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A phytochrome-B-mediated regulatory mechanism of phosphorus acquisition

Nature Plantsvolume 4pages10891101 (2018) | Download Citation

Abstract

Phosphorus (P) is a key macronutrient whose availability has a profound effect on plant growth and productivity. The understanding of the mechanism underlying P availability-responsive P acquisition has expanded largely in the past decade; however, effects of other environmental factors on P acquisition and utilization remain elusive. Here, by imaging natural variation in phosphate uptake in 200 natural accessions of Arabidopsis, we identify two accessions with low phosphate uptake activity, Lm-2 and CSHL-5. In these accessions, natural variants of phytochrome B were found to cause both decreased light sensitivity and lower phosphate uptake. Furthermore, we also found that expression levels of phosphate starvation-responsive genes are directly modulated by phytochrome interacting factors (PIF) PIF4/PIF5 and HY5 transcription factors whose activity is under the control of phytochromes. These findings disclose a new molecular mechanism underlying red-light-induced activation of phosphate uptake, which is responsible for different activity for P acquisition in some natural accessions of Arabidopsis.

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The datasets generated and/or analysed in this study are available from the corresponding author upon any reasonable request.

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References

  1. 1.

    Schachtman, D. P., Reid, R. J. & Ayling, S. M. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 116, 447–453 (1998).

  2. 2.

    Raghothama, K. G. Phosphate acquisition. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 50, 665–693 (1999).

  3. 3.

    Shin, H., Shin, H. S., Dewbre, G. R. & Harrison, M. J. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J. 39, 629–642 (2004).

  4. 4.

    Nussaume, L. et al. Phosphate import in plants: focus on the PHT1 transporters. Front. Plant Sci. 2, 83 (2011).

  5. 5.

    Poirier, Y. & Bucher, M. Phosphate transport and homeostasis in Arabidopsis. Arabidopsis Book 1, e0024 (2002).

  6. 6.

    Versaw, W. K. & Harrison, M. J. A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14, 1751–1766 (2002).

  7. 7.

    Guo, B. et al. Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol. 177, 889–898 (2008).

  8. 8.

    Liu, T. Y. et al. Identification of plant vacuolar transporters mediating phosphate storage. Nat. Commun. 7, 11095 (2016).

  9. 9.

    Rouached, H., Arpat, A. B. & Poirier, Y. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol. Plant 3, 288–299 (2010).

  10. 10.

    Rubio, V. et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15, 2122–2133 (2001).

  11. 11.

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

  12. 12.

    Bustos, R. et al. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 6, e1001102 (2010).

  13. 13.

    Puga, M. I. et al. SPX1 is a phosphate-dependent inhibitor of phosphate starvation response 1 in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 14947–14952 (2014).

  14. 14.

    Lejay, L. et al. Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15, 2218–2232 (2003).

  15. 15.

    Lejay, L. et al. Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol. 146, 2036–2053 (2008).

  16. 16.

    Martin, A. C. et al. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J. 24, 559–567 (2000).

  17. 17.

    Jain, A. et al. Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol. 144, 232–247 (2007).

  18. 18.

    Jiang, C., Gao, X., Liao, L., Harberd, N. P. & Fu, X. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol. 145, 1460–1470 (2007).

  19. 19.

    Maloof, J. N. et al. Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29, 441–446 (2001).

  20. 20.

    Li, J., Li, G., Wang, H. & Deng, X. W. Phytochrome signaling mechanisms. Arabidopsis Book 9, e0148 (2011).

  21. 21.

    Sullivan, J. A. & Deng, X. Y. From seed to seed: the role of photoreceptors in Arabidopsis development. Dev. Biol. 260, 289–297 (2003).

  22. 22.

    Reed, J. W., Nagpal, P., Poole, D. S., Furuya, M. & Chory, J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5, 147–157 (1993).

  23. 23.

    Hornitschek, P. et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 71, 699–711 (2012).

  24. 24.

    Borthwick, H. A., Hendricks, S. B., Parker, M. W., Toole, E. H. & Toole, V. K. A reversible photoreaction controlling seed germination. Proc. Natl Acad. Sci. USA 38, 662–666 (1952).

  25. 25.

    Al-Sady, B., Ni, W., Kircher, S., Schäfer, E. & Quail, P. H. Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell 23, 439–446 (2006).

  26. 26.

    Yanagisawa, S., Yoo, S. D. & Sheen, J. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425, 521–525 (2003).

  27. 27.

    Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565–1572 (2007).

  28. 28.

    Chang, C. S. et al. LZF1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant J. 54, 205–219 (2008).

  29. 29.

    Tsunoyama, Y., Morikawa, K., Shiina, T. & Toyoshima, Y. Blue light specific and differential expression of a plastid sigma factor, Sig5 in Arabidopsis thaliana. FEBS Lett. 516, 225–228 (2002).

  30. 30.

    Sato-Nara, K. et al. Identification of genes regulated by dark adaptation and far-red light illumination in roots of Arabidopsis thaliana. Plant Cell Environ. 27, 1387–1394 (2004).

  31. 31.

    Sharrock, R. S. & Clack, T. Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol. 130, 442–456 (2002).

  32. 32.

    Osterlund, M. T., Hardtke, C. S., Wei, N. & Deng, X. W. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405, 462–466 (2000).

  33. 33.

    Leivar, P. et al. Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr. Biol. 18, 1815–1823 (2008).

  34. 34.

    Nilsson, L., Müller, R. & Nielsen, T. H. Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation. Physiol. Plant. 139, 129–143 (2010).

  35. 35.

    Mlodzinska, E. & Zboinska, M. Phosphate uptake and allocation—a closer look at Arabidopsis thaliana L. and Oryza sativa L. Front. Plant Sci. 7, 1198 (2016).

  36. 36.

    Sun, L., Song, L., Zhang, Y., Zheng, Z. & Liu, D. Arabidopsis PHL2 and PHR1 act redundantly as the key components of the central regulatory system controlling transcriptional responses to phosphate starvation. Plant Physiol. 170, 499–514 (2016).

  37. 37.

    Park, B. S., Seo, J. S. & Chua, N. H. Nitrogen limitation adaptation recruits PHOSPHATE2 to target the phosphate transporter PT2 for degradation during the regulation of Arabidopsis phosphate homeostasis. Plant Cell 26, 454–464 (2014).

  38. 38.

    Chen, Y. F. et al. The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21, 3554–3566 (2009).

  39. 39.

    Martínez-García, J. F., Huq, E. & Quail, P. H. Direct targeting of light signals to a promoter element-bound transcription factor. Science 288, 859–863 (2000).

  40. 40.

    Al-Sady, B., Kikis, E. A., Monte, E. & Quail, P. H. Mechanistic duality of transcription factor function in phytochrome signaling. Proc. Natl Acad. Sci. USA 105, 2232–2237 (2008).

  41. 41.

    Kumar, S. V. et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245 (2012).

  42. 42.

    Shahnejat-Bushehri, S., Tarkowska, D., Sakuraba, Y. & Balazadeh, S. Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nat. Plants 2, 16013 (2016).

  43. 43.

    Toledo-Ortiz, G. et al. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet. 10, e1004416 (2014).

  44. 44.

    Oyama, T., Shimura, Y. & Okada, K. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 11, 2983–2995 (1997).

  45. 45.

    Chen, X. et al. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr. Biol. 26, 640–646 (2016).

  46. 46.

    Lee, B. R., Koprivova, A. & Kopriva, S. The key enzyme of sulfate assimilation, adenosine 5’-phosphosulfate reductase, is regulated by HY5 in Arabidopsis. Plant J. 67, 1042–1054 (2011).

  47. 47.

    Huang, L., Zhang, H., Zhang, H., Deng, X. W. & Wei, N. HY5 regulates nitrite reductase 1 (NIR1) and ammoniumtransporter1; 2 (AMT1;2) in Arabidopsis seedlings. Plant Sci. 238, 330–339 (2015).

  48. 48.

    Sakuraba, Y. & Yanagisawa, S. Light signalling-induced regulation of nutrient acquisition and utilisation in plants. Semin. Cell Dev. Biol. 83, 123–132 (2018).

  49. 49.

    Gundel, P. E., Pierik, R., Mommer, L. & Ballare, C. L. Competing neighbors: light perception and root function. Oecologia. 176, 1–10 (2014).

  50. 50.

    Van Gelderen, K. et al. Far-red light detection in the shoot regulates lateral root development through the HY5 transcription factor. Plant Cell 30, 101–116 (2018).

  51. 51.

    Zhang, Y. et al. A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet. 9, e1003244 (2013).

  52. 52.

    Lee, H. J. et al. Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots. Sci. Signal. 9, ra106 (2016).

  53. 53.

    Liu, T. Y. et al. PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24, 2168–2183 (2012).

  54. 54.

    Huang, T. K. et al. Identification of downstream components of ubiquitin-conjugatinng enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 25, 4044–4060 (2013).

  55. 55.

    Liu, Y. et al. Light and ethylene coordinately regulate the phosphate starvation response through transcriptional regulation of PHOSPHATE STARVATION RESPONSE1. Plant Cell 29, 2269–2284 (2017).

  56. 56.

    Ward, J. T., Lahner, B., Yakubova, E., Salt, D. E. & Raghothama, K. G. The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol. 147, 1181–1191 (2008).

  57. 57.

    Abel, S. Phosphate sensing in root development. Curr. Opin. Plant. Biol. 14, 303–309 (2011).

  58. 58.

    Kisko, M. et al. LPCAT1 controls phosphate homeostasis in a zinc-dependent manner. eLife 7, e32077 (2018).

  59. 59.

    Zheng, L. et al. Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol. 151, 262–274 (2009).

  60. 60.

    Piao, W., Kim, E. Y., Han, S. H., Sakuraba, Y. & Paek, N. C. Rice phytochrome B (OsPhyB) negatively regulates dark- and starvation-induced leaf senescence. Plants 4, 644–663 (2015).

  61. 61.

    Yoshida, S, Forno, D. A, Cock, J. A. & Gomez, K. A. Laboratory Manual for Plant Physiological Studies of Rice 3rd edn (International Rice Research Institute, Manila, Philippines, 1976).

  62. 62.

    Zhang, X., Henriques, R., Lin, S. S., Niu, Q. W. & Chua, N. H. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641–646 (2006).

  63. 63.

    Chiou, T. J. et al. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18, 412–421 (2006).

  64. 64.

    Saleh, A., Alvarez-Venegas, R. & Avramova, Z. An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat. Protoc. 3, 1018–1025 (2008).

  65. 65.

    Sakuraba, Y. et al. Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat. Commun. 5, 4636 (2014).

  66. 66.

    Luehrsen, K. R., de Wet, J. R. & Walbot, V. Transient expression analysis in plants using firefly luciferase reporter gene. Methods Enzymol. 216, 397–414 (1992).

  67. 67.

    Wu, F. H. et al. Tape-Arabidopsis sandwich—a simpler Arabidopsis protoplast isolation method. Plant. Methods. 5, 16 (2009).

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Acknowledgements

We thank the Arabidopsis Biological Resource Center for seeds from the transfer-DNA lines, J. Paz-Ares (Centro Nacional de Biotecnología, Spain) for seeds of the phr1 phl1 mutant and M. Tsumura in our laboratory for assistance in plant cultivation. This work was supported in part by JST CREST grant number JPMJCR 15O5 to S.Y. and K.I., JSPS KAKENHI grant number 26221103 to K.I. and S.Y., and grant numbers 25252014 to S.Y., 17H05024 to Y.S. and 16H07045 to K.M.

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Affiliations

  1. Plant Functional Biotechnology, Biotechnology Research Center, The University of Tokyo, Tokyo, Japan

    • Yasuhito Sakuraba
    • , Satomi Kanno
    •  & Shuichi Yanagisawa
  2. Department of Biology, Faculty of Science, Kyushu University, Fukuoka, Japan

    • Atsushi Mabuchi
    • , Keina Monda
    •  & Koh Iba

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Contributions

Y.S. and S.Y. designed the research. Y.S. performed experiments. S.K., A.M., K.M. and K.I. provided the new analytical tools and plant materials used in this study. Y.S. and S.Y. analysed the data and wrote the article.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Shuichi Yanagisawa.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–21

  2. Reporting Summary

  3. Supplementary Tables 1–6

    Supplementary Table 1: List of Arabidopsis accessions used in this study and their Pi uptake activities. Supplementary Table 2: Genes upregulated or downregulated in pif4 pif5 seedlings grown under the standard Pi condition. Supplementary Table 3: Genes upregulated or downregulated in pif4 pif5 seedlings grown under the Pi-deficient condition. Supplementary Table 4: List of Arabidopsis mutants used in this study. Supplementary Table 5: List of primer sequences used in this study. Supplementary Table 6: List of Arabidopsis accessions used for GWAS.

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https://doi.org/10.1038/s41477-018-0294-7

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