023-01443-8

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