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In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin

Abstract

Plants have evolved sophisticated systems in response to environmental changes, and growth arrest is a common strategy used to enhance stress tolerance. Despite the growth–survival trade-off being essential to the shaping of plant productivity, the mechanisms balancing growth and survival remain largely unknown. Aquaporins play a crucial role in growth and stress responses by controlling water transport across membranes. Here, we show that RhPIP2;1, an aquaporin from rose (Rosa sp.), interacts with a membrane-tethered MYB protein, RhPTM. Water deficiency triggers nuclear translocation of the RhPTM C terminus. Silencing of RhPTM causes continuous growth under drought stress and a consequent decrease in survival rate. RNA sequencing (RNA-seq) indicated that RhPTM influences the expression of genes related to carbohydrate metabolism. Water deficiency induces phosphorylation of RhPIP2;1 at Ser 273, which is sufficient to promote nuclear translocation of the RhPTM C terminus. These results indicate that the RhPIP2;1-RhPTM module serves as a key player in orchestrating the trade-off between growth and stress survival in Rosa.

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Fig. 1: RhPIP2;1 interacts with RhPTM.
Fig. 2: Dehydration stimulates nuclear accumulation of the RhPTM C-terminal region.
Fig. 3: Silencing of RhPTM in rose enhances growth.
Fig. 4: Silencing of RhPTM reduces tolerance of rose plants to drought stress.
Fig. 5: RhPTM influences expression of genes related to carbohydrate metabolism and signalling of auxin and cytokinin in rose plants.
Fig. 6: Nuclear translocation of RhPTM CEND is regulated by phosphorylation of RhPIP2;1.

Data availability

The data that support the findings of this study are available from the corresponding author upon request. All primers used in this study are described in Supplementary Table 3. Information on the genes used in this study is given in Supplementary Table 4. RNA-Seq data that support the findings of this study have been deposited in the NCBI Bioproject database under the accession number PRJNA486271 (https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA486271). The proteomic data of validation for anti-RhPTM antibody and RhPIP2;1 phosphorylation have been deposited in the PRIDE archive (Nos. PXD011942 and PXD011943, respectively; https://www.ebi.ac.uk/pride/archive).

References

  1. 1.

    Achard, P. et al. Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94 (2006).

    CAS  Article  Google Scholar 

  2. 2.

    Claeys, H. & Inze, D. The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol. 162, 1768–1779 (2013).

    CAS  Article  Google Scholar 

  3. 3.

    Sharp, R. E. & LeNoble, M. E. ABA, ethylene and the control of shoot and root growth under water stress. J. Exp. Bot. 53, 33–37 (2002).

    CAS  Article  Google Scholar 

  4. 4.

    Xiong, L., Wang, R. G., Mao, G. & Koczan, J. M. Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiol. 142, 1065–1074 (2006).

    CAS  Article  Google Scholar 

  5. 5.

    Chaumont, F. & Tyerman, S. D. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol. 164, 1600–1618 (2014).

    CAS  Article  Google Scholar 

  6. 6.

    Verdoucq, L., Rodrigues, O., Martinière, A., Luu, D. T. & Maurel, C. Plant aquaporins on the move: reversible phosphorylation, lateral motion and cycling. Curr. Opin. Plant Biol. 22, 101–107 (2014).

    CAS  Article  Google Scholar 

  7. 7.

    Tyerman, S. D., Niemietz, C. M. & Bramley, H. Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ. 25, 173–194 (2002).

    CAS  Article  Google Scholar 

  8. 8.

    Martre, P. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol. 130, 2101–2110 (2002).

    CAS  Article  Google Scholar 

  9. 9.

    Bienert, G. P. & Chaumont, F. in Transporters and Pumps in Plant Signaling (eds Geisler, M. and Venema, K.) 3–36 (Springer, Berlin, 2011).

  10. 10.

    Prado, K. & Maurel, C. Regulation of leaf hydraulics: from molecular to whole plant levels. Front. Plant Sci. 4, 255 (2013).

    Article  Google Scholar 

  11. 11.

    Lian, H. L. et al. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res. 16, 651–660 (2006).

    CAS  Article  Google Scholar 

  12. 12.

    Guo, L. et al. Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res. 16, 277–286 (2006).

    CAS  Article  Google Scholar 

  13. 13.

    Maurel, C. et al. Aquaporins in plants. Physiol. Rev. 95, 1321–1358 (2015).

    CAS  Article  Google Scholar 

  14. 14.

    Boursiac, Y. et al. Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J. 56, 207–218 (2008).

    CAS  Article  Google Scholar 

  15. 15.

    Luu, D.-T., Martinière, A., Sorieul, M., Runions, J. & Maurel, C. Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress: root plasma membrane aquaporin trafficking in salt stress. Plant J. 69, 894–905 (2012).

    CAS  Article  Google Scholar 

  16. 16.

    Törnroth-Horsefield, S. et al. Structural mechanism of plant aquaporin gating. Nature 439, 688–694 (2006).

    Article  Google Scholar 

  17. 17.

    Nyblom, M. et al. Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J. Mol. Biol. 387, 653–668 (2009).

    CAS  Article  Google Scholar 

  18. 18.

    Bienert, G. P. & Chaumont, F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Bioph. Acta 1840, 1596–1604 (2014).

    CAS  Article  Google Scholar 

  19. 19.

    Thiagarajah, J. R., Chang, J., Goettel, J. A., Verkman, A. S. & Lencer, W. I. Aquaporin-3 mediates hydrogen peroxide-dependent responses to environmental stress in colonic epithelia. Proc. Natl Acad. Sci. USA 114, 568 (2017).

    CAS  Article  Google Scholar 

  20. 20.

    Bienert, G. P., Heinen, R. B., Berny, M. C. & Chaumont, F. Maize plasma membrane aquaporin ZmPIP2;5, but not ZmPIP1;2, facilitates transmembrane diffusion of hydrogen peroxide. Biochim. Bioph. Acta 1838, 216–222 (2014).

    CAS  Article  Google Scholar 

  21. 21.

    Bienert, G. P., Bienert, M. D., Jahn, T. P., Boutry, M. & Chaumont, F. Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J. 66, 306–317 (2011).

    CAS  Article  Google Scholar 

  22. 22.

    Azad, A. K., Yoshikawa, N., Ishikawa, T., Sawa, Y. & Shibata, H. Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs. Biochim. Bioph. Acta 1818, 1–11 (2012).

    CAS  Article  Google Scholar 

  23. 23.

    Tian, S. et al. Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol. 171, 1635–1650 (2016).

    CAS  Article  Google Scholar 

  24. 24.

    Rodrigues, O. et al. Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proc. Natl Acad. Sci. USA 114, 9200–9205 (2017).

    CAS  Article  Google Scholar 

  25. 25.

    Ma, N. et al. Rh-PIP2;1, a rose aquaporin gene, is involved in ethylene-regulated petal expansion. Plant Physiol. 148, 894 (2008).

    CAS  Article  Google Scholar 

  26. 26.

    Chen, W. et al. Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Mol. Biol. 83, 219–233 (2013).

    CAS  Article  Google Scholar 

  27. 27.

    Zelazny, E. et al. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc. Natl Acad. Sci. USA 104, 12359–12364 (2007).

    CAS  Article  Google Scholar 

  28. 28.

    Li, L. et al. Identification of AtSM34, a novel tonoplast intrinsic protein-interacting polypeptide expressed in response to osmotic stress in germinating seedlings. Chin. Sci. Bull. 56, 3518–3530 (2011).

    CAS  Article  Google Scholar 

  29. 29.

    Slabaugh, E., Held, M. & Brandizzi, F. Control of root hair development in Arabidopsis thaliana by an endoplasmic reticulum anchored member of the R2R3‐MYB transcription factor family. Plant J. 67, 395 (2011).

    CAS  Article  Google Scholar 

  30. 30.

    Chen, Y.-N., Slabaugh, E. & Brandizzi, F. Membrane-tethered transcription factors in Arabidopsis thaliana: novel regulators in stress response and development. Curr. Opin. Plant Biol. 11, 695–701 (2008).

    CAS  Article  Google Scholar 

  31. 31.

    Prado, K. et al. Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. Plant Cell 25, 1029–1039 (2013).

    CAS  Article  Google Scholar 

  32. 32.

    Grondin, A. et al. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27, 1945–1954 (2015).

    CAS  Article  Google Scholar 

  33. 33.

    Azad, T. et al. A LATS biosensor screen identifies VEGFR as a regulator of the Hippo pathway in angiogenesis. Nat. Commun. 9, 1061 (2018).

    CAS  Article  Google Scholar 

  34. 34.

    Fujikawa, Y. & Kato, N. Technical advance: split luciferase complementation assay to study protein–protein interactions in Arabidopsis protoplasts. Plant J. 52, 185–195 (2007).

    CAS  Article  Google Scholar 

  35. 35.

    Fetter, K. Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16, 215–228 (2004).

    CAS  Article  Google Scholar 

  36. 36.

    Li, D. D. et al. Cotton plasma membrane intrinsic protein 2s (PIP2s) selectively interact to regulate their water channel activities and are required for fibre development. New Phytol. 199, 695–707 (2013).

    CAS  Article  Google Scholar 

  37. 37.

    Bellati, J. et al. Novel aquaporin regulatory mechanisms revealed by interactomics. Mol. Cell Proteomics 15, 3473–3487 (2016).

    CAS  Article  Google Scholar 

  38. 38.

    Qing, D. et al. Quantitative and functional phosphoproteomic analysis reveals that ethylene regulates water transport via the C-terminal phosphorylation of aquaporin PIP2;1 in Arabidopsis. Mol. Plant 9, 158–174 (2016).

    CAS  Article  Google Scholar 

  39. 39.

    Prak, S. et al. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins role in subcellular trafficking of AtPIP2; 1 in response to salt stress. Mol. Cell Proteomics 7, 1019–1030 (2008).

    CAS  Article  Google Scholar 

  40. 40.

    Niittylä, T. et al. Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Mol. Cell. Proteomics 6, 1711–1726 (2007).

    Article  Google Scholar 

  41. 41.

    Di Pietro, M. et al. Coordinated post-translational responses of aquaporins to abiotic and nutritional stimuli in Arabidopsis roots. Mol. Cell. Proteomics M113, 028241 (2013).

    Google Scholar 

  42. 42.

    Johansson, I. et al. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10, 451–459 (1998).

    CAS  Article  Google Scholar 

  43. 43.

    Chinnusamy, V. & Zhu, J.-K. Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol. 12, 133–139 (2009).

    CAS  Article  Google Scholar 

  44. 44.

    Nolan, T. M. et al. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev. Cell 41, 33–46 (2017).

    CAS  Article  Google Scholar 

  45. 45.

    Wang, P. et al. Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol. Cell 69, 100–112 (2018).

    CAS  Article  Google Scholar 

  46. 46.

    Tian, J. et al. TRV-GFP: a modified tobacco rattle virus vector for efficient and visualizable analysis of gene function. J. Exp. Bot. 65, 311–322 (2014).

    CAS  Article  Google Scholar 

  47. 47.

    Wang, W., Vignani, R., Scali, M. & Cresti, M. A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27, 2782–2786 (2006).

    CAS  Article  Google Scholar 

  48. 48.

    Wiśniewski, J. R., Zougman, A., Nagaraj, N. & Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 6, 359–362 (2009).

    Article  Google Scholar 

  49. 49.

    Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367 (2008).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank Z. Li (Biological Mass Spectrometry Laboratory of the Functional Genomic Technology Centre of China Agricultural University) for LC–MS experiments. We thank J. Zhu (Jingjie PTM Biolabs, Inc.) for analysis of LC–MS data. We thank Z. Gong (China Agricultural University) for providing the pSuper1300 vector. We thank D. Zhang (Tsinghua University) for his generous help with MYTH screening. We thank PlantScribe (www.plantscribe.com) for careful editing of this article. This work was supported by the National Natural Science Foundation of China (grant Nos. 31520103913, 31522049, 31730079 and 31401914) and the 111 Project of the Ministry of Education (No. B17043).

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S.Z., M.F., W.C., J.L., Y.W. and Y.L. performed the experiments. N.M. and J.G. designed the research. X.Z., C.J., S.G. and N.M. provided technical support, conceptual advice and data analysis. S.Z., N.M. and J.G. wrote the article.

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Correspondence to Nan Ma or Junping Gao.

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Supplementary information

Supplementary Information

Supplementary Figures 1–10, Supplementary Methods, Supplementary References, legends for Supplementary Tables and Datasets, and Supplementary Tables 1–3.

Reporting Summary

Supplementary Dataset 1

The entire database search results for validation of anti-RhPTM antibody by LC–MS.

Supplementary Dataset 2

Differentially expressed genes in RhPTM-silenced rose plants.

Supplementary Dataset 3

The entire database search results for phosphorylation of RhPIP2;1 by LC–MS.

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Zhang, S., Feng, M., Chen, W. et al. In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin. Nat. Plants 5, 290–299 (2019). https://doi.org/10.1038/s41477-019-0376-1

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