Function and Identification of Mobile Transcription Factors

Chapter
Part of the Advances in Plant Biology book series (AIPB, volume 3)

Abstract

Growth and development of multi-cellular organisms require mechanisms that allow for extensive cell-to-cell communication. In some incidences communication is established by signaling molecules that are directly transported from one cell to the other. These mobile signals in plants have been found in forms of proteins, RNAs, and small molecules. They are transmitted through the vascular system in a long distance (between organs), or through plasmodesmata in a short distance (between cell types). A growing number of studies show that transcription factors contribute as important mobile signals in plants. Transcription factors move in a short or long distance in forms of proteins and RNAs. Such transport activities are very important for patterning and growth of plant organs and tissues. In this chapter, we will comprehensively review transcription factors as mobile signals: factors that have been discovered, mechanisms of their mobility, new tools that will lead to the discovery of mobile transcription factors, and putative mobile transcription factors inferred from cell-type specific RNA profiling data.

Keywords

Maize Recombination Leucine Sorting Heptad 

Notes

Acknowledgments

This work was funded by National Science Foundation (IOS-0818071) and Boyce Thompson Institute to J-Y Lee.

References

  1. Banerjee AK, Chatterjee M, Yu Y, Suh S-G, Miller WA, Hannapel DJ (2006) Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18:3443–3457PubMedCrossRefGoogle Scholar
  2. Banerjee AK, Lin T, Hannapel DJ (2009) Untranslated regions of a mobile transcript mediate RNA metabolism. Plant Physiol 151:1831–1843PubMedCrossRefGoogle Scholar
  3. Bennett T, Scheres B (2010) Root development-two meristems for the price of one? Curr Top Dev Biol (Academic Press) 91:67–102CrossRefGoogle Scholar
  4. Bernhardt C, Zhao M, Gonzalez A, Lloyd A, Schiefelbein J (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132:291–298PubMedCrossRefGoogle Scholar
  5. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960PubMedCrossRefGoogle Scholar
  6. Birnbaum K, Jung JW, Wang JY, Lambert GM, Hirst JA, Galbraith DW, Benfey PN (2005) Cell type-specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat Methods 2:615–619PubMedCrossRefGoogle Scholar
  7. Brady SM, Orlando DA, Lee J-Y, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806PubMedCrossRefGoogle Scholar
  8. Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321PubMedCrossRefGoogle Scholar
  9. Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493PubMedCrossRefGoogle Scholar
  10. Causier B, Schwarz-Sommer Z, Davies B (2009) Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 21:73–79PubMedGoogle Scholar
  11. Chen JJ, Janssen BJ, Williams A, Sinha N (1997) A gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell 9:1289–1304PubMedCrossRefGoogle Scholar
  12. Chen H, Rosin FM, Prat S, Hannapel DJ (2003) Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol 132:1391–1404PubMedCrossRefGoogle Scholar
  13. Chung S-M, Frankman EL, Tzfira T (2005) A versatile vector system for multiple gene expression in plants. Trends Plant Sci 10:357–361PubMedCrossRefGoogle Scholar
  14. Crawford KM, Zambryski PC (2000) Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr Biol 10:1032–1040PubMedCrossRefGoogle Scholar
  15. Crawford KM, Zambryski PC (2001) Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol 125: 1802–1812PubMedCrossRefGoogle Scholar
  16. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425PubMedCrossRefGoogle Scholar
  17. Deeken R, Ache P, Kajahn I, Klinkenberg J, Bringmann G, Hedrich R (2008) Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J 55:746–759PubMedCrossRefGoogle Scholar
  18. Digiuni S, Schellmann S, Geier F, Greese B, Pesch M, Wester K, Dartan B, Mach V, Srinivas BP, Timmer J, Fleck C, Hulskamp M (2008) A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves. Mol Syst Biol 4:217PubMedCrossRefGoogle Scholar
  19. Gallagher KL, Benfey PN (2009) Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J 57:785–797PubMedCrossRefGoogle Scholar
  20. Gallagher KL, Paquette AJ, Nakajima K, Benfey PN (2004) Mechanisms regulating SHORT-ROOT intercellular movement. Curr Biol 14:1847–1851PubMedCrossRefGoogle Scholar
  21. Gómez G, Torres H, Pallás V (2005) Identification of translocatable RNA-binding phloem proteins from melon, potential components of the long-distance RNA transport system. Plant J 41:107–116PubMedCrossRefGoogle Scholar
  22. Goto K, Kyozuka J, Bowman JL (2001) Turning floral organs into leaves, leaves into floral organs. Curr Opin Genet Dev 11:449–456PubMedCrossRefGoogle Scholar
  23. Ham B-K, Brandom JL, Xoconostle-Cázares B, Ringgold V, Lough TJ, Lucas WJ (2009) A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21:197–215PubMedCrossRefGoogle Scholar
  24. Hannapel DJ (2010) A model system of development regulated by the long-distance transport of mRNA. J Integr Plant Biol 52:40–52PubMedCrossRefGoogle Scholar
  25. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411PubMedCrossRefGoogle Scholar
  26. Haywood V, Yu T-S, Huang N-C, Lucas WJ (2005) Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J 42:49–68PubMedCrossRefGoogle Scholar
  27. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser M-T, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567PubMedCrossRefGoogle Scholar
  28. Huang N-C, Yu T-S (2009) The sequences of Arabidopsis GA-INSENSITIVE RNA constitute the motifs that are necessary and sufficient for RNA long-distance trafficking. Plant J 59:921–929PubMedCrossRefGoogle Scholar
  29. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386PubMedCrossRefGoogle Scholar
  30. Ivashikina N, Deeken R, Ache P, Kranz E, Pommerrenig B, Sauer N, Hedrich R (2003) Isolation of AtSUC2 promoter-GFP-marked companion cells for patch-clamp studies and expression profiling. Plant J 36:931–945PubMedCrossRefGoogle Scholar
  31. Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16:S1–S17PubMedCrossRefGoogle Scholar
  32. Jackson D, Veit B, Hake S (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:405–413Google Scholar
  33. Jenik PD, Irish VF (2001) The Arabidopsis floral homeotic gene APETALA3 differentially regulates intercellular signaling required for petal and stamen development. Development 128:13–23PubMedGoogle Scholar
  34. Karimi M, De Meyer B, Hilson P (2005) Modular cloning in plant cells. Trends Plant Sci 10:103–105PubMedCrossRefGoogle Scholar
  35. Karimi M, Depicker A, Hilson P (2007) Recombinational cloning with plant gateway vectors. Plant Physiol 145:1144–1154PubMedCrossRefGoogle Scholar
  36. Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–289PubMedCrossRefGoogle Scholar
  37. Kim JY, Yuan Z, Cilia M, Khalfan-Jagani Z, Jackson D (2002) Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proc Natl Acad Sci USA 99:4103–4108PubMedCrossRefGoogle Scholar
  38. Kim J-Y, Yuan Z, Jackson D (2003) Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130:4351–4362PubMedCrossRefGoogle Scholar
  39. Kim I, Kobayashi K, Cho E, Zambryski PC (2005a) Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc Natl Acad Sci USA 102:11945–11950PubMedCrossRefGoogle Scholar
  40. Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC (2005b) Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci USA 102:2227–2231PubMedCrossRefGoogle Scholar
  41. Kim J-Y, Rim Y, Wang J, Jackson D (2005c) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev 19:788–793PubMedCrossRefGoogle Scholar
  42. Komatsu M, Maekawa M, Shimamoto K, Kyozuka J (2001) The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. Dev Biol 231:364–373PubMedCrossRefGoogle Scholar
  43. Kuijt SJH, Lamers GEM, Rueb S, Scarpella E, Ouwerkerk PBF, Spaink HP, Meijer AH (2004) Different subcellular localization and trafficking properties of KNOX class 1 homeodomain proteins from rice. Plant Mol Biol 55:781–796PubMedGoogle Scholar
  44. Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, Nagasaka R, Tominaga R, Koshino-Kimura Y, Kato T, Sato S, Tabata S, Okada K, Wada T (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132:5387–5398PubMedCrossRefGoogle Scholar
  45. Lee J-Y, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN (2006) Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc Natl Acad Sci USA 103:6055–6060PubMedCrossRefGoogle Scholar
  46. Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B, Benfey PN (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol 4:e143PubMedCrossRefGoogle Scholar
  47. Lin M-K, Lee Y-J, Lough TJ, Phinney BS, Lucas WJ (2009) Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol Cell Proteomics 8:343–356PubMedGoogle Scholar
  48. Long J, Moan E, Medford J, Barton M (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69PubMedCrossRefGoogle Scholar
  49. Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in arabidopsis roots. Plant Cell 22: 2219–2236PubMedCrossRefGoogle Scholar
  50. Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–1983PubMedCrossRefGoogle Scholar
  51. Miyashima S, Koi S, Hashimoto T, Nakajima K (2011) Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303–2313PubMedCrossRefGoogle Scholar
  52. Mustroph A, Zanetti ME, Jang CJH, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci USA 106:18843–18848PubMedCrossRefGoogle Scholar
  53. Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311PubMedCrossRefGoogle Scholar
  54. Nawy T, Lee J-Y, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN (2005) Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17:1908–1925PubMedCrossRefGoogle Scholar
  55. Oikawa T, Kyozuka J (2009) Two-step regulation of LAX PANICLE1 protein accumulation in Axillary meristem formation in rice. Plant Cell 21:1095–1108PubMedCrossRefGoogle Scholar
  56. Ou B, Yin K-Q, Liu S-N, Yang Y, Gu T, Wing Hui JM, Zhang L, Miao J, Kondou Y, Matsui M, Gu H-Y, Qu L-J (2011) A high-throughput screening system for arabidopsis transcription factors and its application to Med25-dependent transcriptional regulation. Mol Plant 4:546–555PubMedCrossRefGoogle Scholar
  57. Perbal MC, Haughn G, Saedler H, Schwarz-Sommer Z (1996) Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122:3433–3441PubMedGoogle Scholar
  58. Ruiz-Medrano R, Xoconostle-Cazares B, Lucas WJ (1999) Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126: 4405–4419PubMedGoogle Scholar
  59. Ruiz-Medrano R, Xoconostle-Cázares B, Ham B-K, Li G, Lucas WJ (2011) Vascular expression in Arabidopsis is predicted by the frequency of CT/GA-rich repeats in gene promoters. Plant J 67:130–144PubMedCrossRefGoogle Scholar
  60. Sablowski R (2011) Plant stem cell niches: from signalling to execution. Curr Opin Plant Biol 14:4–9PubMedCrossRefGoogle Scholar
  61. Schiefelbein J, Kwak S-H, Wieckowski Y, Barron C, Bruex A (2009) The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot 60(5):1515–1521, ern339PubMedCrossRefGoogle Scholar
  62. Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916PubMedCrossRefGoogle Scholar
  63. Sena G, Jung JW, Benfey PN (2004) A broad competence to respond to SHORT ROOT revealed by tissue-specific ectopic expression. Development 131:2817–2826PubMedCrossRefGoogle Scholar
  64. Sessions A, Yanofsky MF, Weigel D (2000) Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–781PubMedCrossRefGoogle Scholar
  65. Shyu A-B, Wilkinson MF, van Hoof A (2008) Messenger RNA regulation: to translate or to degrade. EMBO J 27:471–481PubMedCrossRefGoogle Scholar
  66. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616PubMedCrossRefGoogle Scholar
  67. Urbanus SL, Martinelli AP, Dinh QD, Aizza LCB, Dornelas MC, Angenent GC, Immink RGH (2010) Intercellular transport of epidermis-expressed MADS domain transcription factors and their effect on plant morphology and floral transition. Plant J 63:60–72PubMedGoogle Scholar
  68. Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, Martienssen R, Selvaraj G, Datla R (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci USA 99:4730–4735PubMedCrossRefGoogle Scholar
  69. Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243PubMedCrossRefGoogle Scholar
  70. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116PubMedCrossRefGoogle Scholar
  71. Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, Goto K, Marks MD, Shimura Y, Okada K (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129:5409–5419PubMedCrossRefGoogle Scholar
  72. Wester K, Digiuni S, Geier F, Timmer J, Fleck C, Hülskamp M (2009) Functional diversity of R3 single-repeat genes in trichome development. Development 136:1487–1496PubMedCrossRefGoogle Scholar
  73. Winter N, Kollwig G, Zhang S, Kragler F (2007) MPB2C, a microtubule-associated protein, regulates non-cell-autonomy of the homeodomain protein KNOTTED1. Plant Cell 19:3001–3018PubMedCrossRefGoogle Scholar
  74. Wu XL, Dinneny JR, Crawford KM, Rhee Y, Citovsky V, Zambryski PC, Weigel D (2003) Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130: 3735–3745PubMedCrossRefGoogle Scholar
  75. Xu H, Zhang W, Li M, Harada T, Han Z, Li T (2010) Gibberellic acid insensitive mRNA transport in both directions between stock and scion in Malus. Tree Genet Genom 6:1013–1019CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Boyce Thompson Institute for Plant ResearchIthacaUSA
  2. 2.Department of Plant BiologyCornell UniversityIthacaUSA

Personalised recommendations