Vascular-mediated signalling involved in early phosphate stress response in plants

Abstract

Depletion of finite global rock phosphate (Pi) reserves will impose major limitations on future agricultural productivity and food security. Hence, modern breeding programmes seek to develop Pi-efficient crops with sustainable yields under reduced Pi fertilizer inputs. In this regard, although the long-term responses of plants to Pi stress are well documented, the early signalling events have yet to be elucidated. Here, we show plant tissue-specific responses to early Pi stress at the transcription level and a predominant role of the plant vascular system in this process. Specifically, imposition of Pi stress induces rapid and major changes in the mRNA population in the phloem translocation stream, and grafting studies have revealed that many hundreds of phloem-mobile mRNAs are delivered to specific sink tissues. We propose that the shoot vascular system acts as the site of root-derived Pi stress perception, and the phloem serves to deliver a cascade of signals to various sinks, presumably to coordinate whole-plant Pi homeostasis.

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Figure 1: Spatiotemporal early response to Pi stress in cucumber.
Figure 2: Tissue-specific differentially expressed mRNAs in response to early Pi stress in cucumber.
Figure 3: Tissue-specific differentially expressed miRNAs in response to early Pi stress in cucumber.
Figure 4: Graft-transmissible mRNAs and their response to early Pi stress.
Figure 5: Graft-transmissible mRNA classification and analyses of a group of candidate long-distance signalling mRNAs.

References

  1. 1

    Cordell, D., Drangert, J. O. & White, S. The story of phosphorus: global food security and food for thought. Glob. Environ. Change 19, 292–305 (2009).

  2. 2

    Dawson, C. J. & Hilton, J. Fertiliser availability in a resource-limited world: production and recycling of nitrogen and phosphorus. Food Policy 36, S14–S22 (2011).

  3. 3

    Schroeder, J. I. et al. Using membrane transporters to improve crops for sustainable food production. Nature 497, 60–66 (2013).

  4. 4

    Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 490, 254–257 (2012).

  5. 5

    Chiou, T. J. & Lin, S. I. Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 62, 185–206 (2011).

  6. 6

    Lough, T. J. & Lucas, W. J. Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol. 57, 203–232 (2006).

  7. 7

    Plaxton, W. C. & Tran, H. T. Metabolic adaptations of phosphate-starved plants. Plant Physiol. 156, 1006–1015 (2011).

  8. 8

    Péret, B. et al. Root architecture responses: in search of phosphate. Plant Physiol. 166, 1713–1723 (2014).

  9. 9

    Zhang, Z., Liao, H. & Lucas, W. J. Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J. Integr. Plant Biol. 56, 192–220 (2014).

  10. 10

    Fujii, H., Chiou, T. J., Lin, S. I., Aung, K. & Zhu, J. K. A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15, 2038–2043 (2005).

  11. 11

    Pant, B. D., Buhtz, A., Kehr, J. & Scheible, W. R. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53, 731–738 (2008).

  12. 12

    Lin, S. I. et al. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol. 147, 732–746 (2008).

  13. 13

    Bari, R., Pant, B. D., Stitt, M. & Scheible, W. R. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141, 988–999 (2006).

  14. 14

    Lucas, W. J. et al. The plant vascular system: evolution, development and functions. J. Integr. Plant Biol. 55, 294–388 (2013).

  15. 15

    Lin, W. D. et al. Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling. Plant Physiol. 155, 1383–1402 (2011).

  16. 16

    Wolf, S., Hématy, K. & Höfte, H. Growth control and cell wall signaling in plants. Annu. Rev. Plant Biol. 63, 381–407 (2012).

  17. 17

    Buhtz, A., Springer, F., Chappell, L., Baulcombe, D. C. & Kehr, J. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J. 53, 739–749 (2008).

  18. 18

    Pant, B. D. et al. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 150, 1541–1555 (2009).

  19. 19

    Kim, G., LeBlanc, M. L., Wafula, E. K. & Westwood, J. H. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345, 808–811 (2014).

  20. 20

    Thieme, C. J. et al. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants 1, 15025 (2015).

  21. 21

    Yang, Y. et al. Messenger RNA exchange between scions and rootstocks in grafted grapevines. BMC Plant Biol. 15, 251 (2015).

  22. 22

    Ham, B. K. et al. A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21, 197–215 (2009).

  23. 23

    Liu, J. et al. A vacuolar phosphate transporter essential for phosphate homeostasis in Arabidopsis. Proc. Natl Acad. Sci. USA 112, E6571–E6578 (2015).

  24. 24

    Lin, W. Y., Huang, T. K., Leong, S. J. & Chiou, T. J. Long-distance call from phosphate: systemic regulation of phosphate starvation responses. J. Exp. Bot. 65, 1817–1827 (2014).

  25. 25

    Liu, T. Y. et al. Vacuolar Ca2+/H+ transport activity is required for systemic phosphate homeostasis involving shoot-to-root signaling in Arabidopsis. Plant Physiol. 156, 1176–1189 (2011).

  26. 26

    Secco, D. et al. Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell 25, 4285–4304 (2013).

  27. 27

    O'Rourke, J. A. et al. An RNA-Seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol. 161, 705–724 (2013).

  28. 28

    Brinker, M. et al. Microarray analyses of gene expression during adventitious root development in Pinus contorta. Plant Physiol. 135, 1526–1539 (2004).

  29. 29

    Misson, J. et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl Acad. Sci. USA 102, 11934–11939 (2005).

  30. 30

    Wu, P. et al. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 132, 1260–1271 (2003).

  31. 31

    Hammond, J. P. et al. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol. 132, 578–596 (2003).

  32. 32

    Morcuende, R. et al. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ. 30, 85–112 (2007).

  33. 33

    Ham, B. K., Li, G., Jia, W., Leary, J. A. & Lucas, W. J. Systemic delivery of siRNA in pumpkin by a plant PHLOEM SMALL RNA-BINDING PROTEIN 1-ribonucleoprotein complex. Plant J. 80, 683–694 (2014).

  34. 34

    Yoo, B. C. et al. A systemic small RNA signaling system in plants. Plant Cell 16, 1979–2000 (2004).

  35. 35

    Aoki, K. et al. Destination-selective long-distance movement of phloem proteins. Plant Cell 17, 1801–1814 (2005).

  36. 36

    Brosnan, C. A. et al. Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proc. Natl. Acad. Sci. USA 104, 14741–14746 (2007).

  37. 37

    Kehr, J. & Buhtz, A. Long distance transport and movement of RNA through the phloem. J. Exp. Bot. 59, 85–92 (2008).

  38. 38

    Lucas, W. J., Yoo, B. C. & Kragler, F. RNA as a long-distance information macromolecule in plants. Nature Rev. Mol. Cell Biol. 2, 849–857 (2001).

  39. 39

    Kim, M., Canio, W., Kessler, S. & Sinha, N. Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293, 287–289 (2001).

  40. 40

    Ruiz-Medrano, R., Xoconostle-Cázares, B. & Lucas, W. J. Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126, 4405–4419 (1999).

  41. 41

    Uhde-Stone, C. et al. Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol. 131, 1064–1079 (2003).

  42. 42

    Lee, J. Y. et al. Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299, 392–396 (2003).

  43. 43

    Lin, M. K., Lee, Y. J., Lough, T. J., Phinney, B. S. & Lucas, W. J. Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol. Cell. Proteomics 8, 343–356 (2009).

  44. 44

    Guo, S. et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genet. 45, 51–58 (2013).

  45. 45

    Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

  46. 46

    Huang, S. et al. The genome of the cucumber, Cucumis sativus L. Nature Genet. 41, 1275–1281 (2009).

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Acknowledgements

We thank J. Zeng, W.-c. Hu and S. Zhang for technical support. This work was supported by grants from the USDA National Institute of Food and Agriculture (NIFA; 201015479 to W.J.L. and L.V.K.) and the National Science Foundation (IOS-1339128 to W.J.L.).

Author information

Z.Z., L.V.K., Z.F. and W.J.L. conceived this project and designed the experiments. Z.Z., Y.Z., B.-K.H., J.C. and A.Y. performed the experiments. All authors contributed to data analysis. Z.Z. and W.J.L. wrote the manuscript with input from L.V.K., Z.F., Y.Z., B.-K.H., J.C. and A.Y.

Correspondence to William J. Lucas.

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The authors declare no competing financial interests.

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Zhang, Z., Zheng, Y., Ham, B. et al. Vascular-mediated signalling involved in early phosphate stress response in plants. Nature Plants 2, 16033 (2016). https://doi.org/10.1038/nplants.2016.33

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