, Volume 243, Issue 6, pp 1441–1453 | Cite as

Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens

  • Mauricio Lopez-Obando
  • Caitlin E. Conn
  • Beate Hoffmann
  • Rohan Bythell-Douglas
  • David C. NelsonEmail author
  • Catherine Rameau
  • Sandrine BonhommeEmail author
Original Article
Part of the following topical collections:
  1. Strigolactones


Main conclusion

A set of PpKAI2 - LIKE paralogs that may encode strigolactone receptors in Physcomitrella patens were identified through evolutionary, structural, and transcriptional analyses, suggesting that strigolactone perception may have evolved independently in basal land plants in a similar manner as spermatophytes.

Carotenoid-derived compounds known as strigolactones are a new class of plant hormones that modulate development and interactions with parasitic plants and arbuscular mycorrhizal fungi. The strigolactone receptor protein DWARF14 (D14) belongs to the α/β hydrolase family. D14 is closely related to KARRIKIN INSENSITIVE2 (KAI2), a receptor of smoke-derived germination stimulants called karrikins. Strigolactone and karrikin structures share a butenolide ring that is necessary for bioactivity. Charophyte algae and basal land plants produce strigolactones that influence their development. However phylogenetic studies suggest that D14 is absent from algae, moss, and liverwort genomes, raising the question of how these basal plants perceive strigolactones. Strigolactone perception during seed germination putatively evolved in parasitic plants through gene duplication and neofunctionalization of KAI2 paralogs. The moss Physcomitrella patens shows an increase in KAI2 gene copy number, similar to parasitic plants. In this study we investigated whether P. patens KAI2-LIKE (PpKAI2L) genes may contribute to strigolactone perception. Based on phylogenetic analyses and homology modelling, we predict that a clade of PpKAI2L proteins have enlarged ligand-binding cavities, similar to D14. We observed that some PpKAI2L genes have transcriptional responses to the synthetic strigolactone GR24 racemate or its enantiomers. These responses were influenced by light and dark conditions. Moreover, (+)-GR24 seems to be the active enantiomer that induces the transcriptional responses of PpKAI2L genes. We hypothesize that members of specific PpKAI2L clades are candidate strigolactone receptors in moss.


Bryophytes DWARF14 (D14) Evolution Hormone KARRIKIN INSENSITIVE2 (KAI2) Moss Receptor Signalling Strigolactone 





Differentially expressed








KAI2 ligand


Physcomitrella patens KAI2-LIKE





The authors would like to thank F. -D. Boyer (Institut de Chimie des Substances Naturelles, Gif sur Yvette, France) for providing racemic GR24 and GR24 enantiomers. This research was supported by the Agence Nationale de la Recherche (contract ANR-12-BSV6-004-01), National Science Foundation Grant IOS-1350561 to D. C. N., and a National Science Foundation Graduate Research Fellowship to C. E. C. The IJPB benefits from the support of the Labex Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS).

Supplementary material

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Supplementary material 1 (PPTX 120 kb)
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Supplementary material 6 (DOCX 217 kb)


  1. Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T, Seto Y, Yamaguchi S, Akiyama K, Nomura T (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci USA 111:18084–18089. doi: 10.1073/pnas.1410801111 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akiyama K, Ogasawara S, Ito S, Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117. doi: 10.1093/pcp/pcq058 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186. doi: 10.1146/annurev-arplant-043014-114759 CrossRefPubMedGoogle Scholar
  4. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50:1416–1424. doi: 10.1093/pcp/pcp091 CrossRefPubMedGoogle Scholar
  5. Bennett T, Leyser O (2014) Strigolactone signalling: standing on the shoulders of DWARFs. Curr Opin Plant Biol 22:7–13. doi: 10.1016/j.pbi.2014.08.001 CrossRefPubMedGoogle Scholar
  6. Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J, Schwede T (2009) Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 4:1–13. doi: 10.1038/nprot.2008.197 CrossRefPubMedGoogle Scholar
  7. Bythell-Douglas R, Waters MT, Scaffidi A, Flematti GR, Smith SM, Bond CS (2013) The structure of the karrikin-insensitive protein (KAI2) in Arabidopsis thaliana. PLoS ONE 8:e54758. doi: 10.1371/journal.pone.0054758 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chevalier F, Nieminen K, Sanchez-Ferrero JC, Rodriguez ML, Chagoyen M, Hardtke CS, Cubas P (2014) Strigolactone promotes degradation of DWARF14, an alpha/beta hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26:1134–1150. doi: 10.1105/tpc.114.122903 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Conn CE, Nelson DC (2016) Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front Plant Sci 6:1219. doi: 10.3389/fpls.2015.01219 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B, Westwood JH, Shirasu K, Bond CS, Dyer KA, Nelson DC (2015) Plant evolution. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349:540–543. doi: 10.1126/science.aab1140 CrossRefPubMedGoogle Scholar
  11. Coudert Y, Palubicki W, Ljung K, Novak O, Leyser O, Harrison CJ (2015) Three ancient hormonal cues co-ordinate shoot branching in a moss. Elife. doi: 10.7554/eLife.06808 PubMedGoogle Scholar
  12. de Saint Germain A, Bonhomme S, Boyer FD, Rameau C (2013) Novel insights into strigolactone distribution and signalling. Curr Opin Plant Biol 16:583–589. doi: 10.1016/j.pbi.2013.06.007 CrossRefPubMedGoogle Scholar
  13. DeLano W (2002) The Pymol molecular graphics system. Schrödinger, LLC, San CarlosGoogle Scholar
  14. Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Becard G, Sejalon-Delmas N (2012) Origin of strigolactones in the green lineage. New Phytol 195:857–871. doi: 10.1111/j.1469-8137.2012.04209.x CrossRefPubMedGoogle Scholar
  15. Drummond RS, Janssen BJ, Luo Z, Oplaat C, Ledger SE, Wohlers MW, Snowden KC (2015) Environmental control of branching in petunia. Plant Physiol 168:735–751. doi: 10.1104/pp.15.00486 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34:W116–W118. doi: 10.1093/nar/gkl282 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Flematti GR, Scaffidi A, Goddard-Borger ED, Heath CH, Nelson DC, Commander LE, Stick RV, Dixon KW, Smith SM, Ghisalberti EL (2010) Structure-activity relationship of karrikin germination stimulants. J Agric Food Chem 58:8612–8617. doi: 10.1021/jf101690a CrossRefPubMedGoogle Scholar
  18. Fox J (2005) The R commander: a basic-statistics graphical user interface to R. J Stat Softw 14:1–42Google Scholar
  19. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. doi: 10.1093/nar/gkr944 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Guo Y, Zheng Z, La Clair JJ, Chory J, Noel JP (2013) Smoke-derived karrikin perception by the alpha/beta-hydrolase KAI2 from Arabidopsis. Proc Natl Acad Sci USA 110:8284–8289. doi: 10.1073/pnas.1306265110 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22:2032–2036. doi: 10.1016/j.cub.2012.08.007 CrossRefPubMedGoogle Scholar
  22. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412. doi: 10.1104/pp.109.137646 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hiss M, Laule O, Meskauskiene RM, Arif MA, Decker EL, Erxleben A, Frank W, Hanke ST, Lang D, Martin A, Neu C, Reski R, Richardt S, Schallenberg-Rudinger M, Szovenyi P, Tiko T, Wiedemann G, Wolf L, Zimmermann P, Rensing SA (2014) Large-scale gene expression profiling data for the model moss Physcomitrella patens aid understanding of developmental progression, culture and stress conditions. Plant J 79:530–539. doi: 10.1111/tpj.12572 CrossRefPubMedGoogle Scholar
  24. Hoffmann B, Proust H, Belcram K, Labrune C, Boyer FD, Rameau C, Bonhomme S (2014) Strigolactones inhibit caulonema elongation and cell division in the moss Physcomitrella patens. PLoS ONE 9:e99206. doi: 10.1371/journal.pone.0099206 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y, Yi W, Zhao L, Ma H, He Y, Wu Z, Melcher K, Qian Q, Xu HE, Wang Y, Li J (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504:401–405. doi: 10.1038/nature12870 CrossRefPubMedGoogle Scholar
  26. Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y, Yamaguchi S, Hakoshima T (2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells Devot Mol Cell Mech 18:147–160. doi: 10.1111/gtc.12025 CrossRefGoogle Scholar
  27. Liu W, Wu C, Fu Y, Hu G, Si H, Zhu L, Luan W, He Z, Sun Z (2009) Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 230:649–658. doi: 10.1007/s00425-009-0975-6 CrossRefPubMedGoogle Scholar
  28. Lopez-Obando M, Ligerot Y, Bonhomme S, Boyer F-D, Rameau C (2015) Strigolactone biosynthesis and signaling in plant development. Development 142:3615–3619. doi: 10.1242/dev.120006 CrossRefPubMedGoogle Scholar
  29. Morffy N, Faure L, Nelson DC (2016) Smoke and hormone mirrors: action and evolution of karrikin and strigolactone signaling. Trends Genet. doi: 10.1016/j.tig.2016.01.002 PubMedGoogle Scholar
  30. Nakamura H, Xue Y-L, Miyakawa T, Hou F, Qin H-M, Fukui K, Shi X, Ito E, Ito S, Park S-H, Miyauchi Y, Asano A, Totsuka N, Ueda T, Tanokura M, Asami T (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4:2613. doi: 10.1038/ncomms3613 PubMedGoogle Scholar
  31. Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:8897–8902. doi: 10.1073/pnas.1100987108 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM (2012) Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu Rev Plant Biol 63:107–130. doi: 10.1146/annurev-arplant-042811-105545 CrossRefPubMedGoogle Scholar
  33. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Nogue F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531–1539. doi: 10.1242/dev.058495 CrossRefPubMedGoogle Scholar
  34. Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, Van de Peer Y, Reski R (2007) An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evol Biol 7:130. doi: 10.1186/1471-2148-7-130 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi: 10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165:1221–1232. doi: 10.1104/pp.114.240036 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Smith SM, Li J (2014) Signalling and responses to strigolactones and karrikins. Curr Opin Plant Biol 21:23–29. doi: 10.1016/j.pbi.2014.06.003 CrossRefPubMedGoogle Scholar
  38. Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP, Abbas A, Leyser O, Nelson D (2015) SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27:3143–3159. doi: 10.1105/tpc.15.00562 CrossRefPubMedGoogle Scholar
  39. Stanga JP, Smith SM, Briggs WR, Nelson DC (2013) SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol 163:318–330. doi: 10.1104/pp.113.221259 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Stanga JP, Morffy N, Nelson DC (2016) Functional redundancy in the control of seedling growth by the karrikin signaling pathway. Planta. doi: 10.1007/s00425-015-2458-2 PubMedGoogle Scholar
  41. Sun X-D, Ni M (2011) HYPOSENSITIVE TO LIGHT, an alpha/beta fold protein, acts downstream of ELONGATED HYPOCOTYL 5 to regulate seedling de-etiolation. Mol Plant 4:116–126. doi: 10.1093/mp/ssq055 CrossRefPubMedGoogle Scholar
  42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Toh S, Holbrook-Smith D, Stogios PJ, Onopriyenko O, Lumba S, Tsuchiya Y, Savchenko A, McCourt P (2015) Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350:203–207. doi: 10.1126/science.aac9476 CrossRefPubMedGoogle Scholar
  44. Tsuchiya Y, Yoshimura M, Sato Y, Kuwata K, Toh S, Holbrook-Smith D, Zhang H, McCourt P, Itami K, Kinoshita T, Hagihara S (2015) Parasitic plants. Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349:864–868. doi: 10.1126/science.aab3831 CrossRefPubMedGoogle Scholar
  45. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200. doi: 10.1038/nature07272 CrossRefPubMedGoogle Scholar
  46. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. doi: 10.1093/nar/gkm306 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X (2013) Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27:681–688. doi: 10.1016/j.devcel.2013.11.010 CrossRefPubMedGoogle Scholar
  48. Wang L, Wang B, Jiang L, Liu X, Li X, Lu Z, Meng X, Wang Y, Smith SM, Li J (2015) Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27:3128–3142. doi: 10.1105/tpc.15.00605 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139:1285–1295. doi: 10.1242/dev.074567 CrossRefPubMedGoogle Scholar
  50. Waters MT, Scaffidi A, Flematti G, Smith SM (2015a) Substrate-induced degradation of the alpha/beta-fold hydrolase KARRIKIN INSENSITIVE2 requires a functional catalytic triad but is independent of MAX2. Mol Plant 8:814–817. doi: 10.1016/j.molp.2014.12.020 CrossRefPubMedGoogle Scholar
  51. Waters MT, Scaffidi A, Moulin SL, Sun YK, Flematti GR, Smith SM (2015b) A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 27:1925–1944. doi: 10.1105/tpc.15.00146 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Xie X, Yoneyama K, Kisugi T, Uchida K, Ito S, Akiyama K, Hayashi H, Yokota T, Nomura T, Yoneyama K (2013) Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol Plant 6:153–163. doi: 10.1093/mp/sss139 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. doi: 10.1093/molbev/msm088 CrossRefPubMedGoogle Scholar
  54. Yoneyama K, Kisugi T, Xie X, Yoneyama K (2013) Chemistry of strigolactones: Why and how do plants produce so many strigolactones? In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1, 2. Wiley, Hoboken, NJ, pp 373–379. doi: 10.1002/9781118297674.ch34 CrossRefGoogle Scholar
  55. Zhao LH, Zhou XE, Wu ZS, Yi W, Xu Y, Li S, Xu TH, Liu Y, Chen RZ, Kovach A, Kang Y, Hou L, He Y, Xie C, Song W, Zhong D, Wang Y, Li J, Zhang C, Melcher K, Xu HE (2013) Crystal structures of two phytohormone signal-transducing alpha/beta hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res 23:436–439. doi: 10.1038/cr.2013.19 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Zhao LH, Zhou XE, Yi W, Wu Z, Liu Y, Kang Y, Hou L, de Waal PW, Li S, Jiang Y, Scaffidi A, Flematti GR, Smith SM, Lam VQ, Griffin PR, Wang Y, Li J, Melcher K, Xu HE (2015) Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res 25:1219–1236. doi: 10.1038/cr.2015.122 CrossRefPubMedGoogle Scholar
  57. Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L, Ma W, Gao H, Chen J, Yang C, Wang D, Tan J, Zhang X, Guo X, Wang J, Jiang L, Liu X, Chen W, Chu J, Yan C, Ueno K, Ito S, Asami T, Cheng Z, Lei C, Zhai H, Wu C, Wang H, Zheng N, Wan J (2013) D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 504:406–410. doi: 10.1038/nature12878 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Zimmer AD, Lang D, Buchta K, Rombauts S, Nishiyama T, Hasebe M, Van de Peer Y, Rensing SA, Reski R (2013) Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Genom 14:498. doi: 10.1186/1471-2164-14-498 CrossRefGoogle Scholar
  59. Zwanenburg B, Pospisil T (2013) Structure and activity of strigolactones: new plant hormones with a rich future. Mol Plant 6:38–62. doi: 10.1093/mp/sss141 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Mauricio Lopez-Obando
    • 1
  • Caitlin E. Conn
    • 2
  • Beate Hoffmann
    • 1
  • Rohan Bythell-Douglas
    • 3
  • David C. Nelson
    • 2
    Email author
  • Catherine Rameau
    • 1
  • Sandrine Bonhomme
    • 1
    Email author
  1. 1.Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRSUniversité Paris-SaclayVersailles CedexFrance
  2. 2.Department of GeneticsUniversity of GeorgiaAthensUSA
  3. 3.Department of MedicineImperial College LondonLondonUK

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