Overexpression of the MYB-related transcription factor GCC7 in Arabidopsis thaliana leads to increased levels of Pi and changed P-dependent gene regulation
Maria Lundmark A B , Lena Nilsson A B , Camilla J. Kørner A and Tom H. Nielsen A C
+ Author Affiliations
- Author Affiliations
A Section for Plant Molecular Biology, VKR centre Pro-Active Plants, Department of Plant Biology and Biotechnology, Faculty of Life Sciences, University of Copenhagen, Copenhagen, Denmark.
B These authors contributed equally to the work.
C Corresponding author. Email: thni@life.ku.dk
Functional Plant Biology 38(2) 151-162 https://doi.org/10.1071/FP10081
Submitted: 13 April 2010 Accepted: 24 November 2010 Published: 1 February 2011
Abstract
A proper concentration and turnover of inorganic phosphate (Pi) is essential to maintain cellular processes. Consequently, plants have mechanisms to control Pi homeostasis and to alleviate Pi limitation. The MYB-related transcription factor, PHR1, is important for gene induction during Pi starvation. PHR1 belongs to a family, characterised by the presence of a GARP- and a coiled coil domain. We propose that this family, with 15 members in Arabidopsis thaliana (L.) Heynh., be termed the GCC-family. In this study, transgenic plants overexpressing one member, GCC7, and a T-DNA knockout mutant, gcc7, are characterised. We find overexpressor plants to accumulate more Pi in shoots, irrespective of the Pi supply. Therefore, GCC7 was characterised in relation to Pi starvation. We conclude that GCC7 is not strictly required for a P-starvation response since the gcc7 mutant responds to Pi limitation. However, overexpression of GCC7 strongly interferes with the P-starvation response, abolishing induction of several P-responsive genes including AT4, IPS1 and several P-transporter genes, whereas GCC7 does not directly interfere with the PHR1 (GCC1) dependent regulation of miR399d. Thus GCC7 influences P-accumulation and P-dependent gene regulation, but GCC7 has a function entirely different from PHR1.
Additional keywords: gene regulation, nutrient depletion, phosphate transporters.
References
Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, A phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiology 141, 1000–1011.| pho2, A phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1Ogtrw%3D&md5=abb594087e9f47c312a3a7fa1a669c94CAS | 16679417PubMed |
Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141, 988–999.
| PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1Ogtr8%3D&md5=197dd6fbe5b489d886e82dc7087d51f2CAS | 16679424PubMed |
Beutler HO (1984) Monosaccharides and derivatives. In ‘Methods of enzymatic analysis’. (Ed. HU Bergmeyer) pp. 331–337. (Verlag Chemie: Weinheim, Germany)
Bonke M, Thitamadee S, Mähönen AP, Hauser MT, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426, 181–186.
| APL regulates vascular tissue identity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovVKmtb0%3D&md5=fa9b54661a58aba26d6c11173cfac170CAS | 14614507PubMed |
Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A, Paz-Ares J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genetics 6, e1001102
| A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 20838596PubMed |
Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. The Plant Cell 18, 412–421.
| Regulation of phosphate homeostasis by microRNA in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhs1egu7c%3D&md5=a17ba36b63168bbd1fd10c84f9d8b370CAS | 16387831PubMed |
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
| Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7mvVagsQ%3D%3D&md5=c9ab40d4c4c5e8216321cb905f7c65b8CAS | 10069079PubMed |
Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiology 107, 207–213.
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. Nature Genetics 39, 1033–1037.
| Target mimicry provides a new mechanism for regulation of microRNA activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1CmsLY%3D&md5=c31d0534db7160d17e9b8ee5ebcc2803CAS | 17643101PubMed |
Goloboff P (1998) NONA. Computer program and software. Available at http://www.cladistics.com/aboutNona.htm [Verified 13 December 2010]
Guo B, Jin Y, Wussler C, Blancaflor EB, Motes CM, Versaw WK (2008) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytologist 177, 889–898.
| Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVSnsLw%3D&md5=964c1c29a4dd413c2bcd8d85212541eeCAS | 18086223PubMed |
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. Journal of Experimental Botany 59, 93–109.
| Sucrose transport in the phloem: integrating root responses to phosphorus starvation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1SitbY%3D&md5=29c7af0aac7865b8bea17e77119543b7CAS | 18212031PubMed |
Karimi M, De Meyer B, Hilson P (2005) Modular cloning and expression of tagged fluorescent protein in plant cells. Trends in Plant Science 10, 103–105.
Kunst A, Draeger B, Ziegenhorn J (1984) Monosaccharides and derivatives. In ‘Methods of enzymatic analysis’. (Ed. HU Bergmeyer) pp. 163–172. (Verlag Chemie: Weinheim, Germany)
Lin WY, Lin SI, Chiou TJ (2009) Molecular regulators of phosphate homeostasis in plants. Journal of Experimental Botany 60, 1427–1438.
| Molecular regulators of phosphate homeostasis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktV2nuro%3D&md5=cff32892858dbd4718e1ea012af06b00CAS | 19168668PubMed |
Lundmark M, Kørner CJ, Hamborg Nielsen T (2010) Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiologia Plantarum 140, 57–68.
| Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFaisrnM&md5=45d3d901fe40e8d3e95457953d3219f1CAS | 20487378PubMed |
Misson J, Raghothama K, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrera-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proceedings of the National Academy of Sciences of the United States of America 102, 11934–11939.
| A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFGgu7w%3D&md5=846770a780fef882c547be438e825268CAS | 16085708PubMed |
Miura K, Rus A, Sharkuu 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. Proceedings of the National Academy of Sciences of the United States of America 102, 7760–7765.
| The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkslOmsbg%3D&md5=09b2de40f910db7a5fa2bc4e217523faCAS | 15894620PubMed |
Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Bläsing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell & Environment 30, 85–112.
| Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitVCltb0%3D&md5=e3d043d06aae156df96937c0b2c8e6e8CAS | 17177879PubMed |
Müller R, Nilsson L, Krintel C, Nielsen TH (2004) Gene expression during recovery from phosphate starvation in roots and shoots of Arabidopsis thaliana. Physiologia Plantarum 122, 233–243.
| Gene expression during recovery from phosphate starvation in roots and shoots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Müller 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 Physiology 143, 156–171.
| Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism.Crossref | GoogleScholarGoogle Scholar | 17085508PubMed |
Nielsen TH, Skjærbæk HC, Karlsen P (1991) Carbohydrate metabolism during fruit development in sweet pepper (Capsicum annuum L.) plants. Physiologia Plantarum 82, 311–319.
| Carbohydrate metabolism during fruit development in sweet pepper (Capsicum annuum L.) plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1ymtL0%3D&md5=a5d3c6723a0a8167e7340a68094ef070CAS |
Nilsson L, Müller R, Nielsen TH (2007) Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant, Cell & Environment 30, 1499–1512.
| Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVyjsbbJ&md5=aefcb855c24f8d7a04d5252bdb8c8210CAS | 17927693PubMed |
Nilsson L, Müller R, Nielsen TH (2010) Dissecting the plant transciptome and the regulatory responses to phosphate deprivation. Physiologia Plantarum 139, 129–143.
| Dissecting the plant transciptome and the regulatory responses to phosphate deprivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1Ghsbc%3D&md5=347e912e801b17198bdbeff16b3aa95eCAS | 20113436PubMed |
Nixon KC (1999) Winclada (beta). V. 0.9. Available at http://www.cladistics.com/aboutWinc.htm [Verified 13 December 2010]
Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. The Plant Journal 53, 731–738.
| MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFyjsrk%3D&md5=05ad12c5bc4f195e27fe5a2f1f92ed7eCAS | 17988220PubMed |
Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150, 1541–1555.
| Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing.Crossref | GoogleScholarGoogle Scholar | 19465578PubMed |
Plaxton WC, Carswell MC (1999) Metabolic aspects of the phosphate starvation response in plants. In ‘Plant responses to environmental stresses: from phytohormones to genome reorganisation’. (Ed. HR Lerner) pp. 349–372. (Marcel Dekker: New York)
Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216, 23–37.
| Molecular mechanisms of phosphate transport in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1eht70%3D&md5=20d9c23b8e523b959e195bea508bae37CAS | 12430011PubMed |
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110.
| Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVyjtbk%3D&md5=ae7c08e147932aab15cd4b2ecdbfdba4CAS | 11118137PubMed |
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 & Development 15, 2122–2133.
| A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmt1ajsb8%3D&md5=68d87471fa5ebed12f84db7ff392d6deCAS | 11511543PubMed |
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=9cd36e27497189634ce53eeac77c32fbCAS | 7984417PubMed |
Todd CD, Zeng P, Huete AMR, Hoyos ME, Polacco JC (2004) Transcripts of MYB-like genes respond to phosphorus and nitrogen deprivation in Arabidopsis. Planta 219, 1003–1009.
| Transcripts of MYB-like genes respond to phosphorus and nitrogen deprivation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotlKgtLk%3D&md5=3d7b98212cd78d41f9cca2d28a7347d1CAS | 15592750PubMed |
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157, 423–447.
| Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisF2gu70%3D&md5=fa588ef3613ff19ec8ab9504a3bbe796CAS |
Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proceedings of the National Academy of Sciences of the United States of America 96, 15336–15341.
| Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFehtw%3D%3D&md5=e40f79e2c0c47ab71440654bfe61e6e9CAS | 10611385PubMed |
