doi: 10.15389/agrobiology.2017.5.856eng

UDC 631.522/.524:581.1:581.144.2

Supported financially by Russian Science Foundation (grant № 16-16-00089).
Study of the role of auxin in lateral root initiation in Cucurbitaceae was supported by Russian Foundation for Basic Research (grant № 14-04-01413-a)


BRANCHING (review)

E.L. Ilina1, A.S. Kiryushkin1, V.E. Tsyganov2, К. Pawlowski3,
K.N. Demchenko1, 2

1V.L. Komarov Botanical Institute RAS, Federal Agency of Scientific Organizations, 2, ul. Professora Popova, St. Petersburg, 197376 Russia,
e-mail (corresponding author);
2All-Russian Research Institute for Agricultural Microbiology, Federal Agency of Scientific Organizations, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia,
3Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden

Ilina E.L.
Tsyganov V.E.
Pawlowski K.
Demchenko K.N.

Received November 15, 2016

The most important function of any plant root system is the supply of mineral nutrients. The soil is a heterogeneous environment characterized by irregular distribution of nutrients. The branching of the main root which leads to the formation of the root system is regulated by the necessity of compensation for this unpredictable environment. Different types of root systems may reflect different strategies of adaptation of vascular plants to land (L. Kutschera et al., 1997). In recent years, a vast array of experimental data on this subject has been collected. Investigations were carried out on the model plant Arabidopsis thaliana (J.G. Dubrovsky et al., 2001; B. Parizot et al., 2012; J.G. Dubrovsky et al., 2017) as well as on a wide range of crops (cereals, crucifers, gourds, buckwheat etc.). The accumulated data allow the identification of economically important traits of root systems that can be exploited to design breeding strategies to optimize root system function. This review contains an analysis of the current data on cellular, molecular genetic and physiological mechanisms of lateral root initiation and development. The phytohormone auxin performs multiple functions during lateral root initiation (Y. Du et al., 2017). It participates in the earliest stages by determining of competence for the first division by pericycle cells that leads to primordium formation. Furthermore, auxin facilitates the emergence of the primordium from the parental root cortex. Recent studies have shown that the formation of the lateral root begins with the oscillation of auxin concentrations in the basal part of the parental root meristem and the formation of an auxin response maximum in some cells of central cylinder (I. De Smet et al., 2007; K.H. ten Tusscher et al., 2017). The next stage is the specification of founder cells in the pericycle and the subsequent formation of the prebranch site (M.A. Moreno-Risueno et al., 2010). Questions ranging from the mechanisms that determine which pericycle cells can become founder cells for lateral root primordia, the mechanisms of regulation of cell proliferation, the positioning of lateral roots along the axis of the parental root, and hormonal factors and their targets, all leading to the successive development of lateral roots, are discussed in this review. Data on the role of auxin in this process and on the mechanisms of auxin signal transduction in the course of lateral root initiation are provided. The key factors involved in the determination of the competence of pericycle cells to initiate lateral root primordia are the transcription factor GATA23 (B. De Rybel et al., 2010) and the membrane-associated kinase regulator MAKR4 (W. Xuan et al., 2015). Special attention is paid to the role of neighboring cell layers in the control of the initial stages of cell proliferation in the pericycle that result in the formation of a new organ. However, there are a number of families among flowering plants in which the initiation and development of lateral root primordia occurs directly in the parental root meristem (J.G. Dubrovsky, 1986, 1987; K.N. Demchenko et al., 2001; E.L. Ilina et al., 2012). For the first time, data on the key role of auxin in lateral root primordia initiation in these species, in particular in Cucurbitaceae, are presented in this review, and the mechanisms that open the opportunity for early and rapid branching of the main root are discussed. Special attention is paid to evolutionary mechanisms of branching site determination in flowering plants.

Keywords: auxin, cell proliferation, lateral root initiation, meristem, root branching, root development, transcriptional factors.


Full article (Rus)

Full text (Eng)



  1. Kell D.B. Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Ann. Bot., 2011, 108(3): 407-418 CrossRef
  2. Hufnagel B., de Sousa S.M., Assis L., Guimaraes C.T., Leiser W., Azevedo G.C., Negri B., Larson B.G., Shaff J.E., Pastina M.M., Barros B.A., Weltzien E., Rattunde H.F.W., Viana J.H., Clark R.T., Falcão A., Gazaffi R., Garcia A.A.F., Schaffert R.E., Kochian L.V., Magalhaes J.V. Duplicate and conquer: Multiple homologs of PHOSPHORUS-STARVATION TOLERANCE1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils. Plant Physiol., 2014, 166(2): 659-677 CrossRef
  3. Narayanan S., Mohan A., Gill K.S., Prasad P.V.V. Variability of root traits in spring wheat germplasm. PLoS ONE, 2014, 9(6): e100317 CrossRef
  4. Uga Y., Sugimoto K., Ogawa S., Rane J., Ishitani M., Hara N., Kitomi Y., Inukai Y., Ono K., Kanno N., Inoue H., Takehisa H., Motoyama R., Nagamura Y., Wu J., Matsumoto T., Takai T., Okuno K., Yano M. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet., 2013, 45(9): 1097-1102 CrossRef
  5. Meister R., Rajani M.S., Ruzicka D., Schachtman D.P. Challenges of modifying root traits in crops for agriculture. Trends Plant Sci., 2014, 19(12): 779-788 CrossRef
  6. Bao Y., Aggarwal P., Robbins N.E., Sturrock C.J., Thompson M.C., Tan H.Q., Tham C., Duan L., Rodriguez P.L., Vernoux T., Mooney S.J., Bennett M.J., Dinneny J.R. Plant roots use a patterning mechanism to position lateral root branches toward available water. PNAS, 2014, 111(25): 9319-9324 CrossRef
  7. Tikhonovich I.A., Provorov N.A. Microbiology is the basis of sustainable agriculture: an opinion. Ann. Appl. Biol., 2011, 159(2): 155-168 CrossRef
  8. Pawlowski K., Demchenko K.N. The diversity of actinorhizal symbiosis. Protoplasma, 2012, 249(4): 967-979 CrossRef
  9. Kano M., Inukai Y., Kitano H., Yamauchi A. Root plasticity as the key root trait for adaptation to various intensities of drought stress in rice. Plant Soil, 2011, 342(1-2): 117-128 CrossRef
  10. Grossman J.D., Rice K.J. Evolution of root plasticity responses to variation in soil nutrient distribution and concentration. Evolutionary Applications, 2012, 5(8): 850-857 CrossRef
  11. Lynch J. Root architecture and plant productivity. Plant Physiol., 1995, 109(1): 7-13 CrossRef
  12. Zhu J., Kaeppler S., Lynch J. Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil, 2005, 270(1): 299-310 CrossRef
  13. Kamoshita A., Zhang J., Siopongco J., Sarkarung S., Nguyen H.T., Wade L.J. Ef-fects of phenotyping environment on identification of quantitative trait loci for rice root morphology under anaerobic conditions. Crop Sci., 2002, 42(1): 255-265 CrossRef
  14. Malamy J.E., Benfey P.N. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development, 1997, 124(1): 33-44.
  15. Yadav S.R., Bishopp A., Helariutta Y. Plant development: early events in lateral root initiation. Current Biology, 2010, 20(19): R843-R845 CrossRef
  16. Dolan L., Janmaat K., Willemsen V., Linstead P., Poethig S., Roberts K., Scheres B. Cellular organisation of the Arabidopsis thaliana root. Development, 1993, 119(1): 71-84.
  17. Ivanov V.B. Kletochnye osnovy rosta rastenii [Cellular aspects of plant growth]. Moscow, 1974 (in Russ.).
  18. Demchenko N.P. Tsitologiya, 1984, 26(4): 382-391 (in Russ.).
  19. Parizot B., Laplaze L., Ricaud L., Boucheron-Dubuisson E., Bayle V., Bonke M., De Smet I., Poethig S.R., Helariutta Y., Haseloff J., Chriqui D., Beeckman T., Nussaume L. Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol., 2008, 146(1): 140-148 CrossRef
  20. Peret B., Larrieu A., Bennett M.J. Lateral root emergence: a difficult birth. J. Exp. Bot., 2009, 60(13): 3637-3643 CrossRef
  21. Casimiro I., Marchant A., Bhalerao R.P., Beeckman T., Dhooge S., Swarup R., Graham N., Inze D., Sandberg G., Casero P.J., Bennett M. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell, 2001, 13(4): 843-852 CrossRef
  22. Beemster G.T.S., Fiorani F., Inze D. Cell cycle: the key to plant growth control? Trends Plant Sci., 2003, 8(4): 154-158 CrossRef
  23. De Smet I., Tetsumura T., De Rybel B., Frey N.F.d., Laplaze L., Casimiro I., Swarup R., Naudts M., Vanneste S., Audenaert D., Inze D., Bennett M.J., Beeckman T. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development, 2007, 134(4): 681-690 CrossRef
  24. ten Tusscher K.H., Laskowski M. Periodic lateral root priming, what makes it tick. The Plant Cell, 2017 CrossRef
  25. Overvoorde P., Fukaki H., Beeckman T. Auxin control of root development. Cold Spring Harbor Perspectives in Biology, 2010, 2(6): 2:a001537 CrossRef
  26. Parizot B., Beeckman T. Genomics of root development. In: Root genomics and soil interactions. M. Crespi (ed.). Blackwell Publishing Ltd., Oxford, UK, 2012: 3-28 CrossRef
  27. Dubrovsky J.G., Sauer M., Napsucialy-Mendivil S., Ivanchenko M.G., Friml J., Shishkova S., Celenza J., Benkova E. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. PNAS, 2008, 105(25): 8790-8794 CrossRef
  28. Du Y., Scheres B. Lateral root formation and the multiple roles of auxin. Journal of Experimental Botany, 2017 CrossRef
  29. Tiwari S.B., Wang X.-J., Hagen G., Guilfoyle T.J. AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. The Plant Cell, 2001, 13(12): 2809-2822 CrossRef
  30. Dharmasiri N., Dharmasiri S., Estelle M. The F-box protein TIR1 is an auxin receptor. Nature, 2005, 435(7041): 441-445 CrossRef
  31. Mockaitis K., Estelle M. Auxin receptors and plant development: A new signaling para-digm. Ann. Rev. Cell Dev. Biol., 2008, 24(1): 55-80 CrossRef
  32. Hamann T., Benkova E., Baurle I., Kientz M., Jurgens G. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes and Development, 2002, 16: 1610-1615 CrossRef
  33. Moreno-Risueno M.A., Van Norman J.M., Moreno A., Zhang J., Ahnert S.E., Benfey P.N. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science, 2010, 329(5997): 1306-1311 CrossRef
  34. Rogg L.E., Lasswell J., Bartel B. A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell, 2001, 13(3): 465-480 CrossRef
  35. Brady S.M., Orlando D.A., Lee J.-Y., Wang J.Y., Koch J., Dinneny J.R., Ma-
    ce D., Ohler U., Benfey P.N. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science, 2007, 318(5851): 801-806 CrossRef
  36. De Rybel B., Vassileva V., Parizot B., Demeulenaere M., Grunewald W., Audenaert D., Van Campenhout J., Overvoorde P., Jansen L., Vanneste S., Möller B., Wilson M., Holman T., Van Isterdael G., Brunoud G., Vuylste-
    ke M., Vernoux T., De Veylder L., Inzé D., Weijers D., Bennett M.J., Be-
    eckman T. A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol., 2010, 20(19): 1697-1706 CrossRef
  37. Behringer C., Bastakis E., Ranftl Q.L., Mayer K.F.X., Schwechheimer C. Functional diversification within the family of B-GATA transcription factors through the leucine-leucine-methionine domain. Plant Physiol., 2014, 166(1): 293-305 CrossRef
  38. Schwechheimer C., Behringer C. B-GATA transcription factors — insights into their structure, regulation and role in plant development. Front. Plant Sci., 2015, 6 CrossRef
  39. Parizot B., De Rybel B., Beeckman T. VisuaLRTC: a new view on lateral root initiation by combining specific transcriptome datasets. Plant Physiol., 2010, 153(1): 34-40 CrossRef
  40. De Rybel B., Audenaert D., Xuan W., Overvoorde P., Strader L.C., Kepinski S., Hoye R., Brisbois R., Parizot B., Vanneste S., Liu X., Gilday A., Graham I.A., Nguyen L., Jansen L., Njo M.F., Inzé D., Bartel B., Beeckman T. A role for the root cap in root branching revealed by the non-auxin probe naxillin. Nat. Chem. Biol., 2012, 8(9): 798-805 CrossRef
  41. Xuan W., Audenaert D., Parizot B., Möller B.K., Njo Maria F., De Rybel B., De Rop G., Van Isterdael G., Mähönen Ari P., Vanneste S., Beeckman T. Root cap-derived auxin pre-patterns the longitudinal axis of the Arabidopsis root. Curr. Biol., 2015, 25(10): 1381-1388 CrossRef
  42. Van Norman J.M., Xuan W., Beeckman T., Benfey P.N. To branch or not to branch: the role of pre-patterning in lateral root formation. Development, 2013, 140(21): 4301-4310 CrossRef
  43. Gibbs D.J., Voß U., Harding S.A., Fannon J., Moody L.A., Yamada E., Swarup K., Nibau C., Bassel G.W., Choudhary A., Lavenus J., Bradshaw S.J., Stekel D.J., Bennett M.J., Coates J.C. AtMYB93 is a novel negative regulator of lateral root development in Arabidopsis. New Phytologist, 2014, 203(4): 1194-1207 CrossRef
  44. Möller B.K., Xuan W., Beeckman T. Dynamic control of lateral root positioning. Curr. Opin. Plant Biol., 2017, 35: 1-7 CrossRef
  45. Beeckman T., Burssens S., Inze D. The peri-cell-cycle in Arabidopsis. J. Exp. Bot., 2001, 52(Roots Special Issue): 403-411 CrossRef
  46. Himanen K., Boucheron E., Vanneste S., de Almeida Engler J., Inze D., Beeckman T. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell, 2002, 14(10): 2339-2351 CrossRef
  47. DiDonato R.J., Arbuckle E., Buker S., Sheets J., Tobar J., Totong R., Grisafi P., Fink G.R., Celenza J.L. Arabidopsis ALF4 encodes a nuclear-localized protein required for lateral root formation. Plant J., 2004, 37(3): 340-353 CrossRef
  48. Vanneste S., De Rybel B., Beemster G.T.S., Ljung K., De Smet I., Van Isterdael G., Naudts M., Iida R., Gruissem W., Tasaka M., Inze D., Fukaki H., Beeckman T. Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell, 2005, 17(11): 3035-3050 CrossRef
  49. De Smet I., Lau S., Voß U., Vanneste S., Benjamins R., Rademacher E.H., Schlereth A., De Rybel B., Vassileva V., Grunewald W., Naudts M., Levesque M.P., Ehrismann J.S., Inzé D., Luschnig C., Benfey P.N., Weijers D., Van Montagu M.C.E., Bennett M.J., Jürgens G., Beeckman T. Bimodular auxin response controls organogenesis in Arabidopsis. PNAS, 2010, 107(6): 2705-2710 CrossRef
  50. Sanz L., Dewitte W., Forzani C., Patell F., Nieuwland J., Wen B., Quelhas P., De Jager S., Titmus C., Campilho A., Ren H., Estelle M., Wang H., Mur-
    ray J.A.H. The Arabidopsis D-type cyclin CYCD2;1 and the inhibitor ICK2/KRP2 modulate auxin-induced lateral root formation. Plant Cell, 2011, 23: 1-20 CrossRef
  51. Demchenko N.P., Demchenko K.N. Resumption of DNA synthesis and cell division in wheat roots as related to lateral root initiation. Russian Journal of Plant Physiology, 2001, 48(6): 755-763 CrossRef
  52. Vanneste S., Maes L., De Smet I., Himanen K., Naudts M., Inzé D., Beeckman T. Auxin regulation of cell cycle and its role during lateral root initiation. Physiologia Plantarum, 2005, 123(2): 139-146 CrossRef
  53. Alarcón M.V., Lloret P.G., Martín-Partido G., Salguero J. The initiation of lateral roots in the primary roots of maize (Zea mays L.) implies a reactivation of cell proliferation in a group of founder pericycle cells. J. Plant Physiol., 2016, 192: 105-110 CrossRef
  54. Sugimoto K., Jiao Y., Meyerowitz E.M. Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell, 2010, 18(3): 463-471 CrossRef
  55. Casimiro I., Beeckman T., Graham N., Bhalerao R., Zhang H., Casero P., Sandberg G., Bennett M.J. Dissecting Arabidopsis lateral root development. Trends Plant Sci., 2003, 8(4): 165-171 CrossRef
  56. Jurado S., Abraham Z., Manzano C., López-Torrejón G., Pacios L.F., Del Pozo J.C. The Arabidopsis cell cycle F-box protein SKP2A binds to auxin. Plant Cell, 2010, 22(12): 3891-3904 CrossRef
  57. Berckmans B., Vassileva V., Schmid S.P.C., Maes S., Parizot B., Naramoto S., Magyar Z., Kamei C.L.A., Koncz C., Bogre L., Persiau G., De Jaeger G., Friml J., Simon R., Beeckman T., De Veylder L. Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell, 2011, 23(10): 3671-3683 CrossRef
  58. Nieuwland J., Maughan S., Dewitte W., Scofield S., Sanz L., Murray J.A.H. The D-type cyclin CYCD4;1 modulates lateral root density in Arabidopsis by affecting the basal meristem region. PNAS, 2009, 106(52): 22528-22533 CrossRef
  59. De Veylder L., Beeckman T., Inze D. The ins and outs of the plant cell cycle. Nat. Rev. Mol. Cell Biol., 2007, 8(8): 655-665 CrossRef
  60. Marhavý P., Vanstraelen M., De Rybel B., Zhaojun D., Bennett M.J., Beeckman T., Benkova E. Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO Journal, 2013, 32(1): 149-158 CrossRef
  61. Swarup K., Benkova E., Swarup R., Casimiro I., Peret B., Yang Y., Parry G., Nielsen E., De Smet I., Vanneste S., Levesque M.P., Carrier D., James N., Calvo V., Ljung K., Kramer E., Roberts R., Graham N., Marillonnet S., Patel K., Jones J.D.G., Taylor C.G., Schachtman D.P., May S., Sandberg G., Benfey P., Friml J., Kerr I., Beeckman T., Laplaze L., Bennett M.J. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol., 2008, 10(8): 946-954 CrossRef
  62. Lucas M., Kenobi K., von Wangenheim D., Voβ U., Swarup K., De Smet I., Van Damme D., Lawrence T., Péret B., Moscardi E., Barbeau D., Godin C., Salt D., Guyomarc’h S., Stelzer E.H.K., Maizel A., Laplaze L., Bennett M.J. Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. PNAS, 2013, 110(13): 5229-5234 CrossRef
  63. Marhavý P., Montesinos J.C., Abuzeineh A., Van Damme D., Vermeer J.E.M., Duclercq J., Rakusová H., Nováková P., Friml J., Geldner N., Benková E. Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation. Genes & Development, 2016, 30(4): 471-483 CrossRef
  64. Vermeer J.E.M., von Wangenheim D., Barberon M., Lee Y., Stelzer E.H.K., Maizel A., Geldner N. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science, 2014, 343(6167): 178-183 CrossRef
  65. Blakely L.M., Durham M., Evans T.A., Blakely R.M. Experimental studies on lateral root formation in radish seedling roots. I. General methods, developmental stages, and spontaneous formation of laterals. Botanical Gazette, 1982, 143(3): 341-352.
  66. Laskowski M.J., Williams M.E., Nusbaum H.C., Sussex I.M. Formation of lateral root meristems is a two-stage process. Development, 1995, 121(10): 3303-3310.
  67. Zhao Y., Christensen S.K., Fankhauser C., Cashman J.R., Cohen J.D., Weigel D., Chory J. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science, 2001, 291(5502): 306-309 CrossRef
  68. Cheng Y., Dai X., Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes & Development, 2006, 20(13): 1790-1799 CrossRef
  69. De Smet I., Vassileva V., De Rybel B., Levesque M.P., Grunewald W., Van Damme D., Van Noorden G., Naudts M., Van Isterdael G., De Clercq R., Wang J.Y., Meuli N., Vanneste S., Friml J., Hilson P., Jurgens G., Ingram G.C., Inze D., Benfey P.N., Beeckman T. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science, 2008, 322(5901): 594-597 CrossRef
  70. Fernández-Marcos M., Desvoyes B., Manzano C., Liberman L.M., Ben-
    fey P.N., del Pozo J.C., Gutierrez C. Control of Arabidopsis lateral root primordium boundaries by MYB36. New Phytologist, 2016, 213(1): 105-112 CrossRef
  71. Gulyaev V.A. Botanicheskii zhurnal, 1964, 49(10): 1482-1485 (in Russ.).
  72. Dubrovskii I.G. Botanicheskii zhurnal, 1987, 72(2): 171-176 (in Russ.).
  73. Demchenko K.N., Demchenko N.P. Changes of root structure in connection with the development of lateral root primordia in wheat and pumpkins. In: Recent advances of plant root structure and function. Developments in plant and soil sciences. V. 90. O. Gašparíková, M. Ciamporová, I. Mistrík, F. Baluška (eds.). Springer, Dordrecht, 2001: 39-47 CrossRef
  74. Dubrovskii I.G. Ontogenez, 1986, 17(2): 176-189 (in Russ.).
  75. Mallory T.E., Chiang S.-H., Cutter E.G., Gifford E.M. Sequence and pattern of root formation in five selected species. Am. J. Bot., 1970, 57(7): 800-809.
  76. O'Dell D.H., Foard D.E. Presence of lateral root primordia in the radicle of buckwheat embryos. Bulletin of the Torrey Botanical Club, 1969, 96(1): 1-3 CrossRef
  77. Seago J.L. Developmental anatomy in roots of Ipomoea purpurea. 2. Initiation and development of secondary roots. Am. J. Bot., 1973, 60(7): 607-618.
  78. Charlton W.A. Distribution of lateral roots and sequence of lateral initiation in Potenderia cordata L. Botanical Gazette, 1975, 136(3): 225-235.
  79. Clowes F.A.L. Origin of epidermis and development of root primordia in Pistia, Hydrocharis and Eichhornia. Annals of Botany, 1985, 55(6): 849-857.
  80. Dubrovsky J.G., Laskowski M. Lateral root initiation. In: Encyclopedia of applied plant sciences (Second edition). B. Tomas, B.G. Murray, D.G. Murphy (eds.). Academic Press, Oxford, 2017: 256-264 CrossRef
  81. Ilina E.L., Logachov A.A., Laplaze L., Demchenko N.P., Pawlowski K., Demchenko K.N. Composite Cucurbita pepo plants with transgenic roots as a tool to study root development. Annals of Botany, 2012, 110(2): 479-489 CrossRef