Skip to main content

Advertisement

Log in

Overexpression of a Maize Transcription Factor ZmPHR1 Improves Shoot Inorganic Phosphate Content and Growth of Arabidopsis under Low-Phosphate Conditions

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Maize (Zea mays L.) yield is limited by the poor availability of inorganic phosphate (Pi) in many arable areas worldwide. Phosphorus use efficiency (PUE) is a complex multigene trait, with a single gene contributing only a small percentage to the phenotype. Transcription factors (TFs) are very important as a single TF frequently coordinates the expression of multiple genes in response to environmental signals. Previous studies have indicated that the TFs AtPHR1 and OsPHR2 play important roles in the regulation of plant phosphorus accumulation. However, little is known about the functions of PHR-like genes in maize. In this study, a member of the MYB-CC family encoding a 449-amino acid protein, ZmPHR1, was isolated. The ZmPHR1∷GFP fusion was localized in the nucleus, which indicates that ZmPHR1 is also a TF. Phylogenetic tree analysis revealed that ZmPHR1 belongs to the same subfamily of MYB-CCs as OsPHR1, OsPHR2 and AtPHR1. Transgenic Arabidopsis lines overexpressing ZmPHR1 were used to investigate the pleiotropic effects of this gene under low Pi conditions. Overexpression of ZmPHR1 led to the upregulation of multiple genes that regulate metabolism during Pi-starvation, which in turn resulted in an elevation in Pi content in shoots. Most notably, Arabidopsis overexpressing ZmPHR1 showed better growth under low-Pi conditions. The results presented in this study suggest that PUE could be improved through the manipulation of the TF ZmPHR1 in maize and possibly in other species under Pi-deficient conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2a–c
Fig. 3a,b
Fig. 4
Fig. 5a–f
Fig. 6
Fig. 7a,b
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  PubMed  CAS  Google Scholar 

  • Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6:673–685

    Article  PubMed  CAS  Google Scholar 

  • Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A, Paz-Ares J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6:1–15

    Article  Google Scholar 

  • Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29

    Article  PubMed  CAS  Google Scholar 

  • Chen ZH, Nimmo GA, Jenkins GI, Nimmp HG (2007) BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem J 405:191–198

    PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Coelho GTCP, Carneiro NP, Karthikeyan AS, Raghothama KG, Schaffert RE, Brandão RL, Paiva LV, Souza IRP, Alves VM, Imolesi A, Carvalho CHS, Carneiro AA (2010) A phosphate transporter promoter from Arabidopsis thaliana AtPHT1;4 gene drives preferential gene expression in transgenic maize roots under phosphorus starvation. Plant Mol Biol Rep 28:717–723

    Article  CAS  Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

    Article  Google Scholar 

  • Da Silva ÁE, Gabelman W (1992) Screening maize inbred lines for tolerance to low-P stress condition. Plant Soil 146:181–187

    Article  Google Scholar 

  • Devaiah BN, Karthikeyan AS, Raghothama KG (2007a) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801

    Article  PubMed  CAS  Google Scholar 

  • Devaiah BN, Nagarajan VK, Raghothama KG (2007b) Phosphate homeostasis and root development in Arabidopsis is synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145:147–159

    Article  PubMed  CAS  Google Scholar 

  • Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG (2009) Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant 2:43–58

    Article  PubMed  CAS  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    Article  PubMed  CAS  Google Scholar 

  • Hou XL, Wu P, Jiao FC, Jia QJ, Chen HM, Yu J, Song XW, Yi KK (2005) Regulation of the expression of OsIPS1 and OsIPS2 in rice via systemic and local Pi signalling and hormones. Plant Cell Environ 28:353–364

    Article  CAS  Google Scholar 

  • Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF (2000) Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to Arbuscular mycorrhizal fungi. Crop Sci 40:358–363

    Article  Google Scholar 

  • Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)). Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • May A, Berger S, Hertel T, Köck M (2011) The Arabidopsis thaliana phosphate starvation responsive gene AtPPsPase1 encodes a novel type of inorganic pyrophosphatase. Biochim Biophys Acta 1810:178–185

    Article  PubMed  CAS  Google Scholar 

  • Misson J, Thibaud MC, Bechtold N, Raghothama K, Nussaume L (2004) Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol Biol 55:727–741

    Article  PubMed  CAS  Google Scholar 

  • Muchhal US, Pardo JM, Raghotama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 93:10519–10523

    Article  PubMed  CAS  Google Scholar 

  • Nanamori M, Shinano T, Wasaki J, Yamamura T, Rao IM, Osaki M (2004) Low phosphorus tolerance mechanisms: phosphorus recycling and photosynthate partitioning in the tropical forage grass, Brachiaria hybrid cultivar Mulato compared with rice. Plant Cell Physiol 45:460–469

    Article  PubMed  CAS  Google Scholar 

  • Nilsson L, Müller R, Nielsen TH (2007) Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant Cell Environ 30:1499–1512

    Article  PubMed  CAS  Google Scholar 

  • Rae AL, Jarmey JM, Mudge SR, Smith FW (2004) Overexpression of a high-affinity transporter in transgenic barley plants does not enhance phosphate uptake rates. Funct Plant Biol 31:141–148

    Article  CAS  Google Scholar 

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693

    Article  PubMed  CAS  Google Scholar 

  • Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3:182–187

    PubMed  CAS  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  PubMed  CAS  Google Scholar 

  • Sharply A, Moyer B (2000) Phosphorus forms in manure and compost and their release during simulated rainfall. J Environ Qual 29:1462–1469

    Article  Google Scholar 

  • Sims JT, Edwards AC, Schoumans OF, Simard RR (2000) Integrating soil phosphorus testing into environmentally based agricultural management practices. J Environ Qual 29:60–71

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2439–2442

    Article  Google Scholar 

  • Tan ZJ, Hu YL, Lin ZP (2012) Expression of NtPT5 is correlated with the degree of colonization in tobacco roots inoculated with Glomus etunicatum. Plant Mol Bio Rep 30:885–893

    Article  CAS  Google Scholar 

  • Tang QY, Zhang CX (2012) Data Processing System (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Science 00:1–7

    Google Scholar 

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    Article  PubMed  CAS  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Wu P, Ma LG, Hou XL, Wang MY, Wu YR, Liu FY, Deng XW (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260–1271

    Article  PubMed  CAS  Google Scholar 

  • Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci USA 96:15336–15341

    Article  PubMed  CAS  Google Scholar 

  • Zhang XG, Yin DM, Ma CZ, Fu TD (2011) Phylogenetic analysis of S-locus genes reveals the complicated evolution relationship of S haplotypes in Brassica. Plant Mol Biol Rep 29:481–488

    Article  Google Scholar 

  • Zhou J, Jiao FC, Wu ZC, Li YY, Wang XM, He XW, Zhong WQ, Wu P (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Yiping Tong, Dr. Yu Cheng, Dr. Hui Liang and Mrs. Yuxiang Wen from the Institute of Genetics and Developmental Biology, Chinese Academy of Science for their helpful suggestions and observation of GFP with the Laser Confocal Scanning Microscope. The authors are grateful to Dr. Hongjie Li from the Institute of Crop Science, Chinese Academy of Agriculture Science, and Dr. Ling Yuan from the Department of Plant and Soil Sciences, University of Kentucky for their critical reviews of this manuscript. The research was supported by the grants of Major Transgenic Organism Breeding Projects from Chinese Ministry of Agriculture (2009ZX08003-017B and 2011ZX08003-001) and Shanxi International Cooperation Project (2012081005-1).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jianrong Bai or Huiming Liu.

Additional information

X. Wang and J. Bai contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, X., Bai, J., Liu, H. et al. Overexpression of a Maize Transcription Factor ZmPHR1 Improves Shoot Inorganic Phosphate Content and Growth of Arabidopsis under Low-Phosphate Conditions. Plant Mol Biol Rep 31, 665–677 (2013). https://doi.org/10.1007/s11105-012-0534-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-012-0534-3

Keywords

Navigation