SCARN a Novel Class of SCAR Protein That Is Required for Root-Hair Infection during Legume Nodulation

1. Krause M, Gautreau A (2014) Steering cell migration: lamellipodium dynamics and the regulation of directional persistence. Nat Rev Mol Cell Biol 15 : 577–590. doi: 10.1038/nrm3861 25145849

2. Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, et al. (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J Cell Biol 184 : 269–280. doi: 10.1083/jcb.200806185 19171759

3. Yanagisawa M, Zhang C, Szymanski DB (2013) ARP2/3-dependent growth in the plant kingdom: SCARs for life. Front Plant Sci 4 : 166. doi: 10.3389/fpls.2013.00166 23802001

4. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68 : 280–300. 15187185

5. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5 : 619–633. 17632573

6. Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59 : 519–546. doi: 10.1146/annurev.arplant.59.032607.092839 18444906

7. Breakspear A, Liu C, Roy S, Stacey N, Rogers C, et al. (2014) The root hair "infectome" of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for Auxin signaling in rhizobial infection. Plant Cell 26 : 4680–4701. doi: 10.1105/tpc.114.133496 25527707

8. Esseling JJ (2003) Nod Factor-induced root hair curling: continuous polar growth towards the point of Nod Factor application. Plant Physiology 132 : 1982–1988. 12913154

9. Crdenas L, Vidali L, Domnguez J, Prez H, Snchez F, et al. (1998) Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 116 : 871–877. 9501120

10. Heidstra R, Geurts R, Franssen H, Spaink HP, Van Kammen A, et al. (1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol 105 : 787–797. 12232242

11. Timmers AC, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126 : 3617–3628. 10409507

12. Zepeda I, Sanchez-Lopez R, Kunkel JG, Banuelos LA, Hernandez-Barrera A, et al. (2014) Visualization of highly dynamic F-actin plus ends in growing Phaseolus vulgaris root hair cells and their responses to Rhizobium etli nod factors. Plant Cell Physiol 55 : 580–592. doi: 10.1093/pcp/pct202 24399235

13. Fournier J, Timmers AC, Sieberer BJ, Jauneau A, Chabaud M, et al. (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol 148 : 1985–1995. doi: 10.1104/pp.108.125674 18931145

14. Monahan-Giovanelli H, Pinedo CA, Gage DJ (2006) Architecture of infection thread networks in developing root nodules induced by the symbiotic bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiol 140 : 661–670. 16384905

15. Desbrosses GJ, Stougaard J (2011) Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host & Microbe 10 : 348–358.

16. Foucher F, Kondorosi E (2000) Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 43 : 773–786. 11089876

17. Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45 : 119–144. doi: 10.1146/annurev-genet-110410-132549 21838550

18. Downie JA (2014) Legume nodulation. Curr Biol 24: R184–190. doi: 10.1016/j.cub.2014.01.028 24602880

19. Singh S, Katzer K, Lambert J, Cerri M, Parniske M (2014) CYCLOPS, A DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host & Microbe 15 : 139–152. doi: 10.1016/j.chom.2014.01.011 24528861

20. Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, et al. (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci U S A 101 : 4701–4705. 15070781

21. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402 : 191–195. 10647012

22. Morieri G, Martinez EA, Jarynowski A, Driguez H, Morris R, et al. (2013) Host-specific Nod-factors associated with Medicago truncatula nodule infection differentially induce calcium influx and calcium spiking in root hairs. New Phytol 200 : 656–662. doi: 10.1111/nph.12475 24015832

23. Downie JA (2014) Calcium signals in plant immunity: a spiky issue. New Phytol 204 : 733–735. doi: 10.1111/nph.13119 25367606

24. Zgadzaj R, James EK, Kelly S, Kawaharada Y, de Jonge N, et al. (2015) A legume genetic framework controls infection of nodules by symbiotic and endophytic bacteria. PLoS Genet 11: e1005280. doi: 10.1371/journal.pgen.1005280 26042417

25. Kiss E, Olah B, Kalo P, Morales M, Heckmann AB, et al. (2009) LIN, a novel type of U-box/WD40 protein, controls early infection by rhizobia in legumes. Plant Physiol 151 : 1239–1249. doi: 10.1104/pp.109.143933 19776163

26. Yano K, Shibata S, Chen WL, Sato S, Kaneko T, et al. (2009) CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis. Plant J 60 : 168–180. doi: 10.1111/j.1365-313X.2009.03943.x 19508425

27. Arrighi JF, Godfroy O, de Billy F, Saurat O, Jauneau A, et al. (2008) The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection. Proc Natl Acad Sci U S A 105 : 9817–9822. doi: 10.1073/pnas.0710273105 18621693

28. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, et al. (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19 : 1221–1234. 17449807

29. Laporte P, Lepage A, Fournier J, Catrice O, Moreau S, et al. (2014) The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection. J Exp Bot 65 : 481–494. doi: 10.1093/jxb/ert392 24319255

30. Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, et al. (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci U S A 109 : 633–638. doi: 10.1073/pnas.1113992109 22203959

31. Yokota K, Fukai E, Madsen LH, Jurkiewicz A, Rueda P, et al. (2009) Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21 : 267–284. doi: 10.1105/tpc.108.063693 19136645

32. Miyahara A, Richens J, Starker C, Morieri G, Smith L, et al. (2011) Conservation in function of a SCAR/WAVE component during infection thread and root hair growth in Medicago truncatula. Mol Plant Microbe Interact 23 : 1553–1562.

33. Hossain MS, Liao J, James EK, Sato S, Tabata S, et al. (2012) Lotus japonicus ARPC1 is required for rhizobial infection. Plant Physiol 160 : 917–928. doi: 10.1104/pp.112.202572 22864583

34. Lombardo F, Heckmann AB, Miwa H, Perry JA, Yano K, et al. (2006) Identification of symbiotically defective mutants of Lotus japonicus affected in infection thread growth. Mol Plant Microbe Interact 19 : 1444–1450. 17153928

35. Perry J, Brachmann A, Welham T, Binder A, Charpentier M, et al. (2009) TILLING in Lotus japonicus identified large allelic series for symbiosis genes and revealed a bias in functionally defective ethyl methanesulfonate alleles toward glycine replacements. Plant Physiol 151 : 1281–1291. doi: 10.1104/pp.109.142190 19641028

36. Perry JA, Wang TL, Welham TJ, Gardner S, Pike JM, et al. (2003) A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiol 131 : 866–871. 12644638

37. Zhang C, Mallery EL, Schlueter J, Huang S, Fan Y, et al. (2008) Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis. Plant Cell 20 : 995–1011. doi: 10.1105/tpc.107.055350 18424615

38. Urbanski DF, Malolepszy A, Stougaard J, Andersen SU (2013) High-throughput and targeted genotyping of Lotus japonicus LORE1 insertion mutants. Methods Mol Biol 1069 : 119–146. doi: 10.1007/978-1-62703-613-9_10 23996313

39. Fukai E, Soyano T, Umehara Y, Nakayama S, Hirakawa H, et al. (2012) Establishment of a Lotus japonicus gene tagging population using the exon-targeting endogenous retrotransposon LORE1. Plant J 69 : 720–730. doi: 10.1111/j.1365-313X.2011.04826.x 22014259

40. Maekawa T, Kusakabe M, Shimoda Y, Sato S, Tabata S, et al. (2008) Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol Plant Microbe Interact 21 : 375–382. doi: 10.1094/MPMI-21-4-0375 18321183

41. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, et al. (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1 : 10. doi: 10.1038/ncomms1009 20975672

42. Murray J, Karas B, Ross L, Brachmann A, Wagg C, et al. (2006) Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype. Mol Plant Microbe Interact 19 : 1082–1091. 17022172

43. Basu D, Le J, El-Essal Sel D, Huang S, Zhang C, et al. (2005) DISTORTED3/SCAR2 is a putative arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell 17 : 502–524. 15659634

44. Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell 17 : 2314–2326. 16006582

45. Hayashi T, Shimoda Y, Sato S, Tabata S, Imaizumi-Anraku H, et al. (2014) Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca(2+) spiking. Plant J 77 : 146–159. doi: 10.1111/tpj.12374 24329948

46. Soyano T, Hirakawa H, Sato S, Hayashi M, Kawaguchi M (2014) Nodule Inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. Proc Natl Acad Sci U S A 111 : 14607–14612. doi: 10.1073/pnas.1412716111 25246578

47. Soyano T, Kouchi H, Hirota A, Hayashi M (2013) NODULE INCEPTION directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet 9: e1003352. doi: 10.1371/journal.pgen.1003352 23555278

48. Uhrig JF, Mutondo M, Zimmermann I, Deeks MJ, Machesky LM, et al. (2007) The role of Arabidopsis SCAR genes in ARP2-ARP3-dependent cell morphogenesis. Development 134 : 967–977. 17267444

49. Kollmar M, Lbik D, Enge S (2012) Evolution of the eukaryotic ARP2/3 activators of the WASP family: WASP, WAVE, WASH, and WHAMM, and the proposed new family members WAWH and WAML. BMC Res Notes 5 : 88. doi: 10.1186/1756-0500-5-88 22316129

50. Li QG, Zhang L, Li C, Dunwell JM, Zhang YM (2013) Comparative genomics suggests that an ancestral polyploidy event leads to enhanced root nodule symbiosis in the Papilionoideae. Mol Biol Evol 30 : 2602–2611. doi: 10.1093/molbev/mst152 24008584

51. de Ruijter NCA, Bisseling T., and Emons A.M.C. (1999) Rhizobium Nod factors induce an increase in sub-apical fine bundles of actin filaments in Vicia sativa root hairs within minutes. Mol Plant Microbe Interact 12 : 829–832.

52. Rounds CM, Bezanilla M (2013) Growth mechanisms in tip-growing plant cells. Annu Rev Plant Biol 64 : 243–265. doi: 10.1146/annurev-arplant-050312-120150 23451782

53. Sampathkumar A, Lindeboom JJ, Debolt S, Gutierrez R, Ehrhardt DW, et al. (2011) Live cell imaging reveals structural associations between the actin and microtubule cytoskeleton in Arabidopsis. Plant Cell 23 : 2302–2313. doi: 10.1105/tpc.111.087940 21693695

54. Deeks MJ, Hussey PJ (2005) Arp2/3 and SCAR: plants move to the fore. Nat Rev Mol Cell Biol 6 : 954–964. 16341081

55. Le J, Mallery EL, Zhang C, Brankle S, Szymanski DB (2006) Arabidopsis BRICK1/HSPC300 is an essential WAVE-complex subunit that selectively stabilizes the Arp2/3 activator SCAR2. Curr Biol 16 : 895–901. 16584883

56. Veltman DM, Insall RH (2010) WASP family proteins: their evolution and its physiological implications. Mol Biol Cell 21 : 2880–2893. doi: 10.1091/mbc.E10-04-0372 20573979

57. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17 : 657–665. 10230063

58. King JS, Veltman DM, Georgiou M, Baum B, Insall RH (2010) SCAR/WAVE is activated at mitosis and drives myosin-independent cytokinesis. J Cell Sci 123 : 2246–2255. doi: 10.1242/jcs.063735 20530573

59. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, et al. (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144 : 324–335. 17369436

60. Rotty JD, Wu C, Bear JE (2013) New insights into the regulation and cellular functions of the ARP2/3 complex. Nat Rev Mol Cell Biol 14 : 7–12. doi: 10.1038/nrm3492 23212475

61. Basu D, El-Assal Sel D, Le J, Mallery EL, Szymanski DB (2004) Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development. Development 131 : 4345–4355. 15294869

62. Yang Z (2008) Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol 24 : 551–575. doi: 10.1146/annurev.cellbio.23.090506.123233 18837672

63. Ke D, Fang Q, Chen C, Zhu H, Chen T, et al. (2012) The small GTPase ROP6 interacts with NFR5 and is involved in nodule formation in Lotus japonicus. Plant Physiol 159 : 131–143. doi: 10.1104/pp.112.197269 22434040

64. Wang C, Zhu M, Duan L, Yu H, Chang X, et al. (2015) Lotus japonicus Clathrin Heavy Chain1 is associated with Rho-Like GTPase ROP6 and involved in nodule formation. Plant Physiol 167 : 1497–1510. doi: 10.1104/pp.114.256107 25717037

65. Lei MJ, Wang Q, Li X, Chen A, Luo L, et al. (2015) The Small GTPase ROP10 of Medicago truncatula is required for both tip growth of root hairs and Nod Factor-induced root hair deformation. Plant Cell 27 : 806–822. doi: 10.1105/tpc.114.135210 25794934

66. Fahraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16 : 374–381. 13416514

67. Vernie T, Moreau S, de Billy F, Plet J, Combier JP, et al. (2008) EFD is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20 : 2696–2713. doi: 10.1105/tpc.108.059857 18978033

68. Giovannetti M, and Mosse B. (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84 : 489–500.

69. Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19 : 914–923. 16903357

70. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30 : 2725–2729. doi: 10.1093/molbev/mst197 24132122