Complementation of the embryo-lethal T-DNA insertion mutant of AUXIN-BINDING-PROTEIN 1 (ABP1) with abp1 point mutated versions reveals crosstalk of ABP1 and phytochromes

Journal of Experimental Botany

Volumn 66, Issue 1, 2015, Pages 403-418

  Effendi, Yunus ^a,d   Ferro, Noel ^b   Labusch, Corinna ^a   Geisler, Markus ^c   Scherer, Günther F E ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF FRIBOURG   (Switzerland)

^d University of Al Azhar Indonesia   (Indonesia)

Author keywords

Abp1 mutants; Arabidopsis thaliana; AUXIN BINDING PROTEIN1 (ABP1); Early auxin regulated genes; Early light regulated genes; Gravitropism; Hypocotyl elongation; Phototropism; Phytochrome; Shade avoidance

Indexed keywords

ARABIDOPSIS THALIANA;

AUXIN-BINDING PROTEIN 1; BACTERIAL DNA; CELL SURFACE RECEPTOR; INDOLEACETIC ACID DERIVATIVE; PHYTOCHROME; PLANT PROTEIN; T-DNA;

ARABIDOPSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; POINT MUTATION; RADIATION RESPONSE; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; BIOLOGICAL TRANSPORT; DNA, BACTERIAL; INDOLEACETIC ACIDS; LIGHT; PHYTOCHROME; PLANT PROTEINS; POINT MUTATION; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84922514700     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru433     Document Type: Article

References (58)

1. Alberts IL, Nadassy K, Wodak SJ. 1998. Analysis of zinc binding sites in protein crystal structures. Protein Science 7, 1700-1716.
2. Aukerman MJ, Hirschfeld M, Wester L, Weaver M, Clack T, Amasino RM, Sharrock RA. 1997. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. The Plant Cell 9, 1317-1326.
3. Bailly A, Yang H, Martinoia E, Geisler M, Murphy AS. 2012. Plant lessons: exploring ABCB functionality through structural modeling. Frontiers in Plant Science 2, 108.
4. Becke AD. 1988. Density-functional exchange-energy approximation with correct asymptotic-behavior. Physical Reviews A 38, 3098-3100.
5. Braun N, Wyrzykowska J, Muller P, David K, Couch D, Perrot-Rechenmann C, Fleming AJ. 2008. Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell division and cell expansion during postembryonic development in Arabidopsis and tobacco. The Plant Cell 20, 2746-2762.
6. Chen JG, Shimomura S, Sitbon F, Sandberg G, Jones AM. 2001a. The role of auxin-binding protein 1 in the expansion of tobacco leaf cells. The Plant Journal 28, 607-617.
7. Chen JG, Ullah H, Young JC, Sussman MR, Jones AM. 2001b. ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes and Development 15, 902-911.
8. Covanová M, Sauer M, Rychtář J, Friml J, Petrášek J, Zažímalová E. 2013. Overexpression of the AUXIN BINDING PROTEIN1 modulates PIN-dependent auxin transport in tobacco cells. PLoS One 8, e70050.
9. Dai N, Wang W, Patterson SE, Bleecker AB. 2013. The TMK subfamily of receptor-like kinases in Arabidopsis display an essential role in growth and a reduced sensitivity to auxin. PLoS One 8, e60990.
10. David KM, Couch D, Braun N, Brown S, Grosclaude J, Perrot-Rechenmann C. 2007. The auxin-binding protein 1 is essential for the control of cell cycle. The Plant Journal 50, 197-206.
11. Devlin P, Yanovsky MJ, Kay SA. 2003. A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiology 133, 1617-1629.
12. Effendi Y, Jones AM, Scherer GFE. 2013. AUXIN-BINDING-PROTEIN1 (ABP1) in phytochrome-B-controlled responses. Journal of Experimental Botany 64, 5065-5074.
13. Effendi Y, Radatz K Rietz S, Labusch C, Rietz S, Wimalasekera R, Helizon H, Zeidler M, Scherer GFE. 2014. Mutants of phospholipase A (pPLA-I) have a red light and auxin phenotype. Plant, Cell and Environment 37, 1626-1640.
14. Effendi Y, Rietz S, Fischer U, Scherer GFE. 2011. The heterozygous abp1/ABP1 insertional mutant has defects in functions requiring polar auxin transport and in regulation of early auxin-regulated genes. The Plant Journal 65: 282-294.
15. Effendi Y, Scherer GFE. 2011. AUXIN BINDING-PROTEIN1 (ABP1), a receptor to regulate auxin transport and early auxin genes in an interlocking system with PIN proteins and the receptor TIR1. Plant Signaling and Behavior 6, 1101-1103.
16. Eichkorn K, Weigen F, Treutler O, Ahlrichs R. 1997. Auxiliary basis sets for main row atoms and transition metals and their use to approximate Coulomb potentials. Theoretical Chimica Acta 97, 119-124.
17. Fankhauser C, Casal JJ. 2004. Phenotypic characterization of a photomorphogenic mutant. The Plant Journal 39, 747-760.
18. Ferro N, Gallegos A, Bultinck P, Jacobsen HJ, Carbó-Dorca R, Reinard T. 2006. Coulomb and overlap self-similarities: a comparative selectivity analysis of structure-function relationships for auxin-like molecules. Journal of Chemical Informatics Modeling 46, 1751-1762.
19. Grimme S, Antony J, Ehrlich S, Krieg H. 2010. A consistent and accurate ab initio parametrization of density functional dispersion correction (DFT-D) for the 94 elements H-Pu. Journal of Chemical Physics 132, 154104-154109.
20. Jones AM, Im KH, Savka MA, Wu MJ, DeWitt NG, Shillito R, Binns AN. 1998. Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282, 1114-1117.
21. Karimi M, Inz D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193-195.
22. Keuskamp DH, Pollmann S, Voesenek LACJ, Peeters AJM, Pierik R. 2010. Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proceedings of the National Academy of Sciences, USA 107, 22740-22744.
23. Kunihiro A, Yamashino T, Nakamichi N, Niwa Y, Nakanishi H, Mizuno T. 2011. Phytochrome-interacting factor 4 and 5 (PIF4 and PIF5) activate the homeobox ATHB2 and auxin-inducible IAA29 genes in the coincidence mechanism underlying photoperiodic control of plant growth of Arabidopsis thaliana. Plant and Cell Physiology 52, 1315-1329.
24. Labusch C, Shishova M, Effendi Y, Li M, Wang X, Scherer GFE. 2013. Patterns and timing in expression of early auxin-induced genes in phospholipase A (pPLA) T-DNA insertion mutants reveal a function in auxin signaling. Molecular Plant 6, 1473-1486.
25. Lee C, Yang W, Parr RG. 1988. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Physical Reviews B 37, 785-789.
26. Leivar P, Tepperman JM, Cohn MM, Monte E, Al-Sady B, Erickson E, Quail PH. 2012. Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. The Plant Cell 24, 1398-1419.
27. Lewis DR, Muday GK. 2009. Measurement of auxin transport in Arabidopsis thaliana. Nature Protocols 4, 437-451.
28. Liscum E, Hangarter RP. 1993. Genetic evidence that the red-absorbing form of phytochrome B modulates gravitropism in Arabidopsis thaliana. Plant Physiology 103, 15-19.
29. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408.
30. Medzihradszky M, Bindics J, Dám et al. 2013. Phosphorylation of phytochrome B inhibits light-induced signaling via accelerated dark reversion in Arabidopsis. The Plant Cell 25, 535-544.
31. Mockaitis K, Estelle M. 2008. Auxin receptors and plant development: a new signaling paradigm. Annual Reviews of Cell and Developmental Biology 24, 55-80.
32. Nagashima A, Suzuki G, Uehara Y et al. 2008a. Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. The Plant Journal 53, 516-529.
33. Nagashima A, Uehara Y, Sakai T. 2008b. The ABC subfamily B auxin transporter AtABCB19 is involved in the inhibitory effects of N-1-naphthyphthalamic acid on the phototropic and gravitropic responses of Arabidopsis hypocotyls. Plant and Cell Physiology 49, 1250-1255.
34. Napier RM. 1995. Towards an understanding of ABP1. Journal of Experimental Botany 46, 1787-1795.
35. Nito K, Wong CC, Yates JR 3rd, Chory J. 2013. Tyrosine phosphorylation regulates the activity of phytochrome photoreceptors. Cell Reports 27, 1970-1979.
36. Paque S, Mouille G, Grandont L et al. 2014. AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling, and cell expansion in Arabidopsis. The Plant Cell 26, 280-295.
37. Petrášek J, Friml J. 2009. Auxin transport routes in plant development. Development 136, 2675-2688.
38. Pfaffl MW, Horgan G, Dempfle L. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36.
39. Reddy SK, Finlayson SA. 2014. Phytochrome B promotes branching in Arabidopsis by suppressing auxin signaling. Plant Physiology 164, 1542-1550.
40. Rico JF, López R, Ema I, Ramírez G, Ludea EV. 2004. Analytical method for the representation of atoms-in-molecules densities. Journal of Comparative Chemistry 25, 1355-1363.
41. Robert S, Kleine-Vehn J, Barbez E et al. 2010. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143, 111-121.
42. Robson PRH, Smith H. 1996. Genetic and transgenic evidence that phytochrome A and B act to modulate the gravitropic orientation of Arabidopsis thaliana hypocotyls. Plant Physiology 110, 211-216.
43. Rolo-Naranjo A, Codorniu-Hernández E, Ferro N. 2010. Quantum chemical associations ligand-residue: their role to predict flavonoid binding sites in proteins. Journal of Chemical Informatics Modeling 50, 924-933.
44. Ruberti I, Sessa G, Ciolfi A, Possenti M, Carabelli M, Morelli G. 2012. Plant adaptation to dynamically changing environment: The shade avoidance response. Biotechnology Advances 30, 1047-1058.
45. Santner AA, Watson JC. 2006. The WAG1 and WAG2 protein kinases negatively regulate root waving in Arabidopsis. The Plant Journal 45, 752-764.
46. Scherer GFE. 2011. AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction? Journal of Experimental Botany 62, 3339-3357.
47. Scherer GFE, Labusch C, Effendi Y. 2012. Phospholipases and the network of auxin signal transduction with ABP1 and TIR1 as two receptors: a comprehensive and provocative model. Frontiers in Plant Science 3, 56.
48. Steindler C, Mateucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I. 1999. Shade avoidance responses are mediated by the ATHB-2 HD-Zip protein, a negative regulator of gene expression. Development 126, 4235-4245.
49. Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ. 1994. Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. Physical Chemistry 98, 11623-11627.
50. Tao Y, Ferrer JL, Ljung K et al. 2008. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164-176.
51. Thiel G, Blatt MR, Fricker MD, White IR, Millner P. 1993. Modulation of K+ channels in Vicia stomatal guard cells by peptide homologues to the auxin-binding proteins C-terminus. Proceedings of the National Academy of Sciences, USA 90, 11493-11497.
52. Tromas A, Paque S, Stierl V, Quettier AL, Muller P, Lechner E, Genschik P, Perrot-Rechenmann C. 2013. Auxin-binding protein 1 is a negative regulator of the SCF(TIR1/AFB) pathway. Nature Communications 4, 2496.
53. Wang C, Yan X, Chen Q, Jiang N, Fu W, Ma B, Liu J, Li C, Bednarek SY, Pan J. 2013. Clathrin light chains regulate clathrin-mediated trafficking, auxin signaling, and development in Arabidopsis. The Plant Cell 25, 499-516.
54. Wang JG, Chen CH, Chien CT, Hsieh HL. 2011. FAR-RED INSENSITIVE219 modulates CONSTITUTIVE PHOTOMORPHOGENIC1 activity via physical interaction to regulate hypocotyl elongation in Arabidopsis. Plant Physiology 156, 631-646.
55. Whitelam GC, Johnson E, Peng J, Carol P, Anderson ML, Cowl JS, Harberd NP. 1993. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. The Plant Cell 5, 757-768.
56. Woo EJ, Marshall J, Bauly J, Chen JG, Venis M, Napier RM, Pickersgill RW. 2002. Crystal structure of auxin-binding protein 1 in complex with auxin. EMBO Journal 21, 2877-2885.
57. Xu T, Dai N, Chen J et al. 2014. Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343, 1025-1028.
58. Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z. 2010. Cell surface-and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99-110.