Skip to main content
SpringerLink
Log in

Transcriptional responses of maize seedling root to phosphorus starvation

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Maize (Zea mays) is the most widely cultivated crop around the world, however, it is commonly affected by phosphate (Pi) deficiency and the underlying molecular basis of responses mechanism is still unknown. In this study, the transcriptional response of maize roots to Pi starvation at 3 days after the onset of Pi deprivation was assessed. The investigation revealed a total of 283 Pi-responsive genes, of which 199 and 84 genes were found to be either up- or down-regulated respectively, by 2-fold or more. Pi-responsive genes were found to be involved in sugar and nitrogen metabolic pathways, ion transport, signal transduction, transcriptional regulation, and other processes related to growth and development. In addition, the expression patterns of maize inorganic phosphorus transporters, acid phosphatase, phytase, 2-deoxymugineic acid synthase1, POD and MYB transcription factor were validated in 178 roots response to low phosphorus stress. of which, two genes encoding phytase and acid phosphatase were significantly induced by Pi deficiency and may play a pivotal role in the process of absorption and re-utilization of Pi in Maize. These results not only enhance our knowledge about molecular processes associated with Pi deficiency, but also facilitate the identification of key molecular determinants for improving Pi use in maize. Moreover, this work sets a framework to produce Pi-specific maize microarrays to study the changes in global gene expression between Pi-efficient and Pi-inefficient maize genotypes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Bar-Yosef B (1991) Root excretions and their environmental effects: influence on availability of phosphorus. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 581–605

    Google Scholar 

  2. Bates T, Lynch J (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538

    Article  CAS  Google Scholar 

  3. Calderon-Vazquez C, Ibarra-Laclette E, Caballero-Perez J, Herrera-Estrella L (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant-and species-specific levels. J Exp Bot 59:2479–2497

    Article  PubMed  CAS  Google Scholar 

  4. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su C (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. The Plant Cell Online 18:412–421

    Article  CAS  Google Scholar 

  5. Coello P (2002) Purification and characterization of secreted acid phosphatase in phosphorus-deficient Arabidopsis thaliana. Physiol Plant 116:293–298

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  8. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95:14863

    Article  PubMed  CAS  Google Scholar 

  9. Ezaki B, Yamamoto Y, Matsumoto H (1995) Cloning and sequencing of the cDNAs induced by aluminium treatment and Pi starvation in cultured tobacco cells. Physiol Plant 93:11–18

    Article  CAS  Google Scholar 

  10. Franco-Zorrilla JM, Gonzelez E, Bustos R, Linhares F, Leyva A, Paz-Ares res J (2004) The transcriptional control of plant responses to phosphate limitation. J Exp Bot 55:285–293

    Article  PubMed  CAS  Google Scholar 

  11. Franco-Zorrilla JM, Martan AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138:847–857

    Article  PubMed  CAS  Google Scholar 

  12. George E, Marschner H, Jakobsen I (1995) Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit Rev Biotechnol 15:257–270

    Article  Google Scholar 

  13. Haran S, Logendra S, Seskar M, Bratanova M, Raskin I (2000) Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. Plant Physiol 124:615–626

    Article  PubMed  CAS  Google Scholar 

  14. Hegeman CE, Grabau EA (2001) A novel phytase with sequence similarity to purple acid phosphatases is expressed in cotyledons of germinating soybean seedlings. Plant Physiol 126:1598–1608

    Article  PubMed  CAS  Google Scholar 

  15. Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767

    Article  PubMed  Google Scholar 

  16. Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes ofElsholtzia argyi. J Hazard Mater 154:914–926

    Article  PubMed  CAS  Google Scholar 

  17. Jin X, Yang X, Islam E, Liu D, Mahmood Q (2008) Effects of cadmium on ultrastructure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredii Hance. J Hazard Mater 156:387–397

    Article  PubMed  CAS  Google Scholar 

  18. Kai M, Takazumi K, Adachi H, Wasaki J, Shinano T, Osaki M (2002) Cloning and characterization of four phosphate transporter cDNAs in tobacco. Plant Sci 163:837–846

    Article  CAS  Google Scholar 

  19. Karthikeyan AS, Varadarajan DK, Mukatira UT, D’Urzo MP, Damsz B, Raghothama KG (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221–233

    Article  PubMed  CAS  Google Scholar 

  20. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918

    Article  PubMed  CAS  Google Scholar 

  21. Kouas S, Louche J, Debez A, Plassard C, Drevon JJ, Abdelly C (2009) Effect of phosphorus deficiency on acid phosphatase and phytase activities in common bean (Phaseolus vulgaris L.) under symbiotic nitrogen fixation. Symbiosis 47:141–149

    Article  CAS  Google Scholar 

  22. L Starnes D, Padmanabhan P, Sahi SV (2008) Effect of P sources on growth, P accumulation and activities of phytase and acid phosphatases in two cultivars of annual ryegrass (Lolium multiflorum L.). Plant Physiol Biochem 46:580–589

    Article  PubMed  Google Scholar 

  23. Li M, Osaki M, Madhusudana Rao I, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant Soil 195:161–169

    Article  Google Scholar 

  24. Li K, Xu C, Zhang K, Yang A, Zhang J (2007) Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants. Proteomics 7:1501–1512

    Article  PubMed  CAS  Google Scholar 

  25. Liu Z, He X, Chen W, Yuan F, Yan K, Tao D (2009) Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator–Lonicera japonica Thunb. J Hazard Mater 169:170–175

    Article  PubMed  CAS  Google Scholar 

  26. McLachlan K (1980) Acid phosphatase activity of intact roots and phosphorus nutrition in plants. 1. Assay conditions and phosphatase activity. Aust J Agric Res 31:429–440

    Article  CAS  Google Scholar 

  27. Miao J, Sun J, Liu D, Li B, Zhang A, Li Z, Tong Y (2009) Characterization of the promoter of phosphate transporterTaPHT1. 2 differentially expressed in wheat varieties. J Genet Genomics 36:455–466

    Article  PubMed  CAS  Google Scholar 

  28. Misra S, Miller GJ, Hurley JH (2001) Recognizing phosphatidylinositol 3-phosphate. Cell 107:559–562

    Article  PubMed  CAS  Google Scholar 

  29. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N (2005) 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

    Article  PubMed  CAS  Google Scholar 

  30. Morcuende R, Bari R, Gibon Y, Zheng W, PANT BD, BLÄSING O, USADEL B, Czechowski T, UDVARDI MK, Stitt M (2006) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    Article  Google Scholar 

  31. Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, BLÄSING O, Usadel B, Czechowski T, Udvardi MK, Stitt M (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    Article  PubMed  CAS  Google Scholar 

  32. Muchhal US, Raghothama K (1999) Transcriptional regulation of plant phosphate transporters. Proc Natl Acad Sci 96:5868

    Article  PubMed  CAS  Google Scholar 

  33. Muchhal US, Pardo JM, Raghothama K (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci 93:10519

    Article  PubMed  CAS  Google Scholar 

  34. Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31:341–353

    Article  PubMed  CAS  Google Scholar 

  35. Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–171

    Article  PubMed  CAS  Google Scholar 

  36. Nagy R, Vasconcelos M, Zhao S, McElver J, Bruce W, Amrhein N, Raghothama K, Bucher M (2006) Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol 8:186–197

    Article  PubMed  CAS  Google Scholar 

  37. Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 99:13324

    Article  PubMed  CAS  Google Scholar 

  38. Playsted CWS, Johnston ME, Ramage CM, Edwards DG, Cawthray GR, Lambers H (2006) Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytol 170:491–500

    Article  PubMed  CAS  Google Scholar 

  39. Priya P, Sahi SV (2009) Influence of phosphorus nutrition on growth and metabolism of Duo grass (Duo festulolium). Plant Physiol Biochem 47:31–36

    Article  PubMed  CAS  Google Scholar 

  40. Qiu RL, Zhao X, Tang YT, Yu FM, Hu PJ (2008) Antioxidative response to Cd in a newly discovered cadmium hyperaccumulator, Arabis paniculata F. Chemosphere 74:6–12

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  42. Raghothama K (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693

    Article  CAS  Google Scholar 

  43. Raghothama K, Karthikeyan A (2005) Phosphate acquisition. Plant Soil 274:37–49

    Article  CAS  Google Scholar 

  44. Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C (2005) Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum(Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere 60:97–104

    Article  PubMed  CAS  Google Scholar 

  45. Rubio V, Linhares F, Solano R, Martan 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 

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

    Article  PubMed  CAS  Google Scholar 

  47. Schenmann P, Richardson A, Smith F, Delhaize E (2004) Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). J Exp Bot 55:855–865

    Article  Google Scholar 

  48. Schünmann PHD, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1; 1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136:4205–4214

    Article  PubMed  Google Scholar 

  49. Sharma NC, Sahi SV (2005) Characterization of phosphate accumulation in Lolium multiflorum for remediation of phosphorus-enriched soils. Environ Sci Technol 39:5475–5480

    Article  PubMed  CAS  Google Scholar 

  50. Sharma NC, Starnes DL, Sahi SV (2007) Phytoextraction of excess soil phosphorus. Environ Pollut 146:120–127

    Article  PubMed  CAS  Google Scholar 

  51. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  PubMed  CAS  Google Scholar 

  52. Ticconi CA, Abel S (2004) Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci 9:548–555

    Article  PubMed  CAS  Google Scholar 

  53. Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, Desnos T, Abel S (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci 106:14174–14179

    Article  PubMed  CAS  Google Scholar 

  54. Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131:1064–1079

    Article  PubMed  CAS  Google Scholar 

  55. 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 

  56. Vitória AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710

    Article  PubMed  Google Scholar 

  57. Wang C, Ying S, Huang H, Li K, Wu P, Shou H (2009) Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57:895–904

    Article  PubMed  CAS  Google Scholar 

  58. Wasaki J, Yamamura T, Shinano T, Osaki M (2003) Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency. Plant Soil 248:129–136

    Article  CAS  Google Scholar 

  59. Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant, Cell Environ 26:1515–1523

    Article  CAS  Google Scholar 

  60. Wasaki J, Maruyama H, Tanaka M, Yamamura T, Dateki H, Shinano T, Ito S, Osaki M (2009) Overexpression of the LASAP2 gene for secretory acid phosphatase in white lupin improves the phosphorus uptake and growth of tobacco plants. Soil Sci Plant Nutr 55:107–113

    Article  CAS  Google Scholar 

  61. Xiao K, Harrison MJ, Wang ZY (2005) Transgenic expression of a novel M. truncatula phytase gene results in improved acquisition of organic phosphorus by Arabidopsis. Planta 222:27–36

    Article  PubMed  CAS  Google Scholar 

  62. Xiao K, Harrison M, Wang ZY (2006) Cloning and characterization of a novel purple acid phosphatase gene (MtPAP1) from Medicago truncatula Barrel Medic. J Integr Plant Biol 48:204–211

    Article  CAS  Google Scholar 

  63. Xiao K, Katagi H, Harrison M, Wang ZY (2006) Improved phosphorus acquisition and biomass production in Arabidopsis by transgenic expression of a purple acid phosphatase gene from M. truncatula. Plant Sci 170:191–202

    Article  CAS  Google Scholar 

  64. Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138:2087–2096

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National High Technology Research and Development Program of China (SS2012AA100107, 2012AA10A300), supported by Major Program of National Natural Science Foundation of China (2011AA10A103_2).

Author information

Authors and Affiliations

  1. Key Laboratory of Crop Genetic Resources and Improvement, Ministry of Education, Institute of Maize Research, Sichuan Agricultural University, Wenjiang, 611130, Sichuan, People’s Republic of China

    Hai-Jian Lin, Jian Gao, Zhi-Ming Zhang, Ya-Ou Shen, Hai Lan, Li Liu, Kui Xiang, Shufeng Zhou, Yong-Zhong Zhang, Shi-Bin Gao & Guang-Tang Pan

  2. Life Science College of Sichuan Agricultural University, Ya’an, Sichuan, People’s Republic of China

    Maojun Zhao

Authors
  1. Hai-Jian Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhi-Ming Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ya-Ou Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hai Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Li Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kui Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maojun Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shufeng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yong-Zhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Shi-Bin Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Guang-Tang Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guang-Tang Pan.

Additional information

Hai-Jian Lin and Jian Gao authors contributed equally to this study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 27 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, HJ., Gao, J., Zhang, ZM. et al. Transcriptional responses of maize seedling root to phosphorus starvation. Mol Biol Rep 40, 5359–5379 (2013). https://doi.org/10.1007/s11033-013-2636-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-013-2636-x

Keywords

Search

Navigation