Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis


Autoři: Aline Herger aff001;  Shibu Gupta aff001;  Gabor Kadler aff001;  Christina Maria Franck aff001;  Aurélien Boisson-Dernier aff002;  Christoph Ringli aff001
Působiště autorů: Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland aff001;  Biocenter, Botanical Institute, University of Cologne, Cologne, Germany aff002
Vyšlo v časopise: Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008847
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008847

Souhrn

Plant cell growth requires the coordinated expansion of the protoplast and the cell wall, which is controlled by an elaborate system of cell wall integrity (CWI) sensors linking the different cellular compartments. LRR-eXtensins (LRXs) are cell wall-attached extracellular regulators of cell wall formation and high-affinity binding sites for RALF (Rapid ALkalinization Factor) peptide hormones that trigger diverse physiological processes related to cell growth. LRXs function in CWI sensing and in the case of LRX4 of Arabidopsis thaliana, this activity was shown to involve interaction with the transmembrane Catharanthus roseus Receptor-Like Kinase1-Like (CrRLK1L) protein FERONIA (FER). Here, we demonstrate that binding of RALF1 and FER is common to most tested LRXs of vegetative tissue, including LRX1, the main LRX protein of root hairs. Consequently, an lrx1-lrx5 quintuple mutant line develops shoot and root phenotypes reminiscent of the fer-4 knock-out mutant. The previously observed membrane-association of LRXs, however, is FER-independent, suggesting that LRXs bind not only FER but also other membrane-localized proteins to establish a physical link between intra- and extracellular compartments. Despite evolutionary diversification of various LRX proteins, overexpression of several chimeric LRX constructs causes cross-complementation of lrx mutants, indicative of comparable functions among members of this protein family. Suppressors of the pollen-growth defects induced by mutations in the CrRLK1Ls ANXUR1/2 also alleviate lrx1 lrx2-induced mutant root hair phenotypes. This suggests functional similarity of LRX-CrRLK1L signaling processes in very different cell types and indicates that LRX proteins are components of conserved processes regulating cell growth.

Klíčová slova:

Cell membranes – Membrane proteins – Phenotypes – Plant cell walls – Protein domains – Protein interactions – Root hairs – Seedlings


Zdroje

1. Houston K, Tucker MR, Chowdhury J, Shirley N, Little A (2016) The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front Plant Sci 7: 984. doi: 10.3389/fpls.2016.00984 27559336

2. Braidwood L, Breuer C, Sugimoto K (2014) My body is a cage: mechanisms and modulation of plant cell growth. New Phytol 201: 388–402. doi: 10.1111/nph.12473 24033322

3. Wolf S, Hematy K, Hoefte H (2012) Growth control and cell wall signaling in plants. In: Merchant SS, editor. Annual Review of Plant Biology, Vol 63. pp. 381–407. doi: 10.1146/annurev-arplant-042811-105449 22224451

4. Hématy K, Sado P-E, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou J-P, Höfte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17: 922–931. doi: 10.1016/j.cub.2007.05.018 17540573

5. Schoenaers S, Balcerowicz D, Breen G, Hill K, Zdanio M, Mouille G, Holman TJ, Oh J, Wilson MH, Nikonorova N, Vu LD, De Smet I, Swarup R, De Vos WH, Pintelon I, Adriaensen D, Grierson C, Bennett MJ, Vissenberg K (2018) The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth. Curr Biol 28: 722–732. doi: 10.1016/j.cub.2018.01.050 29478854

6. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U (2009) Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136: 3279–3288. doi: 10.1242/dev.040071 19736323

7. Guo HQ, Li L, Ye HX, Yu XF, Algreen A, Yin YH (2009) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci USA 106: 7648–7653. doi: 10.1073/pnas.0812346106 19383785

8. Franck CM, Westermann J, Boisson-Dernier A (2018a) Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond. In: Merchant SS, editor. Annual Review of Plant Biology, Vol 69. pp. 301–328. doi: 10.1146/annurev-arplant-042817-040557 29539271

9. Kwon T, Sparks JA, Liao FQ, Blancaflor EB (2018) ERULUS is a plasma membrane-localized receptor-like kinase that specifies root hair growth by maintaining tip-focused cytoplasmic calcium oscillations. Plant Cell 30: 1173–1177. doi: 10.1105/tpc.18.00316 29802213

10. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317: 656–660. doi: 10.1126/science.1143562 17673660

11. Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan QH, Liu MC, Maman J, Steinhorst L, Schmitz-Thom I, Yvon R, Kudla J, Wu HM, Cheung AY, Dinneny JR (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28: 666–675. doi: 10.1016/j.cub.2018.01.023 29456142

12. Shih HW, Miller ND, Dai C, Spalding EP, Monshausen GB (2014) The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr Biol 24: 1887–1892. doi: 10.1016/j.cub.2014.06.064 25127214

13. Li C, Wu HM, Cheung AY (2016) FERONIA and her pals: functions and mechanisms. Plant Physiol 171: 2379–2392. doi: 10.1104/pp.16.00667 27342308

14. Pearce G, Moura DS, Stratmann J, Ryan CA (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 98: 12843–12847. doi: 10.1073/pnas.201416998 11675511

15. Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343: 408–411. doi: 10.1126/science.1244454 24458638

16. Haruta M, Monshausen G, Gilroy S, Sussman MR (2008) A cytoplasmic Ca2+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: Identification of AtRALF1 peptide. Biochemistry 47: 6311–6321. doi: 10.1021/bi8001488 18494498

17. Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, Belkhadir Y, Zipfel C (2017) The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355: 287–289. doi: 10.1126/science.aal2541 28104890

18. Murphy E, De Smet I (2014) Understanding the RALF family: a tale of many species. Trends Plant Sci 19: 664–671. doi: 10.1016/j.tplants.2014.06.005 24999241

19. Nissen KS, Willats WGT, Malinovsky FG (2016) Understanding CrRLK1L Function: cell walls and growth control. Trends Plant Sci 21: 516–527. doi: 10.1016/j.tplants.2015.12.004 26778775

20. Gonneau M, Desprez T, Martin M, Doblas VG, Bacete L, Miart F, Sormani R, Hematy K, Renou J, Landrein B, Murphy E, Van De Cotte B, Vernhettes S, De Smet I, Hofte H (2018) Receptor kinase THESEUS1 is a rapid alkalinization factor 34 receptor in Arabidopsis. Curr Biol 28: 2452–2458. doi: 10.1016/j.cub.2018.05.075 30057301

21. Ge ZX, Bergonci T, Zhao YL, Zou YJ, Du S, Liu MC, Luo XJ, Ruan H, Garcia-Valencia LE, Zhong S, Hou SY, Huang QP, Lai LH, Moura DS, Gu HY, Dong J, Wu HM, Dresselhaus T, Xiao JY, Cheung AY, Qu LJ (2017) Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358: 1596–1599. doi: 10.1126/science.aao3642 29242234

22. Li C, Yeh FL, Cheung AY, Duan Q, Kita D, Liu MC, Maman J, Luu EJ, Wu BW, Gates L, Jalal M, Kwong A, Carpenter H, Wu HM (2015) Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. Elife 4: e06587.

23. Duan QH, Kita D, Li C, Cheung AY, Wu HM (2010) FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci USA 107: 17821–17826. doi: 10.1073/pnas.1005366107 20876100

24. Chen J, Yu F, Liu Y, Du CQ, Li XS, Zhu SR, Wang XC, Lan WZ, Rodriguez PL, Liu XM, Li DP, Chen LB, Luan S (2016) FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis. Proc Natl Acad Sci USA 113: E5519–E5527. doi: 10.1073/pnas.1608449113 27566404

25. Du CQ, Li XS, Chen J, Chen WJ, Li B, Li CY, Wang L, Li JL, Zhao XY, Lin JZ, Liu XM, Luan S, Yu F (2016) Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proc Natl Acad Sci USA 113: E8326–E8334. doi: 10.1073/pnas.1609626113 27930296

26. Dressano K, Ceciliato PHO, Silva AL, Guerrero-Abad JC, Bergonci T, Ortiz-Morea FA, Burger M, Silva-Filho MC, Moura DS (2017) BAK1 is involved in AtRALF1-induced inhibition of root cell expansion. PLoS Genet 13: e1007053. doi: 10.1371/journal.pgen.1007053 29028796

27. Xiao Y, Stegmann M, Han ZF, DeFalco TA, Parys K, Xu L, Belkhadir Y, Zipfel C, Chai JJ (2019) Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature 572: 270–274. doi: 10.1038/s41586-019-1409-7 31291642

28. Boisson-Dernier A, Franck CM, Lituiev DS, Grossniklaus U (2015) Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. Proc Natl Acad Sci USA 112: 12211–12216. doi: 10.1073/pnas.1512375112 26378127

29. Franck CM, Westermann J, Burssner S, Lentz R, Lituiev DS, Boisson-Dernier A (2018b) The protein phosphatases ATUNIS1 and ATUNIS2 regulate cell wall integrity in tip-growing cells. Plant Cell 30: 1906–1923.

30. Herger A, Dünser K, Kleine-Vehn J, Ringli C (2019) Leucine-rich repeat extensin proteins and their role in cell wall sensing. Curr Biol 29: R851–R858. doi: 10.1016/j.cub.2019.07.039 31505187

31. Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol 153: 485–513. doi: 10.1104/pp.110.156554 20395450

32. Borassi C, Sede AR, Mecchia MA, Salgado Salter JD, Marzol E, Muschietti JP, Estevez JM (2016) An update on cell surface proteins containing extensin-motifs. ‎J Exp Bot 67: 477–487. doi: 10.1093/jxb/erv455 26475923

33. Baumberger N, Ringli C, Keller B (2001) The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev 15: 1128–1139. doi: 10.1101/gad.200201 11331608

34. Ringli C (2010) The hydroxyproline-rich glycoprotein domain of the Arabidopsis LRX1 requires Tyr for function but not for insolubilization in the cell wall. Plant J 63: 662–669. doi: 10.1111/j.1365-313X.2010.04270.x 20545889

35. Baumberger N, Steiner M, Ryser U, Keller B, Ringli C (2003b) Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development. Plant J 35: 71–81.

36. Draeger C, Fabrice TN, Gineau E, Mouille G, Kuhn BM, Moller I, Abdou M-T, Frey B, Pauly M, Bacic A, Ringli C (2015) Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth. BMC Plant Biol 15: doi: 10.1186/s12870-12015-10548-12878

37. Fabrice T, Vogler H, Draeger C, Munglani G, Gupta S, Herger AG, Knox P, Grossniklaus U, Ringli C (2018) LRX proteins play a crucial role in pollen grain and pollen tube cell wall development. Plant Physiol 176: 1981–1992. doi: 10.1104/pp.17.01374 29247121

38. Sede AR, Borassi C, Wengier DL, Mecchia MA, Estevez JM, Muschietti JP (2018) Arabidopsis pollen extensins LRX are required for cell wall integrity during pollen tube growth. Febs Letters 592: 233–243. doi: 10.1002/1873-3468.12947 29265366

39. Wang XX, Wang KY, Yin GM, Liu XY, Liu M, Cao NN, Duan YZ, Gao H, Wang WL, Ge WN, Wang J, Li R, Guo Y (2018) Pollen-expressed leucine-rich repeat extensins are essential for pollen germination and growth. Plant Physiol 176: 1993–2006. doi: 10.1104/pp.17.01241 29269573

40. Zhao CZ, Zayed O, Yu ZP, Jiang W, Zhu PP, Hsu CC, Zhang LR, Tao WA, Lozano-Duran R, Zhu JK (2018) Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci USA 115: 13123–13128. doi: 10.1073/pnas.1816991115 30514814

41. Dünser K, Gupta S, Herger A, Feraru MI, Ringli C, Kleine-Vehn J (2019) Extracellular matrix sensing by FERONIA and Leucine-Rich Repeat Extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana. EMBO J 38: e100353. doi: 10.15252/embj.2018100353 30850388

42. Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A, Gagliardini V, Martinez-Bernardini A, Fabrice TN, Ringli C, Muschietti JP, Grossniklaus U (2017) RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358: 1600–1603. doi: 10.1126/science.aao5467 29242232

43. Diet A, Link B, Seifert GJ, Schellenberg B, Wagner U, Pauly M, Reiter WD, Ringli C (2006) The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-L-rhamnose synthase. Plant Cell 18: 1630–1641. doi: 10.1105/tpc.105.038653 16766693

44. Leiber RM, John F, Verhertbruggen Y, Diet A, Knox JP, Ringli C (2010) The TOR pathway modulates the structure of cell walls in Arabidopsis. Plant Cell 22: 1898–1908. doi: 10.1105/tpc.109.073007 20530756

45. Dong QK, Zhang ZW, Liu YT, Tao LZ, Liu HL (2019) FERONIA regulates auxin-mediated lateral root development and primary root gravitropism. Febs Letters 593: 97–106. doi: 10.1002/1873-3468.13292 30417333

46. Grabov A, Ashley MK, Rigas S, Hatzopoulos P, Dolan L, Vicente-Agullo F (2005) Morphometric analysis of root shape. New Phytol 165: 641–651. doi: 10.1111/j.1469-8137.2004.01258.x 15720674

47. Baumberger N, Doesseger B, Guyot R, Diet A, Parsons RL, Clark MA, Simmons MP, Bedinger P, Goff SA, Ringli C, Keller B (2003a) Whole-genome comparison of leucine-rich repeat extensins in Arabidopsis and rice: a conserved family of cell wall proteins form a vegetative and a reproductive clade. Plant Physiol 131: 1313–1326.

48. Liu X, Wolfe R, Welch LR, Domozych DS, Popper ZA, Showalter AM (2016) Bioinformatic identification and analysis of extensins in the plant kingdom. PLoS One 11: e0150177. doi: 10.1371/journal.pone.0150177 26918442

49. Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19: 1327–1331. doi: 10.1016/j.cub.2009.06.064 19646876

50. Liu P, Haruta M, Minkoff BB, Sussman MR (2018) Probing a plant plasma membrane receptor kinase's three-dimensional structure using mass spectrometry-based protein footprinting. Biochemistry 57: 5159–5168. doi: 10.1021/acs.biochem.8b00471 30124284

51. Moussu S, Broyart C, Santos-Fernandez G, Augustin S, Wehrle S, Grossniklaus U, Santiago J (2020) Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth. Proceedings of the National Academy of Sciences 117.

52. Srivastava R, Liu JX, Guo HQ, Yin YH, Howell SH (2009) Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J 59: 930–939. doi: 10.1111/j.1365-313X.2009.03926.x 19473327

53. Showalter AM, Basu D (2016) Extensin and arabinogalactan-protein biosynthesis: glycosyltransferases, research challenges, and biosensors. Front Plant Sci 7: 814. doi: 10.3389/fpls.2016.00814 27379116

54. Qi XY, Behrens BX, West PR, Mort AJ (1995) Solubilization and partial characterization of extensin fragments from cell walls of cotton suspension-cultures—evidence for a covalent cross-link between extensin and pectin. Plant Physiol 108: 1691–1701. doi: 10.1104/pp.108.4.1691 7659756

55. Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Molec Biol 49: 281–309.

56. Knox JP (2008) Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol 11: 308–313. doi: 10.1016/j.pbi.2008.03.001 18424171

57. Dardelle F, Lehner A, Ramdani Y, Bardor M, Lerouge P, Driouich A, Mollet JC (2010) Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol 153: 1563–1576. doi: 10.1104/pp.110.158881 20547702

58. Diet A, Brunner S, Ringli C (2004) The enl mutants enhance the lrx1 root hair mutant phenotype of Arabidopsis thaliana. Plant Cell Physiol 45: 734–741. doi: 10.1093/pcp/pch084 15215508

59. Gleave AP (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20: 1203–1207. doi: 10.1007/BF00028910 1463857

60. Laby RJ, Kincaid MS, Kim DG, Gibson SI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23: 587–596. doi: 10.1046/j.1365-313x.2000.00833.x 10972885

61. Matsui K, Tanaka H, Ohme-Takagi M (2004) Suppression of the biosynthesis of proanthocyanidin in Arabidopsis by a chimeric PAP1 repressor. Plant Biotechnology Journal 2: 487–493. doi: 10.1111/j.1467-7652.2004.00094.x 17147621

62. Bourras S, Kunz L, Xue M, Praz CR, Mueller MC, Kalin C, Schlafli M, Ackermann P, Fluckiger S, Parlange F, Menardo F, Schaefer LK, Ben-David R, Roffler S, Oberhaensli S, Widrig V, Lindner S, Isaksson J, Wicker T, Yu D, Keller B (2019) The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat. Nat Commun 10: 2292. doi: 10.1038/s41467-019-10274-1 31123263

63. James P, Halladay J, Craig EA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425–1436. 8978031

64. Jasinski M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13: 1095–1107. 11340184


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