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PRD, an Arabidopsis AINTEGUMENTA-like gene, is involved in root architectural changes in response to phosphate starvation

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Abstract

Changes in root architecture are one of the adaptive strategies used by plants to compensate for local phosphate (Pi) deficiency in soils. Root architecture variables triggered by Pi availability are well documented in Arabidopsis (Arabidopsis thaliana), but the molecular mechanisms behind these adaptive responses remain to be elucidated. By the use of transcriptomic and quantitative RT-PCR analysis, we observed that an AINTEGUMENTA-like gene, named PRD for Phosphate Root Development, was rapidly repressed in roots under low Pi conditions. The physiological function of the PRD gene was analyzed through the null allele mutant prd, which displayed less development of primary and lateral roots under Pi-starvation conditions than wild-type plants. Complementation of the prd mutant with the wild-type gene led to a similar response to Pi starvation as wild-type plants, indicating the complete rescue of the mutant phenotype. These results suggest that PRD gene is involved in the regulation of root architectural responses to Pi starvation by controlling primary and lateral root elongation. This model is in agreement with the tissue-specific pattern of PRD gene expression, which was observed to occur specifically in the apex in both the primary and lateral roots. However, Pi influx, anionic profiles and root expression of genes typically induced by Pi starvation, such as high affinity Pi transporters (PHT1;1 and PHT1;4) and an acid phosphatase (AtACP5), were similar in wild type and prd plants in response to Pi starvation. These results support the hypothesis that the PRD gene is not a checkpoint for Pi-starvation responses, but acts specifically as a regulator of root architectural responses to Pi starvation.

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Abbreviations

BSA:

Bovine serum albumin

EST:

Expressed sequence tag

PBS:

Phosphate buffer saline

QTL:

Quantitative trait locus

RT-PCR:

Real-time PCR

SSC:

Sodium sodium citrate

References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  PubMed  CAS  Google Scholar 

  • Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, Rossignol M, Tardieu F, Doumas P (2003) Temporal response of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant Cell Environ 26:1053–1066

    Article  CAS  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, Van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Drews GN, Meyerowitz EM (1991) Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell 3:749–758

    Article  PubMed  CAS  Google Scholar 

  • Chen DL, Delatorre CA, Bakker A, Abel S (2000) Conditional identification of phosphate-starvation-response mutants in Arabidopsis thaliana. Planta 211:13–22

    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 

  • 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 

  • El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian JC (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241

    Article  PubMed  CAS  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Benkova E, Mayer U, Palme K, Muster G (2003) Automated whole mount localisation techniques for plant seedlings. Plant J 34:115–124

    Article  PubMed  CAS  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  PubMed  CAS  Google Scholar 

  • Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swamp 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 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  CAS  Google Scholar 

  • Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153

    Article  PubMed  CAS  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 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón 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  Google Scholar 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-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  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) 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 

  • 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 

  • Nole-Wilson S, Tranby T, Krizek BA (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 57:613–628

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    Article  CAS  Google Scholar 

  • Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T (2006) Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 29:115–125

    Article  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 

  • Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184

    Article  PubMed  Google Scholar 

  • Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (2006) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiol 140:879–889

    Article  PubMed  Google Scholar 

  • Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124:1477–1480

    Article  PubMed  CAS  Google Scholar 

  • Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796

    Article  PubMed  CAS  Google Scholar 

  • Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801–814

    Article  PubMed  CAS  Google Scholar 

  • Tranbarger TJ, Al-Ghazi Y, Muller B, Doumas P, Touraine B (2003) Transcription factor gene with expression correlated to nitrate-related root plasticity of Arabidopsis thaliana. Plant Cell Environ 26:459–469

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wasaki J, Shimano T, Onishi K, Yonetami R, Yazaki J, Fujii F, Shimbo K, Ishikawa M, Shimatani Z, Nagata Y, Hashimoto A, Ohta T, Sato Y, Miyamoto C, Honda S, Kojima K, Sasaki T, Kishimoto N, Kikuchi S, Osaki M (2006) Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves. J Exp Bot 57:2049–2059

    Article  PubMed  CAS  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 

  • 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 

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Acknowledgments

This work was supported in part by the INRA ECOGENE programme. JJCC and JR received a research fellowship from Consejeria de Educacion y Ciencia (Junta de Andalucía, Spain).

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Correspondence to Patrick Doumas.

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Camacho-Cristóbal, J.J., Rexach, J., Conéjéro, G. et al. PRD, an Arabidopsis AINTEGUMENTA-like gene, is involved in root architectural changes in response to phosphate starvation. Planta 228, 511–522 (2008). https://doi.org/10.1007/s00425-008-0754-9

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  • DOI: https://doi.org/10.1007/s00425-008-0754-9

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