Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission

eLife

Volumn 5, Issue April 2016, 2016, Pages

  Santiago, Julia ^a   Brandt, Benjamin ^a   Wildhagen, Mari ^b   Hohmann, Ulrich ^a   Hothorn, Ludwig A ^c   Butenko, Melinka A ^b   Hothorn, Michael ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF OSLO   (Norway)

^c LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYPROLINE; LEUCINE; PEPTIDE HORMONE; ARABIDOPSIS PROTEIN; IDA PROTEIN, ARABIDOPSIS; PROTEIN BINDING; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; RLK5 PROTEIN, ARABIDOPSIS; SERK1 PROTEIN, ARABIDOPSIS;

ABSCISSION; ARABIDOPSIS THALIANA; ARTICLE; BACULOVIRIDAE; BINDING AFFINITY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISSOCIATION CONSTANT; GEL FILTRATION; GENE MUTATION; GENE SEQUENCE; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; LIGHT INTENSITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PETAL; PHENOTYPE; PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; SIGNAL TRANSDUCTION; SIZE EXCLUSION CHROMATOGRAPHY; SOMATIC EMBRYOGENESIS; STOICHIOMETRY; ARABIDOPSIS; BINDING SITE; BIOSYNTHESIS; CHEMISTRY; FLOWER; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; FLOWERS; GENE EXPRESSION REGULATION, PLANT; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84969150862     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15075     Document Type: Article

References (53)

1. Aalen RB, Wildhagen M, Stø IM, Butenko MA. 2013. Ida: A peptide ligand regulating cell separation processes in Arabidopsis. Journal of Experimental Botany 64:5253-5261. doi: 10.1093/jxb/ert338
2. Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S. 2005. The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. The Plant Cell 17:3337-3349. doi: 10.1105/tpc.105.036814
3. Albrecht C, Russinova E, Kemmerling B, Kwaaitaal M, de Vries SC. 2008. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and -independent signaling pathways. Plant Physiology 148:611-619. doi: 10.1104/pp.108.123216
4. Bojar D, Martinez J, Santiago J, Rybin V, Bayliss R, Hothorn M. 2014. Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. The Plant Journal 78:31-43. doi: 10.1111/tpj.12445
5. Brandt B, Hothorn M. 2016. SERK co-receptor kinases. Current Biology 26:R225-R226. doi: 10.1016/j.cub.2015.12.014
6. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W. 2003. Generation, representation and flow of phase information in structure determination: Recent developments in and around SHARP 2.0. Acta Crystallographica. Section D, Biological Crystallography 59:2023-2030. doi: 10.1107/S0907444903017694
7. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, Aalen RB. 2003. Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. The Plant Cell 15:2296-2307. doi: 10.1105/tpc.014365
8. Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM. 2009. Plant peptides in signalling: Looking for new partners. Trends in Plant Science 14:255-263. doi: 10.1016/j.tplants.2009.02.002
9. Butenko MA, Wildhagen M, Albert M, Jehle A, Kalbacher H, Aalen RB, Felix G. 2014. Tools and strategies to match peptide-ligand receptor pairs. The Plant Cell 26:1838-1847. doi: 10.1105/tpc.113.120071
10. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 105: 15629-15634. doi: 10.1073/pnas.0805539105
11. Clark SE, Running MP, Meyerowitz EM. 1995. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057-2067.
12. Clough SJ, Bent AF. 1998. Floral dip: A simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16:735-743. doi: 10.1046/j.1365-313x.1998.00343.x
13. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI. 2005. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. The Plant Cell 17:3350-3361. doi: 10.1105/tpc.105.036731
14. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, Snoeyink J, Richardson JS, Richardson DC. 2007. Molprobity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Research 35:W375-W383. doi: 10.1093/nar/gkm216
15. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallographica Section D Biological Crystallography 60:2126-2132. doi: 10.1107/S0907444904019158
16. Fenn TD, Ringe D, Petsko GA. 2003. Povscript+: A program for model and data visualization using persistence of vision ray-tracing. Journal of Applied Crystallography 36:944-947. doi: 10.1107/S0021889803006721
17. Gou X, Yin H, He K, Du J, Yi J, Xu S, Lin H, Clouse SD, Li J. 2012. Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genetics 8:e1002452. doi: 10.1371/journal.pgen.1002452
18. Hashimoto Y, Zhang S, Blissard GW. 2010. Ao38, a new cell line from eggs of the black witch moth, Ascalapha odorata (Lepidoptera: Noctuidae), is permissive for AcMNPV infection and produces high levels of recombinant proteins. BMC Biotechnology 10:50. doi: 10.1186/1472-6750-10-50
19. Hasler M, Hothorn LA. 2008. Multiple contrast tests in the presence of heteroscedasticity. Biometrical Journal 50:793-800. doi: 10.1002/bimj.200710466
20. Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC. 2001. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiology 127:803-816. doi: 10.1104/pp.010324
21. Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biometrical Journal 50:346-363. doi: 10.1002/bimj.200810425
22. Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, Wilson IA, Chory J. 2011. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474:467-471. doi: 10.1038/nature10153
23. Jinn TL, Stone JM, Walker JC. 2000. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes & Development 14:108-117. doi: 10.1101/gad.14.1.108
24. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637. doi: 10.1002/bip.360221211
25. Kabsch W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. Journal of Applied Crystallography 26:795-800. doi: 10.1107/S0021889893005588
26. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y. 2006. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845-848. doi: 10.1126/science.1128439
27. Lease KA, Cho SK, Walker JC. 2006. A petal breakstrength meter for Arabidopsis abscission studies. Plant Methods 2:2. doi: 10.1186/1746-4811-2-2
28. Lewis MW, Leslie ME, Fulcher EH, Darnielle L, Healy PN, Youn JY, Liljegren SJ. 2010. The SERK1 receptor-like kinase regulates organ separation in Arabidopsis flowers. The Plant Journal 62:817-828. doi: 10.1111/j.1365-313X.2010.04194.x
29. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408. doi: 10.1006/meth.2001.1262
30. Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y. 2010. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065-1067. doi: 10.1126/science.1191132
31. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. Journal of Applied Crystallography 40:658-674. doi: 10.1107/S0021889807021206
32. Meng X, Chen X, Mang H, Liu C, Yu X, Gao X, Torii KU, He P, Shan L. 2015. Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Current Biology 25:2361-2372. doi: 10.1016/j.cub.2015.07.068
33. Meng X, Zhou J, Tang J, Li B, de Oliveira MVV, Chai J, He P, Shan L. 2016. Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Reports 14:1330-1338. doi: 10.1016/j.celrep.2016.01.023
34. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum- likelihood method. Acta Crystallographica Section D Biological Crystallography 53:240-255. doi: 10.1107/S0907444996012255
35. Muto T, Todoroki Y. 2013. Brassinolide-2,3-acetonide: A brassinolide-induced rice lamina joint inclination antagonist. Bioorganic & Medicinal Chemistry 21:4413-4419. doi: 10.1016/j.bmc.2013.04.048
36. Niederhuth CE, Cho SK, Seitz K, Walker JC. 2013. Letting go is never easy: Abscission and receptor-like protein kinases. Journal of Integrative Plant Biology 55:1251-1263. doi: 10.1111/jipb.12116
37. Niederhuth CE, Patharkar OR, Walker JC. 2013. Transcriptional profiling of the Arabidopsis abscission mutant hae hsl2 by RNA-Seq. BMC Genomics 14:37. doi: 10.1186/1471-2164-14-37
38. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y. 2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294. doi: 10.1126/science.1150083
39. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y. 2009. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nature Chemical Biology 5:578-580. doi: 10.1038/nchembio.182
40. R Core Team. 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria.
41. Salaj J, von Recklinghausen IR, Hecht V, de Vries SC, Schel JH, van Lammeren AA. 2008. AtSERK1 expression precedes and coincides with early somatic embryogenesis in Arabidopsis thaliana. Plant Physiology and Biochemistry 46:709-714. doi: 10.1016/j.plaphy.2008.04.011
42. Sanner MF, Olson AJ, Spehner JC. 1996. Reduced surface: An efficient way to compute molecular surfaces. Biopolymers 38:305-320. doi: 10.1002/(SICI)1097-0282(199603)38:3<305::AID-BIP4>3.0.CO;2-Y
43. Santiago J, Henzler C, Hothorn M. 2013. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341:889-892. doi: 10.1126/science.1242468
44. Shah K, Vervoort J, de Vries SC. 2001. Role of threonines in the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 activation loop in phosphorylation. The Journal of Biological Chemistry 276:41263-41269. doi: 10.1074/jbc.M102381200
45. Sheldrick GM. 2008. A short history of SHELX. Acta Crystallographica Section A Foundations of Crystallography 64:112-122. doi: 10.1107/S0108767307043930
46. Shinohara H, Moriyama Y, Ohyama K, Matsubayashi Y. 2012. Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. The Plant Journal 70:845-854. doi: 10.1111/j.1365-313X.2012.04934.x
47. Stenvik GE, Butenko MA, Urbanowicz BR, Rose JK, Aalen RB. 2006. Overexpression of INFLORESCENCE DEFICIENT IN ABSCISSION activates cell separation in vestigial abscission zones in Arabidopsis. The Plant Cell 18:1467-1476. doi: 10.1105/tpc.106.042036
48. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA. 2008. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. The Plant Cell 20:1805-1817. doi: 10.1105/tpc.108.059139
49. Sun Y, Han Z, Tang J, Hu Z, Chai C, Zhou B, Chai J. 2013. Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Research 23:1326-1329. doi: 10.1038/cr.2013.131
50. Tang J, Han Z, Sun Y, Zhang H, Gong X, Chai J. 2015. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Research 25:110-120. doi: 10.1038/cr.2014.161
51. Taylor I, Wang Y, Seitz K, Baer J, Bennewitz S, Mooney BP, Walker JC. 2016. Analysis of phosphorylation of the receptor-like protein kinase HAESA during arabidopsis floral abscission. PLOS ONE 11:e0147203. doi: 10.1371/journal.pone.0147203
52. Terwilliger TC, Grosse-Kunstleve RW, Afonine PV, Moriarty NW, Zwart PH, Hung L-W, Read RJ, Adams PD. 2008. Iterative model building, structure refinement and density modification with the PHENIX autobuild wizard. Acta Crystallographica Section D Biological Crystallography 64:61-69. doi: 10.1107/S090744490705024X
53. Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, Chang J, Yang W, Chai J. 2015. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525:265-268. doi: 10.1038/nature14858