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Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation

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Abstract

In higher plants, phosphate (Pi) deficiency induces the replacement of phospholipids with the nonphosphorous glycolipids digalactosyldiacylglycerol (DGDG) and sulfoquinovosyldiacylglycerol (SQDG). Genes involved in membrane lipid remodeling are coactivated in response to Pi starvation, but the mechanisms that guide this response are largely unknown. Previously, we reported the importance of auxin transport for DGDG accumulation during Pi starvation. To understand the role of auxin signaling in Arabidopsis membrane lipid remodeling, we analyzed slr-1, a gain-of-function mutant of IAA14 (a repressor of auxin signaling), and arf7arf19, a loss-of-function mutant of auxin response factors ARF7 and ARF19. In slr-1 and arf7arf19, Pi stress-induced accumulation of DGDG and SQDG was suppressed. Reduced upregulation of glycolipid synthase and phospholipase genes in these mutants under Pi-deficient conditions indicates that IAA14 and ARF7/19 affect membrane lipid remodeling at the level of transcription. Pi stress-dependent induction of a non-protein-coding gene, IPS1, was also lower in slr-1 and arf7arf19, whereas expression of At4 (another Pi stress-inducible non-protein-coding gene), anthocyanin accumulation, and phosphodiesterase induction were not reduced in the shoot. High free Pi content was observed in slr-1 and arf7arf19 even under Pi-deficient conditions, suggesting that Pi homeostasis during Pi starvation is altered in these mutants. These results demonstrate a requirement of auxin signaling mediated by IAA14 and ARF7/19 for low-Pi adaptation in Arabidopsis.

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References

  • Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–132. doi:10.1016/S0014-5793(03)00109-1

    Article  CAS  PubMed  Google Scholar 

  • Andersson MX, Larsson KE, Tjellstrom H, Liljenberg C, Sandelius AS (2005) Phosphate-limited oat. The plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280:27578–27586. doi:10.1074/jbc.M503273200

    Article  CAS  PubMed  Google Scholar 

  • Awai K, Maréchal E, Block MA, Brun D, Masuda T, Shimada H, Takamiya K, Ohta H, Joyard J (2001) Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:10960–10965. doi:10.1073/pnas.181331498

    Article  CAS  PubMed  Google Scholar 

  • Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999. doi:10.1104/pp.106.079707

    Article  CAS  PubMed  Google Scholar 

  • Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorous availability. Plant Cell Environ 19:529–538. doi:10.1111/j.1365-3040.1996.tb00386.x

    Article  CAS  Google Scholar 

  • Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280:2397–2400. doi:10.1074/jbc.R400032200

    Article  CAS  PubMed  Google Scholar 

  • Bensadoun A, Weinstein D (1976) Assay of proteins in the presence of interfering materials. Anal Biochem 70:241–250. doi:10.1016/S0003-2697(76)80064-4

    Article  CAS  PubMed  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:412–421. doi:10.1105/tpc.105.038943

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103:6765–6770. doi:10.1073/pnas.0600863103

    Article  PubMed  Google Scholar 

  • Essigmann B, Güler S, Narang RA, Linke D, Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 95:1950–1955

    Article  CAS  PubMed  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037. doi:10.1038/ng2079

    Article  CAS  PubMed  Google Scholar 

  • Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168. doi:10.1046/j.0960-7412.2001.01201.x

    Article  CAS  PubMed  Google Scholar 

  • Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44:382–395. doi:10.1111/j.1365-313X.2005.02537.x

    Article  CAS  PubMed  Google Scholar 

  • Fukaki H, Taniguchi N, Tasaka M (2006) PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J 48:380–389. doi:10.1111/j.1365-313X.2006.02882.x

    Article  CAS  PubMed  Google Scholar 

  • Gaude N, Nakamura Y, Scheible WR, Ohta H, Dörmann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56:28–39. doi:10.1111/j.1365-313X.2008.03582.x

    Article  CAS  PubMed  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460. doi:10.1016/j.pbi.2007.08.014

    Article  CAS  PubMed  Google Scholar 

  • Härtel H, Dörmann P, Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97:10649–10654. doi:10.1073/pnas.180320497

    Article  PubMed  Google Scholar 

  • Holford ICR (1997) Soil phosphorus: its measurements and its uptake by plants. Aust J Soil Res 35:227–239

    Article  CAS  Google Scholar 

  • Hölzl G, Dörmann P (2007) Structure and function of glycoglycerolipids in plants and bacteria. Prog Lipid Res 46:225–243. doi:10.1016/j.plipres.2007.05.001

    Article  PubMed  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. doi:10.1104/pp.106.092130

    Article  CAS  PubMed  Google Scholar 

  • Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J, Block MA (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167:863–874. doi:10.1083/jcb.200407022

    Article  CAS  PubMed  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. doi:10.1104/pp.020007

    Article  CAS  PubMed  Google Scholar 

  • Kelly AA, Froehlich JE, Dörmann P (2003) Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 15:2694–2706. doi:10.1105/tpc.016675

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Awai K, Takamiya K, Ohta H (2004) Arabidopsis type B monogalactosyldiacylglycerol synthase genes are expressed during pollen tube growth and induced by phosphate starvation. Plant Physiol 134:640–648. doi:10.1104/pp.103.032656

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Masuda T, Takamiya K, Ohta H (2006) Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J 47:238–248. doi:10.1111/j.1365-313X.2006.02778.x

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Kondo M, Fukuda H, Nishimura M, Ohta H (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc Natl Acad Sci USA 104:17216–17221. doi:10.1073/pnas.0704680104

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Awai K, Nakamura M, Nagatani A, Masuda T, Ohta H (2009) Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation. Plant J 57:322–331. doi:10.1111/j.1365-313X.2008.03692.x

    Article  CAS  PubMed  Google Scholar 

  • Lai F, Thacker J, Li Y, Doerner P (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50:545–556. doi:10.1111/j.1365-313X.2007.03070.x

    Article  CAS  PubMed  Google Scholar 

  • Li M, Qin C, Welti R, Wang X (2006a) Double knockouts of phospholipases Dzeta1 and Dzeta2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770. doi:10.1104/pp.105.070995

    Article  CAS  PubMed  Google Scholar 

  • Li M, Welti R, Wang X (2006b) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases D zeta1 and D zeta2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142:750–761. doi:10.1104/pp.106.085647

    Article  CAS  PubMed  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. doi:10.1104/pp.010934

    Article  PubMed  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287. doi:10.1016/S1369-5266(03)00035-9

    Article  PubMed  Google Scholar 

  • Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Peña A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:559–567. doi:10.1111/j.1365-313X.2000.00893.x

    Article  PubMed  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. doi:10.1073/pnas.0500778102

    Article  CAS  PubMed  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. doi:10.1046/j.1365-313X.2002.01356.x

    Article  CAS  PubMed  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. doi:10.1104/pp.105.060061

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Awai K, Masuda T, Yoshioka Y, Takamiya K, Ohta H (2005) A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J Biol Chem 280:7469–7476. doi:10.1074/jbc.M408799200

    Article  CAS  PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463. doi:10.1105/tpc.104.028316

    Article  CAS  PubMed  Google Scholar 

  • Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130. doi:10.1105/tpc.106.047761

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Torres CA, López-Bucio J, Cruz-Ramírez 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. doi:10.1105/tpc.108.058719

    Article  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martín 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. doi:10.1101/gad.204401

    Article  CAS  PubMed  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. doi:10.1093/pcp/pci011

    Article  PubMed  Google Scholar 

  • Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642. doi:10.1111/j.1365-313X.2004.02161.x

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Abel S (2004) Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci 9:548–555. doi:10.1016/j.tplants.2004.09.003

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Delatorre CA, Abel S (2001) Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol 127:963–972. doi:10.1104/pp.127.3.963

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623. doi:10.1105/tpc.7.10.1611

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868. doi:10.1126/science.276.5320.1865

    Article  CAS  PubMed  Google Scholar 

  • Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, Inzé D, Fukaki H, Beeckman T (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17:3035–3050. doi:10.1105/tpc.105.035493

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Yi K, Tao Y, Wang F, Wu Z, Jiang D, Chen X, Zhu L, Wu P (2006) Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ 29:1924–1935. doi:10.1111/j.1365-3040.2006.01568.x

    Article  CAS  PubMed  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130. doi:10.1111/j.1365-313X.2005.02432.x

    Article  CAS  PubMed  Google Scholar 

  • Yu B, Xu C, Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99:5732–5737. doi:10.1073/pnas.082696499

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas (No. 18056007 and No. 20053005) from the Ministry of Education, Sports, Science and Culture in Japan. K.K. was supported by a research fellowship of the Japan Society for the Promotion of Science for young scientists. T.N. was supported by the Grant of the 21st Century COE Program.

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Authors and Affiliations

  1. Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259-B-65 Nagatsuta-cho, Midori-ku, Yokohama, 226-8501, Japan

    Takafumi Narise, Koichi Kobayashi & Shinsuke Baba

  2. Department of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo, Komaba 3-8-1, Tokyo, 153-8902, Japan

    Koichi Kobayashi

  3. Center for Biological Resources and Informatics, Tokyo Institute of Technology, 4259-B-65 Nagatsuta-cho, Midori-ku, Yokohama, 226-8501, Japan

    Mie Shimojima, Shinji Masuda & Hiroyuki Ohta

  4. Research Center for the Evolving Earth and Planets, Tokyo Institute of Technology, 4259-B-65 Nagatsuta-cho, Midori-ku, Yokohama, 226-8501, Japan

    Mie Shimojima & Hiroyuki Ohta

  5. Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, Kobe, 657-8501, Japan

    Hidehiro Fukaki

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  1. Takafumi Narise
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  2. Koichi Kobayashi
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Correspondence to Hiroyuki Ohta.

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Takafumi Narise and Koichi Kobayashi contributed equally to this work.

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11103_2009_9589_MOESM1_ESM.pdf

Table S1. Primers used for quantitative real-time PCR analysis. Primers for MGD1, MGD2, DGD1, DGD2, SQD1, SQD2, NPC4 and NPC5 were designed to avoid non-specific amplifications and primer dimerization. (PDF 27 kb)

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Narise, T., Kobayashi, K., Baba, S. et al. Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation. Plant Mol Biol 72, 533–544 (2010). https://doi.org/10.1007/s11103-009-9589-4

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