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Phosphorylation of SWEET sucrose transporters regulates plant root:shoot ratio under drought

Abstract

The root:shoot ratio has long been known to be enhanced in plants under drought stress. Here we discovered that osmotic stress enhances long-distance sucrose transport to increase the root:shoot ratio in an abscisic-acid-dependent manner. The Arabidopsis sucrose transporters SWEET11 and 12, key players in phloem loading, are rapidly phosphorylated upon drought and abscisic acid treatments. The drought- and abscisic-acid-activated SnRK2 protein kinases phosphorylate the carboxy-terminal cytosolic regions of SWEET11 and 12. This phosphorylation enhances the oligomerization and sucrose transport activity of SWEETs, which results in elevated sucrose contents in roots and improved root growth under drought stress, leading to the enhanced root:shoot ratio of biomass and drought resistance. Notably, the expression of phospho-mimic SWEETs led to improved root growth even under non-stressed conditions. The phosphorylation of sucrose transporters provides an explanation for the long-standing observation that drought stress enhances the root:shoot ratio in plants and suggests a strategy for engineering drought-resistant crops.

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Fig. 1: ABA and sucrose transport regulate root growth under osmotic stress.
Fig. 2: SnRK2s interact with SWEET11 and SWEET12.
Fig. 3: SWEET11 and 12 are phosphorylated by SnRK2s under osmotic stress.
Fig. 4: Phosphorylation of SWEET11 and 12 enhances sucrose transport.
Fig. 5: Phosphorylation of SWEET11 and 12 controls root growth under osmotic stress.
Fig. 6: Schematic model for SnRK2- and SWEET-mediated root growth under drought stress.

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All materials are available from the corresponding author upon request. Source data are provided with this paper.

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Acknowledgements

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB27040107), the National Natural Science Foundation of China (NSFC grant no. 31970293) and the Shanghai Center for Plant Stress Biology, Chinese Academy of Sciences.

Author information

Authors and Affiliations

Authors

Contributions

Y.Z. conceived and designed the research. Q.C., T.H. and X.L. performed the experiments. Q.C., Y.Z., L.C., C.-P.S. and J.-K.Z. analysed the results. Y.Z., Q.C. and L.C. wrote the manuscript.

Corresponding author

Correspondence to Yang Zhao.

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The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Shuhua Yang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Reduced root growth and root sugar levels in ABA insensitive mutants and sweet11/12 mutant under osmotic stress.

a, Fresh weight of roots from Col-0 wild-type, pyl duodecuple (pyl), snrk2.2/3/6 (snrk2) and sweet11/12 mutants, and SWEETpro::SWEET-HA transgenic plants expressing wild-type SWEET11 or 12 in the sweet11/12 mutant background, without or with mannitol, PEG or ABA treatments. b, Sucrose contents in roots of Col-0 wild-type, pyl duodecuple (pyl), snrk2.2/3/6 (snrk2) and sweet11/12 mutants, and SWEETpro::SWEET-HA transgenic plants expressing wild-type SWEET11 or 12 in the sweet11/12 mutant background, without or with mannitol or ABA treatments. c-d, Root growth of Col-0 wild-type, snrk2.2/3/6 (snrk2) and pyl duodecuple (pyl) mutants, grown on mannitol plates with (right panel) or without (left panel) exogenous sucrose. The primary root length was quantified (d). e-f, Glucose (e) and fructose (f) levels in roots of Col-0 wild-type, pyl duodecuple (pyl), snrk2.2/3/6 (snrk2) and sweet11/12 mutants, without or with mannitol or ABA treatments. g-h, Root growth of Col-0 wild-type and sweet11/12 mutant grown on mannitol plates with (right panel) or without (left panel) exogenous sucrose. The primary root length was quantified (h). Error bars indicate SEM (n = 10 seedlings) in (a, d, h), SEM (n = 5 seedlings) in (b) and SEM (n = 3 seedlings) in (e, f). Student’s t-test (two-sided). ‘a,’ ‘b,’ and ‘c’, significance evaluated by post hoc Tukey test after one way ANOVA (p < 0.05). The experiments in (c and g) were repeated independently at least three times with similar results.

Source data

Extended Data Fig. 2 SnRK2s interact with and phosphorylate SWEET11 and 12.

a, SnRK2s are co-immunoprecipitated with SWEET12 in SWEET12pro::SWEET12-GFP transgenic plants. SWEET12 protein was immunoprecipitated using SWEET12pro::SWEET12-GFP transgenic plants treated without or with 100 μM ABA. b, Coimmunoprecipitation (coIP) assay in Arabidopsis protoplast. Total proteins were extracted from protoplasts co-transfected with HA-SnRK2.6 and FLAG-SWEET11, FLAG-SWEET12 or FLAG empty vector control, and immunoprecipitated using anti-FLAG beads. Coimmunoprecipitated HA-SnRK2.6 was detected with anti-HA antibody. The experiments in (b) were repeated independently at least two times with similar results.

Source data

Extended Data Fig. 3 SnRK2s phosphorylate SWEET11 and 12.

a, Phosphopeptides containing Ser248 from the C-terminus of SWEET12 were detected in SWEET12pro::SWEET12-GFP transgenic plants following ABA treatment. ‘pep score’, peptide score, which determines the probability that the peptide fragments detected by the mass spectrum. b, Phosphorylation of Ser248 of SWEET11 and 12 in Col-0 wild-type and sweet11/12 mutant seedlings, with or without mannitol or ABA treatment. Anti-SWEET11P and anti-SWEET12P indicate anti-phospho-Ser248-SWEET11 and 12 antibodies, respectively. Anti-phospho-Ser248-SWEET11 and 12 antibodies were used to detect phosphorylation of SWEET11 and 12, respectively. Actin was used as a loading control. c,d, Protein abundance of HA-tagged SWEET11 and SWEET12 in SWEET11pro::SWEET11-HA (c) and SWEET12pro::SWEET12-HA (d) transgenic plants. Anti-HA antibody was used for western blot. Total proteins were detected by Ponceau S staining. e-f, Phosphorylation of SWEET11 and SWEET12 under mannitol or ABA treatment in SWEET11pro::SWEET11-HA (e) and SWEET12pro::SWEET12-HA (f) transgenic plants. Total proteins were separated in a Phos-tag gel, and HA-tagged SWEET were detected with anti-HA antibody. g, Phosphorylation of SWEET11 and SWEET12 under ABA treatment in protoplasts of Col-0 and snrk2.2/3/6 (snrk2). Total proteins were separated in a Phos-tag gel, and FLAG-tagged SWEET were detected with an anti-FLAG antibody. Actin was used as a loading control. The experiments in (b-g) were repeated independently at least two times with similar results.

Source data

Extended Data Fig. 4 Phosphorylation enhances oligomerization of SWEET11 and 12.

a, Prediction of cytosolic regions in SWEET11 and SWEET12 proteins using TMHMM Server v. 2.0. b-c, Result matrix of homo- and hetero-oligomerization between combinations of wild-type, phospho-mimic (S-to-D/E) or non-phosphorylatable (S-to-A) SWEET11 and 12 LUC-fusion proteins without (left half of box) or with (right half of box) ABA treatment in protoplasts of sweet11/12 (b) and snrk2.2/3/6 (snrk2) mutants (c). The strength of the interaction is categorized from light blue to dark red as indicated below or to the right of the matrix. We define the hetero-interaction strength of wild type SWEET11 and SWEET12 as n.s., and determines the interaction strength of other combinations according to the mathematical multiple relation with n.s.. No experiment was conducted with combinations depicted as an empty box. The right histogram in (b) shows the illustrative rough data. Error bars indicate SEM (n = 3 biologically independent samples). d-e, Interactions between C-terminal and internal cytosolic regions of SWEETs in the yeast two-hybrid assay. Interactions was determined by yeast growth in media lacking Leu, Trp and His (-L-W-H) with dilutions (10−1, 10−2, and 10−3) of saturated cultures.

Source data

Extended Data Fig. 5 Genotyping of SWEETpro::SWEETs-HA transgenic plants.

a, Schematic representation of the SWEET11 and 12 loci and the respective T-DNA insertion sites. Genomic DNA sequence (upper panel) and protein sequence (lower panel). b, Amplification of native SWEET11 and SWEET12 in SWEETpro:: SWEET-HA transgenic plants in sweet11/12 mutant background using primers that bind to the 3’UTR of SWEETs as reverse primers. Col-0 wild-type, and sweet11, sweet12 and sweet11/12 mutants were used as controls. c, Amplification of recombinant SWEET11 and SWEET12 in SWEETpro:: SWEET-HA transgenic plants in sweet11/12 mutant background using a primer binding to HA as reverse primer. d, Sanger sequencing chromatograms indicate mutations on SWEETs. The experiments in (b, c) were repeated independently at least two times with similar results.

Extended Data Fig. 6 Phosphorylation of SWEET11 and 12 Enhances Sucrose transport and accumulation in Roots.

a,b, Protein abundance of wild-type and mutated SWEET11 (a) and SWEET12 (b) in protoplasts without or with 5 μM ABA treatment overnight. Anti-FLAG antibody was used to detect SWEET11 and 12. Actin was used as a loading control. c-d, Protein abundance of SWEET11 and 12 in SWEETpro::SWEET-HA transgenic plants, without or with 20 μM ABA (c) or 200 mM mannitol (d) treatments for the indicated time points. Anti-HA antibody was used to detect SWEET11 and 12. Actin was used as a loading control. e, Sucrose levels in phloem exudates of Col-0 wild-type, sweet11/12 mutant, and SWEET12pro::SWEET12-HA transgenic plants expressing wild-type and mutated SWEET12 in the sweet11/12 mutant background, with or without ABA treatment. f, Sucrose levels in roots of Col-0 wild-type, sweet11/12 mutant and SWEETpro::SWEET-HA transgenic plants expressing wild-type and mutated SWEET11 and SWEET12 in the sweet11/12 mutant background, without or with mannitol or ABA treatments. Error bars indicate SEM (n = 3 biologically independent samples) in (e), and SEM (n = 5 seedlings) in (f). Student’s t-test (two-sided). The experiments in (a-d) were repeated independently at least two times with similar results.

Source data

Extended Data Fig. 7 Phosphorylation of SWEET11 contributes to root growth under osmotic stress.

Root growth of Col-0 wild-type, sweet11/12 mutant and SWEETpro::SWEET-HA transgenic plants expressing wild-type and mutated SWEETs in the sweet11/12 mutant background, grown on mannitol plates with (right panel) or without (left panel) exogenous sucrose. The primary root length was quantified (b). Values are mean ± SEM (n = 15 seedlings). ‘a,’ ‘b,’ and ‘c’, significance evaluated by post hoc Tukey test after one way ANOVA (p < 0.05). The experiments in (a) were repeated independently at least three times with similar results.

Source data

Extended Data Fig. 8 Phosphorylation of SWEET11 contributes to root growth under drought stress.

a, Vertical sections of representative root systems of Col-0 wild-type, sweet11/12 mutant, and SWEET11pro::SWEET11-HA transgenic plants expressing wild-type and mutated SWEET11 in the sweet11/12 mutant background, grown in well-watered or arid soil for 30 days. Red lines: traced roots from the image; red bars, 5 cm. The experiments in (a) were repeated independently at least three times with similar results. b-e, Fresh and dry weight in roots (b,d) and shoots (c,e) of Col-0 wild-type, sweet11/12 mutant and SWEET11pro::SWEET11-HA transgenic plants expressing wild-type and mutated SWEET11 in the sweet11/12 mutant background, without or with mannitol, PEG or ABA treatments. Error bars indicate SEM (n = 10 seedlings). Student’s t-test (two-sided). f, Representative images of Col-0 wild-type, sweet11/12 mutant and SWEET11pro::SWEET11-HA transgenic plants expressing wild-type and mutated SWEET11 in the sweet11/12 mutant background, grown under drought stress in soil. Water was withheld from 10-day-old Arabidopsis plants for 21 d under short-day conditions. The experiments in (f) were repeated independently at least three times with similar results.

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Supplementary Tables 1–3.

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Supplementary Data 1

IP-MS data for SWEET12.

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Unprocessed western blots.

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Chen, Q., Hu, T., Li, X. et al. Phosphorylation of SWEET sucrose transporters regulates plant root:shoot ratio under drought. Nat. Plants 8, 68–77 (2022). https://doi.org/10.1038/s41477-021-01040-7

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