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A phytochrome-B-mediated regulatory mechanism of phosphorus acquisition

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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Fig. 1: Natural variation in phyB affects Pi uptake activity.
Fig. 2: Effect of red light on Pi uptake and accumulation.
Fig. 3: PIF4 and PIF5 are involved in the regulation of Pi uptake.
Fig. 4: Modifications in expression of Pi uptake-related and Pi starvation-responsive genes in the pif4 pif5 mutant.
Fig. 5: PIF4 and PIF5 directly repress transcription of PHT1;1 and PHL1.
Fig. 6: HY5 directly activates PHT1;1 transcription.

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Data availability

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

References

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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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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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.

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Correspondence to Shuichi Yanagisawa.

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Supplementary Figures 1–21

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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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Sakuraba, Y., Kanno, S., Mabuchi, A. et al. A phytochrome-B-mediated regulatory mechanism of phosphorus acquisition. Nature Plants 4, 1089–1101 (2018). https://doi.org/10.1038/s41477-018-0294-7

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