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Transcription factors involved in acid stress responses in plants

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Abstract

With the fast growth of world population and climate change, agricultural production is being a main global issue and challenge. Leading to deficiencies of several essential elements and toxicity of heavy metals in plants, acid soil is one of the most important limitations to crop productivity worldwide. Although lime is widely used to ameliorate acid soil, it is not economic and ideal. Identification of the mechanisms and genes conferring tolerance to acid soil stress could be an alternative way to improve the productivity in acid soil through breeding tolerant crops. Aluminum (Al) toxicity and phosphorous (P) deficiency are considered as two severe constraints to plant growth in acid soil. Several genes related to tolerance to Al toxicity and P deficiency have been identified and analysed in various crop plants. This review describes the current understanding of transcription factors involved in the transcriptional regulation of tolerance to Al toxicity and P deficiency in Arabidopsis and rice.

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References

  1. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M. A novel mode of DNA recognition by a β-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J. 1998;17:5484–96.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408:796–815.

    Article  Google Scholar 

  3. Arenhart RA, Bai Y, de Oliveira LF, Neto LB, Schunemann M, Maraschin Fdos S, et al. New insights into aluminum tolerance in rice: the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol Plant. 2014;7(4):709–21.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Arenhart RA, Schunemann M, Bucker Neto L, Margis R, Wang ZY, Margis-Pinheiro M (2015) Rice ASR1 and ASR5 are complementary transcription factors regulating aluminum responsive genes. Plant Cell Environ

  5. Baek D, Kim MC, Chun HJ, Kang S, Park HC, Shin G, et al. Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol. 2013;161(1):362–73.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Baek D, Park HC, Kim MC, Yun DJ. The role of Arabidopsis MYB2 in miR399f-mediated phosphate-starvation response. Plant Signal Behav. 2013;8(3), e23488.

    Article  PubMed Central  PubMed  Google Scholar 

  7. Belal R, Tang R, Li Y, Mabrouk Y, Badr E, Luan S. An ABC transporter complex encoded by Aluminum Sensitive 3 and NAP3 is required for phosphate deficiency responses in Arabidopsis. Biochem Biophys Res Commun. 2015;463(1–2):18–23.

    Article  CAS  PubMed  Google Scholar 

  8. Briat JF, Rouached H, Tissot N, Gaymard F, Dubos C. Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Front Plant Sci. 2015;6:290.

    Article  PubMed Central  PubMed  Google Scholar 

  9. Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, et al. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 2010;6, e1001102.

    Article  PubMed Central  PubMed  Google Scholar 

  10. Chandrika NN, Sundaravelpandian K, Yu SM, Schmidt W. ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis. New Phytol. 2013;198(3):709–20.

    Article  CAS  PubMed  Google Scholar 

  11. Chen ZH, Nimmo GA, Jenkins GI, Nimmo HG. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem J. 2007;405:191–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Chen CY, Schmidt W. The paralogous R3 MYB proteins CAPRICE, TRIPTYCHON and ENHANCER OF TRY AND CPC1 play pleiotropic and partly non-redundant roles in the phosphate starvation response of Arabidopsis roots. J Exp Bot. 2015;66(15):4821–34.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP. An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics. 2008;179(1):669–82.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Cominelli E, Tonelli C. Transgenic crops coping with water scarcity. N Biotechnol. 2010;27(5):473–7.

    Article  CAS  PubMed  Google Scholar 

  15. Dai X, Wang Y, Yang A, Zhang WH. OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol. 2012;159(1):169–83.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Delhaize E, Ma JF, Ryan PR. Transcriptional regulation of aluminum tolerance genes. Trends Plant Sci. 2012;17(6):341–8.

    Article  CAS  PubMed  Google Scholar 

  17. Devaiah BN, Karthikeyan AS, Raghothama KG. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 2007;143:1789–801.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Devaiah BN, Nagarajan VK, Raghothama KG. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol. 2007;145:147–59.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant. 2009;2:43–58.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Ding ZJ, Yan JY, Xu XY, Li GX, Zheng SJ. WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J. 2013;76(5):825–35.

    Article  CAS  PubMed  Google Scholar 

  21. Ernst HA, Olsen AN, Larsen S, Lo LL. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep. 2004;5:297–303.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Eulgem T, Somssich IE. Networks of WRKY transcription factors in defense signaling. CurrOpin Plant Biol. 2007;10(4):366–71.

    CAS  Google Scholar 

  23. Famoso AN, Clark RT, Shaff JE, Craft E, McCouch SR, Kochian LV. Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol. 2010;153:1678–91.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Fan W, Lou HQ, Gong YL, Liu MY, Cao MJ, Liu Y, et al. Characterization of an inducible C2 H2 -type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytol. 2015;208(2):456–68.

    Article  CAS  PubMed  Google Scholar 

  25. Garcia-Oliveira AL, Benito C, Prieto P, de Andrade MR, Rodrigues-Pousada C, Guedes-Pinto H, et al. Molecular characterization of TaSTOP1 homoeologues and their response to aluminium and proton (H(+)) toxicity in bread wheat (Triticum aestivum L.). BMC Plant Biol. 2013;13:134.

    Article  PubMed Central  PubMed  Google Scholar 

  26. González-Mendoza V, Zurita-Silva A, Sánchez-Calderón L, Sánchez-Sandoval ME, Oropeza-Aburto A, Gutiérrez-Alanís D, Alatorre-Cobos F, Herrera-Estrella L (2013) APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability. Plant Sci 205–206:2–12

  27. Gruber BD, Ryan PR, Richardson AE, Tyerman SD, Ramesh S, Hebb DM, et al. HvALMT1 from barley is involved in the transport of organic anions. J Exp Bot. 2010;61:1455–67.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Haling RE, Simpson RJ, Delhaize E, Hocking PJ, Richardson AE. Effect of lime on root growth, morphology and the rhizosheath of cereal seedlings growing in an acid soil. Plant Soil. 2010;327:199–212.

    Article  CAS  Google Scholar 

  29. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M. Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 2003;34(5):733–9.

    Article  CAS  PubMed  Google Scholar 

  30. Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J, Kobayashi Y, et al. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci U S A. 2006;103(25):9738–43.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, et al. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol. 2011;156(3):1101–15.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell. 2009;21:655–67.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Huang CF, Yamaji N, Chen Z, Ma JF. A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J. 2012;69(5):857–67.

    Article  CAS  PubMed  Google Scholar 

  34. Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Kobayashi Y, et al. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci U S A. 2007;104(23):9900–5.

    Article  PubMed Central  PubMed  Google Scholar 

  35. Ikeda M, Ohme-Takagi M. A novel group of transcriptional repressors in Arabidopsis. Plant Cell Physiol. 2009;50:970–5.

    Article  CAS  PubMed  Google Scholar 

  36. Ikka T, Kobayashi Y, Iuchi S, Sakurai N, Shibata D, Kobayashi M, et al. Natural variation of Arabidopsis thaliana reveals that aluminum resistance and proton resistance are controlled by different genetic factors. Theor Appl Genet. 2007;115(5):709–19.

    Article  CAS  PubMed  Google Scholar 

  37. Jain A, Nagarajan VK, Raghothama KG. Transcriptional regulation of phosphate acquisition by higher plants. Cell Mol Life Sci. 2012;69(19):3207–24.

    Article  CAS  PubMed  Google Scholar 

  38. Kobayashi K, Masuda T, Takamiya K, Ohta H. Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J. 2006;47(2):238–48.

    Article  CAS  PubMed  Google Scholar 

  39. Kobayashi Y, Ohyama Y, Kobayashi Y, Ito H, Iuchi S, Fujita M, et al. STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol Plant. 2014;7(2):311–22.

    Article  CAS  PubMed  Google Scholar 

  40. Kochian LV, Hoekenga OA, Pineros MA. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol. 2004;55:459–93.

    Article  CAS  PubMed  Google Scholar 

  41. Kochian LV, Piñeros MA, Liu J, Magalhaes JV. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol. 2015;66:571–98.

    Article  CAS  PubMed  Google Scholar 

  42. Larsen PB, Geisler MJ, Jones CA, Williams KM, Cancel JD. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J. 2005;41:353–63.

    Article  CAS  PubMed  Google Scholar 

  43. Larsen PB, Cancel J, Rounds M, Ochoa V. Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta. 2007;225:1447–58.

    Article  CAS  PubMed  Google Scholar 

  44. Li XF, Ma JF, Matsumoto H. Pattern of Al-induced secretion of organic acids differs between rye and wheat. Plant Physiol. 2000;123:1537–43.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Liang C, Piñeros MA, Tian J, Yao Z, Sun L, Liu J, et al. Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol. 2013;161(3):1347–61.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Ligaba A, Maron L, Shaff J, Kochian L, Piñeros M. Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux. Plant Cell Environ. 2012;35:1185–200.

    Article  CAS  PubMed  Google Scholar 

  47. Liu J, Magalhaes JV, Shaff J, Kochian LV. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J. 2009;57:389–99.

    Article  CAS  PubMed  Google Scholar 

  48. Liu J, Piňeros MA, Kochian LV. The role of aluminum sensing and signaling in plant aluminum resistance. J Integr Plant Biol. 2014;56(3):221–30.

    Article  CAS  PubMed  Google Scholar 

  49. Liu X, Zhou J, Li W, Xu J, Brookes PC. The combined effects of urea application and simulated acid rain on soil acidification and microbial community structure. Environ Sci Pollut Res Int. 2014;21(10):6623–31.

    Article  CAS  PubMed  Google Scholar 

  50. Ma JF, Ryan PR, Delhaize E. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 2001;6:273–8.

    Article  CAS  PubMed  Google Scholar 

  51. Ma JF. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol. 2007;264:225–52.

    Article  CAS  PubMed  Google Scholar 

  52. Maron LG, Piñeros MA, Guimarães CT, Magalhaes JV, Pleiman JK, Mao C, et al. Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J. 2010;61:728–40.

    Article  CAS  PubMed  Google Scholar 

  53. Matsui K, Umemura Y, Ohme-Takagi M. AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J. 2008;55:954–67.

    Article  CAS  PubMed  Google Scholar 

  54. Mattiello L, Kirst M, da Silva FR, Jorge RA, Menossi M. Transcriptional profile of maize roots under acid soil growth. BMC Plant Biol. 2010;10:196.

    Article  PubMed Central  PubMed  Google Scholar 

  55. Metali F, Salim KA, Burslem DF. Evidence of foliar aluminum accumulation in local, regional and global datasets of wild plants. New Phytol. 2011;193:637–49.

    Article  PubMed  Google Scholar 

  56. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A. 2005;102:11934–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS. Responses of root architecture development to low phosphorus availability: a review. Ann Bot. 2013;112(2):391–408.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, et al. Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci. 2011;2:83.

    Article  PubMed Central  PubMed  Google Scholar 

  59. Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M. Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell. 2001;13:1959–68.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Ohyama Y, Ito H, Kobayashi Y, Ikka T, Morita A, Kobayashi M, et al. Characterization of AtSTOP1 orthologous genes in tobacco and other plant species. Plant Physiol. 2013;162(4):1937–46.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Panda SK, Baluska F, Matsumoto H. Aluminum stress signaling in plants. Plant Signal Behav. 2009;4(7):592–7.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Pereira JF, Zhou G, Delhaize E, Richardson T, Zhou M, Ryan PR. Engineering greater aluminum resistance in wheat by over-expressing TaALMT1. Ann Bot. 2010;106:205–14.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Péret B, Clément M, Nussaume L, Desnos T. Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci. 2011;16(8):442–50.

    Article  PubMed  Google Scholar 

  64. Ramaiah M, Jain A, Raghothama KG. Ethylene Response Factor070 regulates root development and phosphate starvation-mediated responses. Plant Physiol. 2014;164(3):1484–98.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, KeddieJ AL, et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 2000;290:2105–10.

    Article  CAS  PubMed  Google Scholar 

  66. Ruan W, Guo M, Cai L, Hu H, Li C, Liu Y, et al. Genetic manipulation of a high-affinity PHR1 target cis-element to improve phosphorous uptake in Oryza sativa L. Plant Mol Biol. 2015;87(4–5):429–40.

    Article  CAS  PubMed  Google Scholar 

  67. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 2001;15:2122–33.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, et al. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 2004;37:645–53.

    Article  CAS  PubMed  Google Scholar 

  69. Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T, Sakurai N, et al. STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol. 2009;150:281–94.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  70. Sawaki Y, Kobayashi Y, Kihara-Doi T, Nishikubo N, Kawazu T, Kobayashi M, et al. Identification of a STOP1-like protein in Eucalyptus that regulates transcription of Al tolerance genes. Plant Sci. 2014;223:8–15.

    Article  CAS  PubMed  Google Scholar 

  71. Schünmann PH, Richardson AE, Smith FW, Delhaize E. Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeumvulgare L.). J Exp Bot. 2004;55(398):855–65.

    Article  PubMed  Google Scholar 

  72. Schünmann PH, Richardson AE, Vickers CE, Delhaize E. Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol. 2004;136(4):4205–14.

    Article  PubMed Central  PubMed  Google Scholar 

  73. Shen C, Wang S, Zhang S, Xu Y, Qian Q, Qi Y, et al. OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.). Plant Cell Environ. 2013;36(3):607–20.

    Article  CAS  PubMed  Google Scholar 

  74. Shavrukov Y, Hirai Y. Good and bad protons: genetic aspects of acidity stress responses in plants. J Exp Bot. 2016;67(1):15–30.

    Article  PubMed  Google Scholar 

  75. Stass A, Smit I, Eticha D, Oettler G, Horst WJ. The significance of organic-anion exudation for the aluminum resistance of primary triticale derived from wheat and rye parents differing in aluminum resistance. J Plant Nutr Soil Sci. 2008;171:634–42.

    Article  CAS  Google Scholar 

  76. Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R, et al. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J. 2010;64(5):775–89.

    Article  CAS  PubMed  Google Scholar 

  77. Ticconi CA, Abel S. Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci. 2004;9(11):548–55.

    Article  CAS  PubMed  Google Scholar 

  78. Tokizawa M, Kobayashi Y, Saito T, Kobayashi M, Iuchi S, Nomoto M, et al. SENSITIVE TO PROTON RHIZOTOXICITY1, CALMODULIN BINDING TRANSCRIPTION ACTIVATOR2, and other transcription factors are involved in ALUMINUM-ACTIVATED MALATE TRANSPORTER1 expression. Plant Physiol. 2015;167(3):991–1003.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  79. Tsutsui T, Yamaji N, Ma JF. Identification of a cis-acting element of ART1, a C2H2-type zinc-finger transcription factor for aluminum tolerance in rice. Plant Physiol. 2011;156:925–31.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  80. Ulker B, Somssich IE. WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol. 2004;7(5):491–8.

    Article  PubMed  Google Scholar 

  81. Wang S, Zhang S, Sun C, Xu Y, Chen Y, Yu C, et al. Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytol. 2014;201(1):91–103.

    Article  CAS  PubMed  Google Scholar 

  82. Woo J, MacPherson CR, Liu J, Wang H, Kiba T, Hannah MA, et al. The response and recovery of the Arabidopsis thaliana transcriptome to phosphate starvation. BMC Plant Biol. 2012;12:62.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, et al. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 2003;132:1260–71.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  84. Wu P, Shou H, Xu G, Lian X. Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol. 2013;16(2):205–12.

    Article  CAS  PubMed  Google Scholar 

  85. Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K. Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci U S A. 1999;96:15336–41.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  86. Xia J, Yamaji N, Kasai T, Ma JF. Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci U S A. 2010;107(43):18381–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  87. Yamaguchi M, Sasaki T, Sivaguru M, Yamamoto Y, Osawa H, Ahn SJ, et al. Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). Plant Cell Physiol. 2005;46:812–6.

    Article  CAS  PubMed  Google Scholar 

  88. Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, et al. A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell. 2009;21:3339–49.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  89. Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, et al. A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J Mol Biol. 2004;337:49–63.

    Article  CAS  PubMed  Google Scholar 

  90. Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, et al. Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell. 2005;17:944–56.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  91. Yokosho K, Yamaji N, Ma JF. An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J. 2011;68:1061–9.

    Article  CAS  PubMed  Google Scholar 

  92. Yang WT, Baek D, Yun DJ, Hwang WH, Park DS, Nam MH, et al. Overexpression of OsMYB4P, an R2R3-type MYB transcriptional activator, increases phosphate acquisition in rice. Plant Physiol Biochem. 2014;80:259–67.

    Article  CAS  PubMed  Google Scholar 

  93. Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, et al. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol. 2005;138(4):2087–96.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  94. Zhang WH, Ryan PR, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD. Characterization of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotianatabacum L.) cells. Plant Cell Physiol. 2008;49(9):1316–30.

    Article  CAS  PubMed  Google Scholar 

  95. Zhou J, Jiao F, Wu Z, Li Y, Wang X, He X, et al. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol. 2008;146(4):1673–86.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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  1. Graduate School of Science and Engineering, Saitama University, Saitama, 338-8570, Japan

    Chuan-Ming Yeh & Masaru Ohme-Takagi

  2. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tukuba, Ibaraki, 305-8566, Japan

    Masaru Ohme-Takagi

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Yeh, CM., Ohme-Takagi, M. Transcription factors involved in acid stress responses in plants. Nucleus 58, 191–197 (2015). https://doi.org/10.1007/s13237-016-0159-2

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