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Karin Ljung - Root Development and Shoot-Root Communication Print E-mail

show_ghroup_bw The research in my group is focused on the mechanisms and processes regulating plant growth and development. We are particularly interested in the role of different plant growth regulating substances (plant hormones) in primary and secondary root development. We are also interested in understanding how a plant coordinates the growth of its aerial parts with its root system, and the role that plant hormones play in this.
Ljung_Karin_portrait

ljung_1 ljung_2Above.Confocal laser scanning picture of the Arabidopsis DR5:GFP line, expressing Green Flourescent Protein in specific cell types of the root apex.

Left. The picture shows the relative auxin distribution in the Arabidopsis root. The highest concentration (dark blue) was observed in the quiescent cen- tre of the root apex (Petersson et al. 2009).

Below. Arabidopsis seedlings growing on agar plates
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Auxins and cytokinins are plant hormones that are absolutely essential during the whole of a plant's life cycle. They play important roles in cell division, cell differentiation and cell elongation and are believed to act in a concentration dependent manner. Different regulatory mechanisms (synthesis, degradation, transport) act in concert to maintain optimal hormone concentrations for particular plant growth and development processes. Interactions between different hormone signalling pathways are also important for the regulation of plant development in response to integrated external and internal signals. Auxin, cytokinins and other molecules can be transported between root and shoot tissues to coordinate the growth of the roots with the shoot. Cytokinins are transported via the xylem from the root to the shoot, and auxin is transported via both polar auxin transport and phloem transport from the shoot to the root.
We have previously observed that a leaf-mediated pulse of auxin is important for lateral root development, and we are now studying how light and the circadian clock regulate auxin biosynthesis, metabolism and transport and how this influences the coordinated growth of plants. Very little is known about the metabolic pathways involved, and we are using various biochemical and molecular genetic techniques, such as analysis of gene expression, metabolites and proteins, to elucidate these pathways.

The other main area of enquiry in my group is the unravelling of auxin and cytokinin interactions. These two hormones sometimes act synergistically and sometimes antagonistically during growth and development, and the mechanisms behind these interactions are largely unknown. We are currently studying the regulation of auxin and cytokinin metabolism in Arabidopsis, and we have recently shown that auxin and cytokinins regulate each other's biosynthesis. In root tips and young developing leaves, cytokinins upregulate auxin synthesis, whereas auxin down-regulates cytokinin biosynthesis in Arabidopsis seedlings. We are now investigating the mechanisms behind these interactions, and the importance that they have in developmental processes in plants.

By using sensitive mass spectrometry-based methods for plant hormone analysis, we have also shown the formation of local hormone gradients and maxima in plant tissues, e.g. in the primary root apex. It is believed that the formation of such gradients and maxima are very important for specifying stem cell niches and for the regulation of cell division and differentiation in the root apex. We have also shown that the Arabidopsis root system has auxin biosynthesis capacity, and we are trying to understand which factors are important for the regulation of auxin biosynthesis and metabolism in the root. A better understanding of the basic cellular processes we are studying will be very important in the improvement of crop and tree growth and productivity.


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Key Publications

Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant Journal 28: 465-474.

Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17: 1090-1104.

Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19: 2186-2196.

Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Bal- laré CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133: 164-176.

Petersson SV, Johansson AI, Kowalczyk K, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659-1668.

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  1. Zheng Z, Guo Y, Novák O, Dai X, Zhao Y, Ljung K, Noel JP, Chory J
    Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1
    Nat Chem Biol. 2013, 9(4):244-6.  Epub 2013 Feb 3
  2. Ljung K
    Auxin metabolism and homeostasis during plant development
    Development 2013, 140(5):943-50
  3. Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, Hatzopoulos P
    Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex
    New Phytol. 2012 Dec 18 [Epub ahead of print]
  4. Sairanen I, Novák O, Pencík A, Ikeda Y, Jones B, Sandberg G, Ljung K
    Soluble Carbohydrates Regulate Auxin Biosynthesis via PIF Proteins in Arabidopsis
    Plant Cell. 2012 Dec 3. [Epub ahead of print]
  5. Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C, Cole BJ, Ivans LJ, Pedmale UV, Jung HS, Ecker JR, Kay SA, Chory J
    Linking photoreceptor excitation to changes in plant architecture
    Genes Dev. 2012, 26(8):785-90
  6. Tiwari A, Vivian-Smith A, Ljung K, Offringa R, Heuvelink E
    Physiological and morphological changes during early and later stages of fruit growth in Capsicum annuum
    Physiol Plant. 2012 Aug 13. [Epub ahead of print]
  7. Lilley JL, Gee CW, Sairanen I, Ljung K, Nemhauser JL
    An endogenous carbon-sensing pathway triggers increased auxin flux and hypocotyl elongation
    Plant Physiol. 2012 Oct 16. [Epub ahead of print]
  8. Fuentes S, Ljung K, Sorefan K, Alvey E, Harberd NP, Ostergaard L
    Fruit Growth in Arabidopsis Occurs via DELLA-Dependent and DELLA-Independent Gibberellin Responses
    Plant Cell. 2012 Oct;24(10):3982-96
  9. Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K
    Tissue specific profiling of the Arabidopsis thaliana auxin metabolome
    Plant J. 2012 72(3):523-536
  10. Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, López-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M, Pradervand S, Xenarios I, Fankhauser C
    Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling
    Plant J. 2012 71(5):699-711
  11. Ståldal V, Cierlik I, Chen S, Landberg K, Baylis T, Myrenås M, Sundström JF, Eklund DM, Ljung K, Sundberg E
    The Arabidopsis thaliana transcriptional activator STYLISH1 regulates genes affecting stamen development, cell expansion and timing of flowering
    Plant Molecular Biology 2012, 78(6):545-559
  12. Band LR, Wells DM, Larrieu A, Sun J, Middleton AM, French AP, Brunoud G, Sato EM, Wilson MH, Péret B, Oliva M, Swarup R, Sairanen I, Parry G, Ljung K, Beeckman T, Garibaldi JM, Estelle M, Owen MR, Vissenberg K, Hodgman TC, Pridmore TP, King JR, Vernoux T, Bennett MJ
    Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism
    PNAS 2012, 109(12):4668-4673
  13. Stepanova AN, Yun J, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM.
    The Arabidopsis YUCCA1 Flavin Monooxygenase Functions in the Indole-3-Pyruvic Acid Branch of Auxin Biosynthesis.
    Plant Cell 2011 [Epub ahead of print]
  14. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T.
    Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants.
    Proc Natl Acad Sci USA 2011 [Epub ahead of print]
  15. Jones B, Ljung K
    Subterranean space exploration: the development of root system architecture
    Curr Opin Plant Biol.  2012 15(1):97-102
  16. Jones B, Ljung K
    Auxin and cytokinin regulate each other's levels via a metabolic feedback loop
    Plant Signal Behav.: 2011, 6(6):901-4
  17. Greenham K, Santner A, Castillejo C, Mooney S, Sairanen I, Ljung K, Estelle M
    The AFB4 auxin receptor is a negative regulator of auxin signaling in seedlings
    Current Biology: 2011 21:520-525
  18. Rizzardi K, Landberg K, Nilsson L, Ljung K, Sundas-Larsson A
    TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes
    Plant Journal: 2011 65:897-906
  19. Lucas M, Swarup R, Paponov IA, Swarup K, Casimiro I, Lake D, Peret B, Zappala S, Mairhofer S, Whitworth M, Wang JH, Ljung K, Marchant A, Sandberg G, Holdsworth MJ, Palme K, Pridmore T, Mooney S, Bennett MJ
    SHORT-ROOT regulates primary, lateral, and adventitious root development in Arabidopsis
    Plant Physiology: 2011 155:384-398
  20. Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blázquez MA, Carbonell J
    Role of polyamines in plant vascular development
    Plant Physiology and Biochemistry: 2010 48:534-539
  21. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A.
    Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants
    Developmental Cell: 2010 18:927-37
  22. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU
    Hormonal control of the shoot stem-cell niche
    Nature: 2010 465:1089-1092
  23. Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock JM, Ljung K, Charrier B
    Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus
    Plant Physiology: 2010 153:128-144
  24. Wu G, Cameron JN, Ljung K, Spalding EP
    A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome 1 and phytochrome B
    The Plant Journal: 2010 62:179-191
  25. Eklund DM, Thelander M, Landberg K, Ståldal V, Nilsson A, Johansson M, Valsecchi I, Pederson ERA, Kowalczyk M, Ljung K, Ronne H, Sundberg E
    Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens
    Development: 2010 137:1275-1284
  26. Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld J-P
    Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling
    The Plant Cell: 2010 22: 376-391
  27. Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, Zhao Y, Ljung K, Harmer SL
    REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways
    Proceedings of the National Academy of Science of the United States of America: 2009 106:16883-16888
  28. Prusinkiewicz P, Crawford S, Smith RS, Ljung K, Bennett T, Ongaro V, Leyser O
    Control of bud activation by an auxin transport switch
    Proceedings of the National Academy of Sciences of the United States of America: 2009 106:17431-17436
  29. Tromas A, Braun N, Muller P, Khodus T, Paponov IA, Palme K, Ljung K, Lee J-Y, Benfey P, Murray JAH, Scheres B, Perrot-Rechenmann C
    The AUXIN BINDING PROTEIN 1 is required for differential auxin responses mediating root growth
    PloS One: 2009 4:e6648
  30. Lewis DR, Wu G, Ljung K, Spalding EP
    Auxin transport into cotyledons and cotyledon growth depend similarly on the ABCB19 Multidrug Resistance-like transporter
    The Plant Journal: 2009 60:91-101
  31. Ali B, Sabri AN, Ljung K, Hasnain S
    Quantification of indole-3-acetic acid from plant associated Bacillus spp. and their phytostimulatory effect on Vigna radiata (L.)
    World Journal of Microbiology and Biotechnology: 2009 25:519-526
  32. Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P, Galván-Ampudia CS, Offringa R, Friml J, Yanovsky MF, Østergaard L
    A regulated auxin minimum is required for seed dispersal in Arabidopsis
    Nature: 2009 459: 583-586
  33. Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K
    An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis
    The Plant Cell: 2009 21:1659-1668
  34. Ikeda Y, Men S, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M
    Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis
    Nature Cell Biology: 2009 11:731-738
  35. Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Tähtiharju S, Elo A, Decourteix M, Ljung K, Bhalerao R, Keinonen K, Albert VA, Helariutta Y
    Cytokinin signaling regulates cambial development in poplar
    Proceedings of the National Academy of Sciences of the United States of America: 2008 105:20032-20037
  36. Stone BB, Stowe-Evans EL, Harper RM, Celaya RB, Ljung K, Sandberg G, Liscum E
    Disruptions in AUX1-dependent auxin influx alter hypocotyl phototropism in Arabidopsis
    Molecular Plant: 2008 1:129-144
  37. Ståldal V, Sohlberg JJ, Eklund DM, Ljung K, Sundberg E
    Auxin can act independently of CRC, LUG, SEU, SPT and STY1 in style development but not apical-basal patterning of the Arabidopsis gynoecium
    New Phytologist: 2008 180:798-808
  38. Swarup K, Benkova E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JDG, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ
    The auxin influx carrier LAX3 promotes lateral root emergence
    Nature Cell Biology: 2008 10:946-954
  39. Tao Y, Ferrer J-L, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, BallaréCL, Sandberg G, Noel JP, Chory J
    Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants
    Cell: 2008 133:164-176
  40. Andersen SU, Buechel S, Zhao Z, Ljung K, Novák O, Busch W, Schuster C, Lohmann JU
    Requirement of B2-Type Cyclin-Dependent Kinases for Meristem Integrity in Arabidopsis thaliana.
    The Plant Cell: 2008 20:88-100
  41. Larsson E, Sitbon F, Ljung K, von Arnold S.
    Inhibited polar auxin transport results in aberrant embryo development in Norway spruce
    New Phytologist: 2008 177:356-366
  42. Ruzicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benkova E
    Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution
    The Plant Cell: 2007 19:2197-2212
  43. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ
    Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation
    The Plant Cell: 2007 19: 2186-2196
  44. Yin X-J, Volk S, Ljung K, Mehlmer N, Dolezal K, Ditengou F, Hanano S, Davis SJ, Schmelzer E, Sandberg G, Teige M, Palme K, Pickart C, Bachmair A
    Ubiquitin lysine 63 chain-forming ligases regulate apical dominance in Arabidopsis
    The Plant Cell: 2007 19:1898-1911
  45. Fischer U, Ikeda Y, Ljung K, Serralbo O, Singh M, Heidstra R, Palme K, Scheres B, Grebe M
    Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity
    Current Biology: 2006 16:2143-2149
  46. Esmon CA, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E
    A gradient of auxin and auxin-dependent transcription precedes tropic growth responses
    Proc Natl Acad Sci U S A: 2006 103:236-241
  47. de Reuille PB, Bohn-Courseau I, Ljung K, Morin H, Carraro N, Godin C, Traas J
    Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis
    Proc Natl Acad Sci U S A: 2006 103:1627-1632
  48. Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, Geiss G, McKhann H, Garcion C, Vaucheret H, Sandberg G, Bellini C
    Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1
    Plant Cell: 2005 17:1343-1359
  49. Vanneste S, De Rybel B, Beemster GTS, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, Inze D, Fukaki H, Beeckman T
    Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana
    Plant Cell: 2005 17:3035-3050
  50. Weijers D, Sauer M, Meurette O, Friml J, Ljung K, Sandberg G, Hooykaas P, Offringa R
    Maintenance of embryonic auxin distribution for apical-basal patterning by PIN-FORMED-dependent auxin transport in Arabidopsis
    Plant Cell: 2005 17:2517-2526
  51. Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G
    Sites and regulation of auxin biosynthesis in Arabidopsis roots
    Plant Cell: 2005 17:1090-1104
  52. Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G, Bartel B
    A family of auxin-conjugate hydrolases that contributes to free indole- 3- acetic acid levels during Arabidopsis germination
    Plant Physiol: 2004 135:978-988
  53. Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PBF, Ljung K, Sandberg G, Hooykaas PJJ, Palme K, Offringa R
    A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux
    Science: 2004 306:862-865
  54. Fuchs I, Philippar K, Ljung K, Sandberg G, Hedrich R
    Blue light regulates an auxin-induced K+-channel gene in the maize coleoptile
    Proc Natl Acad Sci U S A: 2003 100:11795-11800
  55. Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jurgens G, Palme K
    AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis
    Cell: 2002 108:661-673
  56. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G
    Biosynthesis, conjugation, catabolism and homeostasis of indole- 3- acetic acid in Arabidopsis thaliana
    Plant Molecular Biology: 2002 50:309-332
  57. Grebe M, Friml J, Swarup R, Ljung K, Sandberg G, Terlou M, Palme K, Bennett MJ, Scheres B
    Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway
    Curr Biol: 2002 12:329-334
  58. Santamaria RTa, Bliek M, Ljung K, Sandberg G, Mol JNM, Souer E, Koes R
    FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture
    Genes Dev: 2002 16:753-763
  59. Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G
    Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings
    Plant Journal: 2002 29:325-332
  60. Tantikanjana T, Yong JW, Letham DS, Griffith M, Hussain M, Ljung K, Sandberg G, Sundaresan V
    Control of axillary bud initiation and shoot architecture in Arabidopsis through the SUPERSHOOT gene
    Genes Dev: 2001 15:1577-1588
  61. Ljung K, Ostin A, Lioussanne L, Sandberg G
    Developmental regulation of indole- 3- acetic acid turnover in Scots pine seedlings
    Plant Physiol: 2001 125:464-475
  62. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M
    Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex
    Genes Dev: 2001 15:2648-2653
  63. Ljung K, Bhalerao RP, Sandberg G
    Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth
    Plant J: 2001 28:465-474
  64. Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R, Bennett M, Sandberg G, Bellini C
    The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis
    Proc Natl Acad Sci U S A: 2000 97:14819-14824
  65. Philippar K, Fuchs I, Luthen H, Hoth S, Bauer CS, Haga K, Thiel G, Ljung K, Sandberg G, Bottger M, Becker D, Hedrich R
    Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropism
    Proc Natl Acad Sci U S A: 1999 96:12186-12191
 
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