Advertisement

Plant Molecular Biology Reporter

, Volume 31, Issue 3, pp 665–677 | Cite as

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

  • Xiuhong Wang
  • Jianrong Bai
  • Huiming Liu
  • Yi Sun
  • Xiangyuan Shi
  • Zhiqiang Ren
Original Paper

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.

Keywords

Maize Transcription factor ZmPHR1 Phosphorus use efficiency Arabidopsis thaliana 

Notes

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).

References

  1. Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8PubMedCrossRefGoogle Scholar
  2. Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999PubMedCrossRefGoogle Scholar
  3. 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 6:673–685PubMedCrossRefGoogle Scholar
  4. 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 6:1–15CrossRefGoogle Scholar
  5. Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29PubMedCrossRefGoogle Scholar
  6. 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 405:191–198PubMedGoogle Scholar
  7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  8. 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 28:717–723CrossRefGoogle Scholar
  9. Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305CrossRefGoogle Scholar
  10. Da Silva ÁE, Gabelman W (1992) Screening maize inbred lines for tolerance to low-P stress condition. Plant Soil 146:181–187CrossRefGoogle Scholar
  11. Devaiah BN, Karthikeyan AS, Raghothama KG (2007a) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801PubMedCrossRefGoogle Scholar
  12. 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 145:147–159PubMedCrossRefGoogle Scholar
  13. 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 2:43–58PubMedCrossRefGoogle Scholar
  14. 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 39:1033–1037PubMedCrossRefGoogle Scholar
  15. 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 28:353–364CrossRefGoogle Scholar
  16. 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 40:358–363CrossRefGoogle Scholar
  17. 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 147:732–746PubMedCrossRefGoogle Scholar
  18. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)). Methods 25:402–408PubMedCrossRefGoogle Scholar
  19. 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 1810:178–185PubMedCrossRefGoogle Scholar
  20. 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 55:727–741PubMedCrossRefGoogle Scholar
  21. Muchhal US, Pardo JM, Raghotama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 93:10519–10523PubMedCrossRefGoogle Scholar
  22. 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 45:460–469PubMedCrossRefGoogle Scholar
  23. 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 30:1499–1512PubMedCrossRefGoogle Scholar
  24. 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 31:141–148CrossRefGoogle Scholar
  25. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693PubMedCrossRefGoogle Scholar
  26. Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3:182–187PubMedGoogle Scholar
  27. 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 15:2122–2133PubMedCrossRefGoogle Scholar
  28. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453PubMedCrossRefGoogle Scholar
  29. Sharply A, Moyer B (2000) Phosphorus forms in manure and compost and their release during simulated rainfall. J Environ Qual 29:1462–1469CrossRefGoogle Scholar
  30. Sims JT, Edwards AC, Schoumans OF, Simard RR (2000) Integrating soil phosphorus testing into environmentally based agricultural management practices. J Environ Qual 29:60–71CrossRefGoogle Scholar
  31. 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 28:2439–2442CrossRefGoogle Scholar
  32. 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 30:885–893CrossRefGoogle Scholar
  33. 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 00:1–7Google Scholar
  34. Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397PubMedCrossRefGoogle Scholar
  35. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447CrossRefGoogle Scholar
  36. 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 132:1260–1271PubMedCrossRefGoogle Scholar
  37. 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 96:15336–15341PubMedCrossRefGoogle Scholar
  38. 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 29:481–488CrossRefGoogle Scholar
  39. 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 146:1673–1686PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.College of Life ScienceShanxi UniversityTaiyuanChina
  2. 2.Institute of Crop ScienceShanxi Academy of Agricultural SciencesTaiyuanChina
  3. 3.Shanxi Academy of Agricultural SciencesTaiyuanChina
  4. 4.Key Laboratory of Crop Gene Resources and Germplasm Enhancement on Loess PlateauMinistry of AgricultureTaiyuanPeople’s Republic of China
  5. 5.Modern Agricultural Research CenterShanxi Academy of Agricultural SciencesTaiyuanChina
  6. 6.Biotechnology Research CenterShanxi Academy of Agricultural SciencesTaiyuanChina

Personalised recommendations