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Plant Molecular Biology

, Volume 85, Issue 3, pp 233–245 | Cite as

Transcriptional coordination between leaf cell differentiation and chloroplast development established by TCP20 and the subgroup Ib bHLH transcription factors

  • Megan E. Andriankaja
  • Selahattin Danisman
  • Lorin F. Mignolet-Spruyt
  • Hannes Claeys
  • Irina Kochanke
  • Mattias Vermeersch
  • Liesbeth De Milde
  • Stefanie De Bodt
  • Veronique Storme
  • Aleksandra Skirycz
  • Felix Maurer
  • Petra Bauer
  • Per Mühlenbock
  • Frank Van Breusegem
  • Gerco C. Angenent
  • Richard G. H. Immink
  • Dirk InzéEmail author
Article

Abstract

The establishment of the photosynthetic apparatus during chloroplast development creates a high demand for iron as a redox metal. However, iron in too high quantities becomes toxic to the plant, thus plants have evolved a complex network of iron uptake and regulation mechanisms. Here, we examined whether four of the subgroup Ib basic helix-loop-helix transcription factors (bHLH38, bHLH39, bHLH100, bHLH101), previously implicated in iron homeostasis in roots, also play a role in regulating iron metabolism in developing leaves. These transcription factor genes were strongly up-regulated during the transition from cell proliferation to expansion, and thus sink-source transition, in young developing leaves of Arabidopsis thaliana. The four subgroup Ib bHLH genes also showed reduced expression levels in developing leaves of plants treated with norflurazon, indicating their expression was tightly linked to the onset of photosynthetic activity in young leaves. In addition, we provide evidence for a mechanism whereby the transcriptional regulators SAC51 and TCP20 antagonistically regulate the expression of these four subgroup Ib bHLH genes. A loss-of-function mutant analysis also revealed that single mutants of bHLH38, bHLH39, bHLH100, and bHLH101 developed smaller rosettes than wild-type plants in soil. When grown in agar plates with reduced iron concentration, triple bhlh39 bhlh100 bhlh101 mutant plants were smaller than wild-type plants. However, measurements of the iron content in single and multiple subgroup Ib bHLH genes, as well as transcript profiling of iron response genes during early leaf development, do not support a role for bHLH38, bHLH39, bHLH100, and bHLH101 in iron homeostasis during early leaf development.

Keywords

Leaf development Arabidopsis thaliana Iron metabolism Gene regulation Basic helix-loop-helix transcription factors  

Notes

Acknowledgments

We would like to thank Jacqueline Busscher-Lange for performing the yeast one-hybrid assays. This work and M.A. was supported by grants from the Interuniversity Attraction Poles Program (IUAP P7/29 "MARS") initiated by the Belgian Science Policy Office; the Bijzonder Onderzoeksfonds Methusalem Project no. BOF08/01M00408 and the Multidisciplinary Research Partnership "Biotechnology for a Sustainable Economy" no. 01MRB510W of Ghent University. L.M.-S. is supported by the Agency for Innovation by Science and Technology in Flanders (IWT). H.C. is a predoctoral fellow of the Research Foundation-Flanders (FWO).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (PPT 63 kb)
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11103_2014_180_MOESM5_ESM.docx (587 kb)
Supplementary material 5 (DOCX 587 kb)

References

  1. Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472PubMedCentralPubMedCrossRefGoogle Scholar
  2. Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Mühlenbock P, Skirycz A, Gonzalez N, Beemster GTS, Inzé D (2012) Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell 22:64–78PubMedCrossRefGoogle Scholar
  3. Apel K, Hirt H (2004) REACTIVE OXYGEN SPECIES: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  4. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113PubMedCrossRefGoogle Scholar
  5. Bashir K, Ishimaru Y, Shimo H, Nagasaka S, Fujimoto M, Takanashi H, Tsutsumi N, An G, Nakanishi H, Nishizawa NK (2011) The rice mitochondrial iron transporter is essential for plant growth. Nat Commun 2:322PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bauer P, Ling H-Q, Guerinot ML (2007) FIT, the F ER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis. Plant Physiol Biochem 45:260–261PubMedCrossRefGoogle Scholar
  7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B-Stat Methodol 57:289–300Google Scholar
  8. Breuninger H, Lenhard M (2010) Control of tissue and organ growth in plants. Curr Top Dev Biol 91:185–220PubMedCrossRefGoogle Scholar
  9. Briat J-F, Curie C, Gaymard F (2007) Iron utilization and metabolism in plants. Curr Opin Plant Biol 10:276–282PubMedCrossRefGoogle Scholar
  10. Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153:1398–1412PubMedCentralPubMedCrossRefGoogle Scholar
  11. Castrillo G, Turck F, Leveugle M, Lecharny A, Carbonero P, Coupland G, Paz-Ares J, Oñate-Sánchez L (2011) Speeding cistrans regulation discovery by phylogenomic analyses coupled with screenings of an arrayed library of Arabidopsis transcription factors. PLoS ONE 6:e21524PubMedCentralPubMedCrossRefGoogle Scholar
  12. Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412PubMedCentralPubMedCrossRefGoogle Scholar
  13. Crawford BCW, Nath U, Carpenter R, Coen ES (2004) CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of Antirrhinum. Plant Physiol 135:244–253PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222PubMedCrossRefGoogle Scholar
  15. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17PubMedCentralPubMedCrossRefGoogle Scholar
  16. Danisman S, van der Wal F, Dhondt S, Waites R, de Folter S, Bimbo A, van Dijk ADJ, Muino JM, Cutri L, Dornelas MC, Angenent GC, Immink RGH (2012) Arabidopsis class I and class II TCP transcription factors regulate jasmonic acid metabolism and leaf development antagonistically. Plant Physiol 159:1511–1523PubMedCentralPubMedCrossRefGoogle Scholar
  17. de Folter S, Urbanus SL, van Zuijlen LGC, Kaufmann K, Angenent GC (2007) Tagging of MADS domain proteins for chromatin immunoprecipitation. BMC Plant Biol 7:47PubMedCentralPubMedCrossRefGoogle Scholar
  18. De Sutter V, Vanderhaeghen R, Tilleman S, Lammertyn F, Vanhoutte I, Karimi M, Inzé D, Goossens A, Hilson P (2005) Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J 44:1065–1076PubMedCrossRefGoogle Scholar
  19. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419PubMedCrossRefGoogle Scholar
  20. Duy D, Wanner G, Meda AR, von Wirén N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19:986–1006PubMedCentralPubMedCrossRefGoogle Scholar
  21. Duy D, Stübe R, Wanner G, Philippar K (2011) The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol 155:1709–1722PubMedCentralPubMedCrossRefGoogle Scholar
  22. Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20:2293–2306PubMedCentralPubMedCrossRefGoogle Scholar
  23. Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628PubMedCentralPubMedCrossRefGoogle Scholar
  24. Gonzalez N, De Bodt S, Sulpice R, Jikumaru Y, Chae E, Dhondt S, Van Daele T, De Milde L, Weigel D, Kamiya Y, Stitt M, Beemster GTS, Inzé D (2010) Increased leaf size: different means to an end. Plant Physiol 153:1261–1279PubMedCentralPubMedCrossRefGoogle Scholar
  25. Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340PubMedCrossRefGoogle Scholar
  26. Grevelding C, Suter-Crazzolara C, von Menges A, Kemper E, Masterson R, Schell J, Reiss B (1996) Characterisation of a new allele of pale cress and its role in greening in Arabidopsis thaliana. Mol Gen Genet 251:532–541PubMedGoogle Scholar
  27. Gustafsson JP, Visual MINTEQ ver. 3.0. 2010. http://www2.lwr.kth.se/English/OurSoftware/vminteq/index.htm
  28. Henriques R, Jásik J, Klein M, Martinoia E, Feller U, Schell J, Pais MS, Koncz C (2002) Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol Biol 50:587–597PubMedCrossRefGoogle Scholar
  29. Hervé C, Dabos P, Bardet C, Jauneau A, Auriac MC, Ramboer A, Lacout F, Tremousaygue D (2009) In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiol 149:1462–1477PubMedCentralPubMedCrossRefGoogle Scholar
  30. Hong S, Kim SA, Guerinot ML, McClung CR (2013) Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis. Plant Physiol 161:893–903PubMedCentralPubMedCrossRefGoogle Scholar
  31. Hou YM, Von Arnim AG, Deng XW (1993) A new class of Arabidopsis constitutive photomorphogenic genes involved in regulating cotyledon development. Plant Cell 5:329–339PubMedCentralPubMedCrossRefGoogle Scholar
  32. Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T (2006) The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133:3575–3585PubMedCrossRefGoogle Scholar
  33. Ivanov R, Brumbarova T, Bauer P (2012) Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Mol Plant 5:27–42PubMedCrossRefGoogle Scholar
  34. Jakoby M, Wang H-Y, Reidt W, Weisshaar B, Bauer P (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577:528–534PubMedCrossRefGoogle Scholar
  35. Jeong J, Guerinot ML (2009) Homing in on iron homeostasis in plants. Trends Plant Sci 14:280–285PubMedCrossRefGoogle Scholar
  36. Kampfenkel K, Van Montagu M, Inzé D (1995) Effects of iron excess on Nicotiana plumbaginifolia plants—implications to oxidative stress. Plant Physiol 107:725–735PubMedCentralPubMedGoogle Scholar
  37. Kaufmann K, Muiño JM, Østerås M, Farinelli L, Krajewski P, Angenent GC (2010) Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nat Protoc 5:457–472PubMedCrossRefGoogle Scholar
  38. Kobayashi Y, Kanesaki Y, Tanaka A, Kuroiwa H, Kuroiwa T, Tanaka K (2009) Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc Natl Acad Sci USA 106:803–807PubMedCentralPubMedCrossRefGoogle Scholar
  39. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim IJ, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719PubMedCrossRefGoogle Scholar
  40. Larbi A, Abadía A, Abadía J, Morales F (2006) Down co-regulation of light absorption, photochemistry, and carboxylation in Fe-deficient plants growing in different environments. Photosynth Res 89:113–126PubMedCrossRefGoogle Scholar
  41. Li H, Culligan K, Dixon RA, Chory J (1995) CUE1: a mesophyll cell-specific positive regulator of light-controlled gene expression in Arabidopsis. Plant Cell 7:1599–1610PubMedCentralPubMedCrossRefGoogle Scholar
  42. Li C, Potuschak T, Colón-Carmona A, Gutiérrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102:12978–12983PubMedCentralPubMedCrossRefGoogle Scholar
  43. Li L-Y, Cai Q-Y, Yu D-S, Guo C-H (2011) Overexpression of AtFRO6 in transgenic tobacco enhances ferric chelate reductase activity in leaves and increases tolerance to iron-deficiency chlorosis. Mol Biol Rep 38:3605–3613PubMedCrossRefGoogle Scholar
  44. Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39PubMedCrossRefGoogle Scholar
  45. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  46. Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci USA 106:22534–22539PubMedCentralPubMedCrossRefGoogle Scholar
  47. Nishio JN, Terry N (1983) Iron nutrition-mediated chloroplast development. Plant Physiol 71:688–691PubMedCentralPubMedCrossRefGoogle Scholar
  48. Ogo Y, Itai RN, Kobayashi T, Aung MS, Nakanishi H, Nishizawa NK (2011) OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Mol Biol 75:593–605PubMedCrossRefGoogle Scholar
  49. Osteryoung KW, Nunnari J (2003) The division of endosymbiotic organelles. Science 302:1698–1704PubMedCrossRefGoogle Scholar
  50. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263PubMedCrossRefGoogle Scholar
  51. Palmer CM, Guerinot ML (2009) Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5:333–340PubMedCentralPubMedCrossRefGoogle Scholar
  52. Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, den Boer B, van der Geest L, Boutilier K (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol Biol 68:225–237PubMedCrossRefGoogle Scholar
  53. Pires N, Dolan L (2010) Early evolution of bHLH proteins in plants. Plant Signal Behav 5:911–912PubMedCentralPubMedCrossRefGoogle Scholar
  54. Ravet K, Touraine B, Kim SA, Cellier F, Thomine S, Guerinot ML, Briat J-F, Gaymard F (2009) Post-translational regulation of AtFER2 ferritin in response to intracellular iron trafficking during fruit development in Arabidopsis. Mol Plant 2:1095–1106PubMedCrossRefGoogle Scholar
  55. Raynaud C, Perennes C, Reuzeau C, Catrice O, Brown S, Bergounioux C (2005) Cell and plastid division are coordinated through the prereplication factor AtCDT1. Proc Natl Acad Sci USA 102:8216–8221PubMedCentralPubMedCrossRefGoogle Scholar
  56. Reiter RS, Coomber SA, Bourett TM, Bartley GE, Scolnik PA (1994) Control of leaf and chloroplast development by the Arabidopsis gene pale cress. Plant Cell 6:1253–1264PubMedCentralPubMedCrossRefGoogle Scholar
  57. Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697PubMedCrossRefGoogle Scholar
  58. Roschzttardtz H, Conéjéro G, Divol F, Alcon C, Verdeil JL, Curie C, Mari S (2013) New insights into Fe localization in plant tissues. Front Plant Sci 4:350PubMedCentralPubMedCrossRefGoogle Scholar
  59. Salomé PA, Oliva M, Weigel D, Krämer U (2013) Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function. EMBO J 32:511–523PubMedCentralPubMedCrossRefGoogle Scholar
  60. Sivitz AB, Hermand V, Curie C, Vert G (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS ONE 7:e44843PubMedCentralPubMedCrossRefGoogle Scholar
  61. Skirycz A, Claeys H, De Bodt S, Oikawa A, Shinoda S, Andriankaja M, Maleux K, Eloy NB, Coppens F, Yoo S-D, Saito K, Inzé D (2011) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell 23:1876–1888PubMedCentralPubMedCrossRefGoogle Scholar
  62. Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749–1770PubMedCentralPubMedCrossRefGoogle Scholar
  63. Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J 31:589–599PubMedCrossRefGoogle Scholar
  64. Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat J-F, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233PubMedCentralPubMedCrossRefGoogle Scholar
  65. Vorwieger A, Gryczka C, Czihal A, Douchkov D, Tiedemann J, Mock H-P, Jakoby M, Weisshaar B, Saalbach I, Bäumlein H (2007) Iron assimilation and transcription factor controlled synthesis of riboflavin in plants. Planta 226:147–158PubMedCrossRefGoogle Scholar
  66. Wang H-Y, Klatte M, Jakoby M, Bäumlein H, Weisshaar B, Bauer P (2007) Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana. Planta 226:897–908PubMedCrossRefGoogle Scholar
  67. Wang N, Cui Y, Liu Y, Fan H, Du J, Huang Z, Yuan Y, Wu H, Ling H-Q (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6:503–513PubMedCrossRefGoogle Scholar
  68. Wu H, Chen C, Du J, Liu H, Cui Y, Zhang Y, He Y, Wang Y, Chu C, Feng Z, Li J, Ling H-Q (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158:790–800PubMedCentralPubMedCrossRefGoogle Scholar
  69. Yuan YX, Zhang J, Wang DW, Ling HQ (2005) AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 15:613–621PubMedCrossRefGoogle Scholar
  70. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling H-Q (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Megan E. Andriankaja
    • 1
    • 2
  • Selahattin Danisman
    • 3
    • 4
  • Lorin F. Mignolet-Spruyt
    • 1
    • 2
  • Hannes Claeys
    • 1
    • 2
  • Irina Kochanke
    • 4
  • Mattias Vermeersch
    • 1
    • 2
  • Liesbeth De Milde
    • 1
    • 2
  • Stefanie De Bodt
    • 1
    • 2
  • Veronique Storme
    • 1
    • 2
  • Aleksandra Skirycz
    • 1
    • 2
  • Felix Maurer
    • 5
  • Petra Bauer
    • 5
  • Per Mühlenbock
    • 1
    • 2
    • 6
  • Frank Van Breusegem
    • 1
    • 2
  • Gerco C. Angenent
    • 3
    • 7
  • Richard G. H. Immink
    • 7
  • Dirk Inzé
    • 1
    • 2
    Email author
  1. 1.Department of Plant Systems BiologyVIBGhentBelgium
  2. 2.Department of Plant Biotechnology and BioinformaticsGhent UniversityGhentBelgium
  3. 3.Laboratory of Molecular BiologyWageningen UniversityWageningenThe Netherlands
  4. 4.Department of Molecular Cell PhysiologyBielefeld UniversityBielefeldGermany
  5. 5.Department of Biosciences, Plant BiologySaarland UniversitySaarbrückenGermany
  6. 6.Department of Plant Protection BiologySwedish University of Agricultural SciencesAlnarpSweden
  7. 7.BiosciencePlant Research InternationalWageningenThe Netherlands

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