Cellular and Molecular Life Sciences

, Volume 75, Issue 18, pp 3329–3338 | Cite as

Pivotal role of LBD16 in root and root-like organ initiation

  • Wu Liu
  • Jie Yu
  • Yachao Ge
  • Peng Qin
  • Lin XuEmail author


In the post-embryonic stage of Arabidopsis thaliana, roots can be initiated from the vascular region of the existing roots or non-root organs; they are designated as lateral roots (LRs) and adventitious roots (ARs), respectively. Some root-like organs can also be initiated from the vasculature. In tissue culture, auxin-induced callus, which is a group of pluripotent root-primordium-like cells, is formed via the rooting pathway. The formation of feeding structures from the vasculature induced by root-knot nematodes also borrows the rooting pathway. In this review, we summarize and discuss recent progress on the role of LATERAL ORGAN BOUNDARIES DOMAIN16 (LBD16; also known as ASYMMETRIC LEAVES2-LIKE18, ASL18), a member of the LBD/ASL gene family encoding plant-specific transcription factors, in roots and root-like organ initiation. Different root and root-like organ initiation processes have distinct priming mechanisms to specify founder cells. All these priming mechanisms converge to activate LBD16 expression in the primed founder cells. The activation of LBD16 expression leads to organ initiation via promotion of cell division and establishment of root-primordium identity. Therefore, LBD16 might play a common and pivotal role in root and root-like organ initiation.


Root founder cell Lateral root Adventitious root LBD16 Callus Root-knot nematodes 



Adventitious root












Callus-inducing medium




Enhanced yeast one-hybrid






Lateral root




Root-inducing medium




Shoot-inducing medium







We apologize for references not cited due to space limitations. This work was supported by grants from the National Natural Science Foundation of China (31630007), National Basic Research Program of China (973 Program, 2014CB943500), the Key Research Program of CAS (QYZDB-SSW-SMC010), the Strategic Priority Research Program “Molecular Mechanism of Plant Growth and Development” of CAS (XDPB0403), and National Key Laboratory of Plant Molecular Genetics.

Compliance with ethical standards

Conflict of interest

No conflicts of interest declared.


  1. 1.
    Falasca G, Altamura MM (2003) Histological analysis of adventitious rooting in Arabidopsis thaliana (L.) Heynh seedlings. Plant Biosyst 137(3):265–274CrossRefGoogle Scholar
  2. 2.
    da Costa CT, de Almeida MR, Ruedell CM, Schwambach J, Maraschin FS, Fett-Neto AG (2013) When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci 4:133. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Atkinson JA, Rasmussen A, Traini R, Voss U, Sturrock C, Mooney SJ, Wells DM, Bennett MJ (2014) Branching out in roots: uncovering form, function, and regulation. Plant Physiol 166(2):538–550. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666. CrossRefPubMedGoogle Scholar
  5. 5.
    Verstraeten I, Schotte S, Geelen D (2014) Hypocotyl adventitious root organogenesis differs from lateral root development. Front Plant Sci 5:495. CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Birnbaum KD (2016) How many ways are there to make a root? Curr Opin Plant Biol 34:61–67. CrossRefPubMedGoogle Scholar
  7. 7.
    Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170(2):603–617. CrossRefPubMedGoogle Scholar
  8. 8.
    Xu L (2018) De novo root regeneration from leaf explants: wounding, auxin, and cell fate transition. Curr Opin Plant Biol 41:39–45. CrossRefPubMedGoogle Scholar
  9. 9.
    Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19(1):118–130. CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329(5997):1306–1311. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Xuan W, Audenaert D, Parizot B, Moller BK, Njo MF, De Rybel B, De Rop G, Van Isterdael G, Mahonen AP, Vanneste S, Beeckman T (2015) Root cap-derived auxin pre-patterns the longitudinal axis of the Arabidopsis root. Curr Biol 25(10):1381–1388. CrossRefPubMedGoogle Scholar
  12. 12.
    Xuan W, Band LR, Kumpf RP, Van Damme D, Parizot B, De Rop G, Opdenacker D, Moller BK, Skorzinski N, Njo MF, De Rybel B, Audenaert D, Nowack MK, Vanneste S, Beeckman T (2016) Cyclic programmed cell death stimulates hormone signaling and root development in Arabidopsis. Science 351(6271):384–387. CrossRefPubMedGoogle Scholar
  13. 13.
    Du Y, Scheres B (2018) Lateral root formation and the multiple roles of auxin. J Exp Bot 69(2):155–167. CrossRefPubMedGoogle Scholar
  14. 14.
    Stoeckle D, Thellmann M, Vermeer JE (2018) Breakout-lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Biol 41:67–72. CrossRefPubMedGoogle Scholar
  15. 15.
    Esau K (1965) Plant anatomy, 2nd edn. Wiley, New YorkGoogle Scholar
  16. 16.
    Barlow PW (1986) Adventitious roots of whole plants: their forms, functions, and evolution. In: Jackson MB (ed) New root formation in plants and cuttings. Martinus Nijhoff, Hingham, pp 67–110CrossRefGoogle Scholar
  17. 17.
    Charlton WA (1996) Lateral root initiation. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, 2nd edn. Marcel Dekker Inc., New York, pp 149–173Google Scholar
  18. 18.
    Paolillo DJ Jr, Zobel RW (2002) The formation of adventitious roots on root axes is a widespread occurrence in field-grown dicotyledonous plants. Am J Bot 89(9):1361–1372. CrossRefPubMedGoogle Scholar
  19. 19.
    Hou G, Hill JP, Blancaflor EB (2004) Developmental anatomy and auxin response of lateral root formation in Ceratopteris richardii. J Exp Bot 55(397):685–693. CrossRefPubMedGoogle Scholar
  20. 20.
    Sheng L, Hu X, Du Y, Zhang G, Huang H, Scheres B, Xu L (2017) Non-canonical WOX11-mediated root branching contributes to plasticity in Arabidopsis root system architecture. Development 144(17):3126–3133. CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Xu D, Miao J, Yumoto E, Yokota T, Asahina M, Watahiki M (2017) YUCCA9-mediated auxin biosynthesis and polar auxin transport synergistically regulate regeneration of root systems following root cutting. Plant Cell Physiol 58(10):1710–1723. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Baesso B, Chiatante D, Terzaghi M, Zenga D, Nieminen K, Mahonen AP, Siligato R, Heliariutta Y, Scippa GS, Montagnoli A (2018) PRE3 and WOX11 transcription factors are involved in the formation of new lateral roots from secondary growth taproot in A. thaliana. Plant Biol (Stuttg). CrossRefGoogle Scholar
  23. 23.
    Ge Y, Fang X, Liu W, Sheng L, Xu L (2018) Adventitious lateral rooting: the plasticity of root system architecture. Physiol Plant. PubMedCrossRefGoogle Scholar
  24. 24.
    Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. Trends Plant Sci 16(11):597–606. CrossRefPubMedGoogle Scholar
  25. 25.
    Sugimoto K, Gordon SP, Meyerowitz EM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol 21(4):212–218. CrossRefPubMedGoogle Scholar
  26. 26.
    Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25(9):3159–3173. CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Su YH, Zhang XS (2014) The hormonal control of regeneration in plants. Curr Top Dev Biol 108:35–69. CrossRefPubMedGoogle Scholar
  28. 28.
    Xu L, Huang H (2014) Genetic and epigenetic controls of plant regeneration. Curr Top Dev Biol 108:1–33. CrossRefPubMedGoogle Scholar
  29. 29.
    Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. Development 143(9):1442–1451. CrossRefPubMedGoogle Scholar
  30. 30.
    Kareem A, Radhakrishnan D, Sondhi Y, Aiyaz M, Roy MV, Sugimoto K, Prasad K (2016) De novo assembly of plant body plan: a step ahead of Deadpool. Regeneration (Oxf) 3(4):182–197. CrossRefGoogle Scholar
  31. 31.
    Lee K, Seo PJ (2018) Dynamic epigenetic changes during plant regeneration. Trends Plant Sci 23(3):235–247. CrossRefPubMedGoogle Scholar
  32. 32.
    Sang YL, Cheng ZJ, Zhang XS (2018) iPSCs: a comparison between animals and plants. Trends Plant Sci. PubMedCrossRefGoogle Scholar
  33. 33.
    Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18(3):463–471. CrossRefPubMedGoogle Scholar
  34. 34.
    Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res 22(7):1169–1180. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    He C, Chen X, Huang H, Xu L (2012) Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet 8(8):e1002911. CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26(3):1081–1093. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, Meyerowitz EM, Scheres B, Prasad K (2015) PLETHORA genes control regeneration by a two-step mechanism. Curr Biol 25(8):1017–1030. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Liu J, Hu X, Qin P, Prasad K, Hu Y, Xu L (2018) The WOX11-LBD16 pathway promotes pluripotency acquisition in callus cells during de novo shoot regeneration in tissue culture. Plant Cell Physiol 59(4):734–743. CrossRefPubMedGoogle Scholar
  39. 39.
    Kyndt T, Vieira P, Gheysen G, de Almeida-Engler J (2013) Nematode feeding sites: unique organs in plant roots. Planta 238(5):807–818. CrossRefPubMedGoogle Scholar
  40. 40.
    Olmo R, Cabrera J, Moreno-Risueno MA, Fukaki H, Fenoll C, Escobar C (2017) Molecular transducers from roots are triggered in Arabidopsis leaves by root-knot nematodes for successful feeding site formation: a conserved post-embryogenic de novo organogenesis program? Front Plant Sci 8:875. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Barthels N, van der Lee FM, Klap J, Goddijn OJ, Karimi M, Puzio P, Grundler FM, Ohl SA, Lindsey K, Robertson L, Robertson WM, Van Montagu M, Gheysen G, Sijmons PC (1997) Regulatory sequences of Arabidopsis drive reporter gene expression in nematode feeding structures. Plant Cell 9(12):2119–2134CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Koltai H, Dhandaydham M, Opperman C, Thomas J, Bird D (2001) Overlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont. Mol Plant Microbe Interact 14(10):1168–1177. CrossRefPubMedGoogle Scholar
  43. 43.
    Favery B, Complainville A, Vinardell JM, Lecomte P, Vaubert D, Mergaert P, Kondorosi A, Kondorosi E, Crespi M, Abad P (2002) The endosymbiosis-induced genes ENOD40 and CCS52a are involved in endoparasitic–nematode interactions in Medicago truncatula. Mol Plant Microbe Interact 15(10):1008–1013. CrossRefPubMedGoogle Scholar
  44. 44.
    Mathesius U (2003) Conservation and divergence of signaling pathways between roots and soil microbes-the Rhizobium-legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and matode-induced galls. Plant Soil 255:105–119CrossRefGoogle Scholar
  45. 45.
    Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148(1):358–368. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Quentin M, Abad P, Favery B (2013) Plant-parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Front Plant Sci 4:53. CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Cabrera J, Diaz-Manzano FE, Sanchez M, Rosso MN, Melillo T, Goh T, Fukaki H, Cabello S, Hofmann J, Fenoll C, Escobar C (2014) A role for LATERAL ORGAN BOUNDARIES-DOMAIN 16 during the interaction Arabidopsis-Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development. New Phytol 203(2):632–645. CrossRefPubMedGoogle Scholar
  48. 48.
    Cabrera J, Fenoll C, Escobar C (2015) Genes co-regulated with LBD16 in nematode feeding sites inferred from in silico analysis show similarities to regulatory circuits mediated by the auxin/cytokinin balance in Arabidopsis. Plant Signal Behav 10(3):e990825. CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43(5):467–478CrossRefPubMedGoogle Scholar
  50. 50.
    Shuai B, Reynaga-Pena CG, Springer PS (2002) The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol 129(2):747–761. CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Yang Y, Yu X, Wu P (2006) Comparison and evolution analysis of two rice subspecies LATERAL ORGAN BOUNDARIES domain gene family and their evolutionary characterization from Arabidopsis. Mol Phylogenet Evol 39(1):248–262. CrossRefPubMedGoogle Scholar
  52. 52.
    Majer C, Hochholdinger F (2011) Defining the boundaries: structure and function of LOB domain proteins. Trends Plant Sci 16(1):47–52. CrossRefPubMedGoogle Scholar
  53. 53.
    Coudert Y, Dievart A, Droc G, Gantet P (2013) ASL/LBD phylogeny suggests that genetic mechanisms of root initiation downstream of auxin are distinct in lycophytes and euphyllophytes. Mol Biol Evol 30(3):569–572. CrossRefPubMedGoogle Scholar
  54. 54.
    Kong Y, Xu P, Jing X, Chen L, Li L, Li X (2017) Decipher the ancestry of the plant-specific LBD gene family. BMC Genom 18(Suppl 1):951. CrossRefGoogle Scholar
  55. 55.
    Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14(7):399–408. CrossRefPubMedGoogle Scholar
  56. 56.
    Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18(8):450–458. CrossRefPubMedGoogle Scholar
  57. 57.
    Goh T, Toyokura K, Wells DM, Swarup K, Yamamoto M, Mimura T, Weijers D, Fukaki H, Laplaze L, Bennett MJ, Guyomarc’h S (2016) Quiescent center initiation in the Arabidopsis lateral root primordia is dependent on the SCARECROW transcription factor. Development 143(18):3363–3371. CrossRefPubMedGoogle Scholar
  58. 58.
    Goh T, Joi S, Mimura T, Fukaki H (2012) The establishment of asymmetry in Arabidopsis lateral root founder cells is regulated by LBD16/ASL18 and related LBD/ASL proteins. Development 139(5):883–893. CrossRefPubMedGoogle Scholar
  59. 59.
    Lee HW, Kim NY, Lee DJ, Kim J (2009) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol 151(3):1377–1389. CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Feng Z, Zhu J, Du X, Cui X (2012) Effects of three auxin-inducible LBD members on lateral root formation in Arabidopsis thaliana. Planta 236(4):1227–1237. CrossRefPubMedGoogle Scholar
  61. 61.
    Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17(2):444–463. CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29(2):153–168CrossRefPubMedGoogle Scholar
  63. 63.
    Ito J, Fukaki H, Onoda M, Li L, Li C, Tasaka M, Furutani M (2016) Auxin-dependent compositional change in mediator in ARF7- and ARF19-mediated transcription. Proc Natl Acad Sci USA 113(23):6562–6567. CrossRefPubMedGoogle Scholar
  64. 64.
    Chen X, Qu Y, Sheng L, Liu J, Huang H, Xu L (2014) A simple method suitable to study de novo root organogenesis. Front Plant Sci 5:208. CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Hu X, Xu L (2016) Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis. Plant Physiol 172(4):2363–2373. CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43(1):118–130. CrossRefPubMedGoogle Scholar
  67. 67.
    Che P, Lall S, Howell SH (2007) Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture. Planta 226(5):1183–1194. CrossRefPubMedGoogle Scholar
  68. 68.
    Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc’h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57(4):626–644. CrossRefPubMedGoogle Scholar
  69. 69.
    Yu J, Liu W, Liu J, Qin P, Xu L (2017) Auxin control of root organogenesis from callus in tissue culture. Front Plant Sci 8:1385. CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Xu C, Cao H, Zhang Q, Wang H, Xin W, Xu E, Zhang S, Yu R, Yu D, Hu Y (2018) Control of auxin-induced callus formation by bZIP59-LBD complex in Arabidopsis regeneration. Nat Plants 4(2):108–115. CrossRefPubMedGoogle Scholar
  71. 71.
    Lee K, Park OS, Seo PJ (2017) Arabidopsis ATXR2 deposits H3K36me3 at the promoters of LBD genes to facilitate cellular dedifferentiation. Sci Signal 10(507):eaan0316. CrossRefPubMedGoogle Scholar
  72. 72.
    Ikeuchi M, Shibata M, Rymen B, Iwase A, Bagman AM, Watt L, Coleman D, Favero DS, Takahashi T, Ahnert SE, Brady SM, Sugimoto K (2018) A gene regulatory network for cellular reprogramming in plant regeneration. Plant Cell Physiol. PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Lee HW, Kim MJ, Kim NY, Lee SH, Kim J (2013) LBD18 acts as a transcriptional activator that directly binds to the EXPANSIN14 promoter in promoting lateral root emergence of Arabidopsis. Plant J 73:212–224. CrossRefPubMedGoogle Scholar
  74. 74.
    Liu W, Xu L (2018) Recruitment of IC-WOX genes in root evolution. Trends Plant Sci 23(6):490–496. CrossRefPubMedGoogle Scholar
  75. 75.
    Nardmann J, Werr W (2012) The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns. Plant Mol Biol 78(1–2):123–134. CrossRefPubMedGoogle Scholar
  76. 76.
    Feng Z, Sun X, Wang G, Liu H, Zhu J (2012) LBD29 regulates the cell cycle progression in response to auxin during lateral root formation in Arabidopsis thaliana. Ann Bot 110(1):1–10. CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Porco S, Larrieu A, Du Y, Gaudinier A, Goh T, Swarup K, Swarup R, Kuempers B, Bishopp A, Lavenus J, Casimiro I, Hill K, Benkova E, Fukaki H, Brady SM, Scheres B, Peret B, Bennett MJ (2016) Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3. Development 143(18):3340–3349. CrossRefPubMedGoogle Scholar
  78. 78.
    Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17(5):1387–1396. CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Taramino G, Sauer M, Stauffer JL Jr, Multani D, Niu X, Sakai H, Hochholdinger F (2007) The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation. Plant J 50(4):649–659. CrossRefPubMedGoogle Scholar
  80. 80.
    Majer C, Xu C, Berendzen KW, Hochholdinger F (2012) Molecular interactions of ROOTLESS CONCERNING CROWN AND SEMINAL ROOTS, a LOB domain protein regulating shoot-borne root initiation in maize (Zea mays L.). Philos Trans R Soc Lond B Biol Sci 367(1595):1542–1551. CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Coudert Y, Le VA, Adam H, Bes M, Vignols F, Jouannic S, Guiderdoni E, Gantet P (2015) Identification of CROWN ROOTLESS1-regulated genes in rice reveals specific and conserved elements of post-embryonic root formation. New Phytol 206(1):243–254. CrossRefPubMedGoogle Scholar
  82. 82.
    Xu C, Tai H, Saleem M, Ludwig Y, Majer C, Berendzen KW, Nagel KA, Wojciechowski T, Meeley RB, Taramino G, Hochholdinger F (2015) Cooperative action of the paralogous maize lateral organ boundaries (LOB) domain proteins RTCS and RTCL in shoot-borne root formation. New Phytol 207(4):1123–1133. CrossRefPubMedGoogle Scholar
  83. 83.
    Berckmans B, Vassileva V, Schmid SP, Maes S, Parizot B, Naramoto S, Magyar Z, Kamei CL, Koncz C, Bogre L, Persiau G, De Jaeger G, Friml J, Simon R, Beeckman T, De Veylder L (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23(10):3671–3683. CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Kang NY, Lee HW, Kim J (2013) The AP2/EREBP gene PUCHI Co-Acts with LBD16/ASL18 and LBD18/ASL20 downstream of ARF7 and ARF19 to regulate lateral root development in Arabidopsis. Plant Cell Physiol 54(8):1326–1334. CrossRefPubMedGoogle Scholar
  85. 85.
    Lee HW, Kim J (2013) EXPANSINA17 upregulated by LBD18/ASL20 promotes lateral root formation during the auxin response. Plant Cell Physiol 54(10):1600–1611. CrossRefPubMedGoogle Scholar
  86. 86.
    Lee HW, Cho C, Kim J (2015) Lateral Organ Boundaries Domain16 and 18 act downstream of the AUXIN1 and LIKE-AUXIN3 auxin influx carriers to control lateral root development in Arabidopsis. Plant Physiol 168(4):1792–1806. CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Jeon E, Young Kang N, Cho C, Joon Seo P, Chung Suh M, Kim J (2017) LBD14/ASL17 positively regulates lateral root formation and is involved in ABA response for root architecture in Arabidopsis. Plant Cell Physiol 58(12):2190–2201. CrossRefPubMedGoogle Scholar
  88. 88.
    Lee HW, Kang NY, Pandey SK, Cho C, Lee SH, Kim J (2017) Dimerization in LBD16 and LBD18 transcription factors is critical for lateral root formation. Plant Physiol 174(1):301–311. CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Hofhuis H, Laskowski M, Du Y, Prasad K, Grigg S, Pinon V, Scheres B (2013) Phyllotaxis and rhizotaxis in Arabidopsis are modified by three PLETHORA transcription factors. Curr Biol 23(11):956–962. CrossRefPubMedGoogle Scholar
  90. 90.
    Du Y, Scheres B (2017) PLETHORA transcription factors orchestrate de novo organ patterning during Arabidopsis lateral root outgrowth. Proc Natl Acad Sci USA 114(44):11709–11714. CrossRefPubMedGoogle Scholar
  91. 91.
    Ge Y, Liu J, Zeng M, He J, Qin P, Huang H, Xu L (2016) Identification of wox family genes in Selaginella kraussiana for studies on stem cells and regeneration in lycophytes. Front Plant Sci 7:93. CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and EcologyChinese Academy of SciencesShanghaiChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Instrument Science and EngineeringShanghai Jiao Tong UniversityShanghaiChina

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