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Overexpression of GbWRKY1 positively regulates the Pi starvation response by alteration of auxin sensitivity in Arabidopsis

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Overexpression of a cotton defense-related gene GbWRKY1 in Arabidopsis resulted in modification of the root system by enhanced auxin sensitivity to positively regulate the Pi starvation response.

Abstract

GbWRKY1 was a cloned WRKY transcription factor from Gossypium barbadense, which was firstly identified as a defense-related gene and showed moderate similarity with AtWRKY75 from Arabidopsis thaliana. Overexpression of GbWRKY1 in Arabidopsis resulted in attenuated Pi starvation stress symptoms, including reduced accumulation of anthocyanin and impaired density of lateral roots (LR) in low Pi stress. The study also indicated that overexpression of GbWRKY1 caused plants constitutively exhibited Pi starvation response including increased development of LR, relatively high level of total P and Pi, high expression level of some high-affinity Pi transporters and phosphatases as well as enhanced accumulation of acid phosphatases activity during Pi-sufficient. It was speculated that GbWRKY1 may act as a positive regulator in the Pi starvation response as well as AtWRKY75. GbWRKY1 probably involves in the modulation of Pi homeostasis and participates in the Pi allocation and remobilization but do not accumulate more Pi in Pi-deficient condition, which was different from the fact that AtWRKY75 influenced the Pi status of the plant during Pi deprivation by increasing root surface area and accumulation of more Pi. Otherwise, further study suggested that the overexpression plants were more sensitive to auxin than wild-type and GbWRKY1 may partly influence the LPR1-dependent (low phosphate response 1) Pi starvation signaling pathway and was putatively independent of SUMO E3 ligase SIZ1 and PHR1 (phosphate starvation response 1) in response to Pi starvation.

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References

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

    Article  PubMed  CAS  Google Scholar 

  • Blakely LM, Blakely RM, Colowit PM, Elliott DS (1988) Experimental studies on lateral root formation in radish seedling roots: II. Analysis of the dose-response to exogenous auxin. Plant Physiol 87:414–419

    Article  PubMed  CAS  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  PubMed  CAS  Google Scholar 

  • Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21:3554–3566

    Article  PubMed  CAS  Google Scholar 

  • Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206

    Article  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 

  • Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213

    PubMed  CAS  Google Scholar 

  • 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 

  • Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F, de los Santos B, Romero F, Pliego-Alfaro F, Munoz-Blanco J, Caballero JL (2009) Evidence for a positive regulatory role of strawberry (Fragaria × ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance. J Exp Bot 60:3043–3065

    Article  PubMed  CAS  Google Scholar 

  • Farquharson KL (2008) Phosphate-deprived roots are hypersensitive to auxin. Plant Cell 20:3183

    Article  PubMed  CAS  Google Scholar 

  • Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN, Tasaka M (1998) Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14:425–430

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132:578–596

    Article  PubMed  CAS  Google Scholar 

  • Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, Murphy AS, Raghothama KG (2007) 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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Koenig T, Hubl D, Dierks T, Jelic V, Wahlund LO, John ER, Prichep L (2002) Brain field dynamics in Alzheimer’s disease. Neurobiol Aging 23:S480–S480

    Google Scholar 

  • Linkohr BI, Williamson LC, Fitter AH, Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 137:681–691

    Article  PubMed  CAS  Google Scholar 

  • Matsuda F, Miyazawa H, Wakasa K, Miyagawa H (2005) Quantification of indole-3-acetic acid and amino acid conjugates in rice by liquid chromatography-electrospray ionization-tandem mass spectrometry. Biosci Biotechnol Biochem 69:778–783

    Article  PubMed  CAS  Google Scholar 

  • Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (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 

  • Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Jin JB, Hasegawa PM (2007) Sumoylation, a post-translational regulatory process in plants. Curr Opin Plant Biol 10:495–502

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155:1000–1012

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074

    Article  PubMed  CAS  Google Scholar 

  • Nilsson L, Muller 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 

  • Nilsson L, Lundmark M, Jensen PE, Nielsen TH (2012) The Arabidopsis transcription factor PHR1 is essential for adaptation to high light and retaining functional photosynthesis during phosphate starvation. Physiol Plant 144:35–47

    Article  PubMed  CAS  Google Scholar 

  • Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  PubMed  CAS  Google Scholar 

  • Perez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649

    Article  PubMed  CAS  Google Scholar 

  • Rieu I, Powers SJ (2009) Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell 21:1031–1033

    Article  PubMed  CAS  Google Scholar 

  • Robatzek S, Somssich IE (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. Plant J 28:123–133

    Article  PubMed  CAS  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  PubMed  CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  PubMed  CAS  Google Scholar 

  • Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498

    Article  PubMed  Google Scholar 

  • Wang XM, Du GK, Wang XM, Meng YJ, Li YY, Wu P, Yi KK (2010) The function of LPR1 is controlled by an element in the promoter and is independent of SUMO E3 ligase SIZ1 in response to low Pi stress in Arabidopsis thaliana. Plant Cell Physiol 51:380–394

    Article  PubMed  Google Scholar 

  • Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882

    Article  PubMed  CAS  Google Scholar 

  • Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, 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 

  • Xu L, Zhu L, Tu L, Guo X, Long L, Sun L, Gao W, Zhang X (2011) Differential gene expression in cotton defence response to Verticillium dahliae by SSH. J Phytopathol 159:606–615

    Article  CAS  Google Scholar 

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Acknowledgment

This study is financially supported by the National High-tech R&D Program of China (2011AA10A102) and the National Natural Science Foundation of China (30971822).

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Correspondence to Longfu Zhu.

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Communicated by P. Lakshmanan.

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Xu, L., Jin, L., Long, L. et al. Overexpression of GbWRKY1 positively regulates the Pi starvation response by alteration of auxin sensitivity in Arabidopsis. Plant Cell Rep 31, 2177–2188 (2012). https://doi.org/10.1007/s00299-012-1328-7

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  • DOI: https://doi.org/10.1007/s00299-012-1328-7

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