Abstract
Plants generate various tissues and organs via a strictly regulated developmental program. The plant vasculature is a complex tissue system consisting of xylem and phloem tissues with a layer of cambial cells in between. Multiple regulatory steps are involved in vascular development. Although molecular and genetic studies have uncovered a variety of key factors controlling vascular development, studies of the actual functions of these factors have been limited due to the inaccessibility of the plant vasculature. Thus, to obtain a different perspective, culture systems have been widely used to analyze the sequential processes that occur during vascular development. A tissue culture system known as VISUAL, in which molecular genetic analysis can easily be performed, was recently established in Arabidopsis thaliana. This reconstitutive approach to vascular development enables this process to be investigated quickly and easily. In this review, I summarize our recent knowledge of the regulatory mechanisms underlying vascular development and provide future perspectives on vascular analyses that can be performed using VISUAL.
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References
Aloni R (1980) Role of auxin and sucrose in the differentiation of sieve and tracheary elements in plant tissue cultures. Planta 150:255–263
Barratt DH, Kölling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM (2011) Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiol 155:328–341
Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benková E, Mähönen AP, Helariutta Y (2011a) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21:917–926
Bishopp A, Lehesranta S, Vatén A, Help H, El-Showk S, Scheres B, Helariutta K, Mähönen AP, Sakakibara H, Helariutta Y (2011b) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21:927–932
Blob B, Heo JO, Helariutta Y (2017) Phloem differentiation: an integrative model for cell specification. J Plant Res. https://doi.org/10.1007/s10265-017-0999-0
Bonke M, Thitamadee S, Mähönen AP, Hauser MT, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426:181–186
Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806
Breda AS, Hazak O, Hardtke CS (2017) Phosphosite charge rather than shootward localization determines OCTOPUS activity in root protophloem. Proc Natl Acad Sci USA 114:E5721–E5730
Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321
De Rybel B, Möller B, Yoshida S, Grabowicz I, Barbier de Reuille P, Boeren S, Smith RS, Borst JW, Weijers D (2013) A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev Cell 4:426–437
De Rybel B, Adibi M, Breda AS, Wendrich JR, Smit ME, Novák O, Yamaguchi N, Yoshida S, Van Isterdael G, Palovaara J, Nijsse B, Boekschoten MV, Hooiveld G, Beeckman T, Wagner D, Ljung K, Fleck C, Weijers D (2014) Plant development. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 345:1255215
De Rybel B, Mähönen AP, Helariutta Y, Weijers D (2016) Plant vascular development: from early specification to differentiation. Nat Rev Mol Cell Biol 17:30–40
Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS (2013) Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proc Natl Acad Sci USA 110:7074–7079
Derbyshire P, Ménard D, Green P, Saalbach G, Buschmann H, Lloyd CW, Pesquet E (2015) Proteomic analysis of microtubule interacting proteins over the course of xylem tracheary element formation in Arabidopsis. Plant Cell 27:2709–2726
Devillard C, Walter C (2014) Formation of plant tracheary elements in vitro—a review. N Z J For Sci 44:22
Etchells JP, Provost CM, Turner SR (2012) Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Genet 8:e1002997
Fisher K, Turner S (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol 17:1061–1066
Fukuda H (2016) Signaling, transcriptional regulation, and asynchronous pattern formation governing plant xylem development. Proc Jpn Acad Ser B Phys Biol Sci 92:98–107
Fukuda H, Komamine A (1980) Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol 65:57–60
Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S, Heo JO, Vatén A, Lindgren O, De Rybel B, Van Isterdael G, Somervuo P, Lichtenberger R, Rocha R, Thitamadee S, Tähtiharju S, Auvinen P, Beeckman T, Jokitalo E, Helariutta Y (2014) Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science 345:933–937
Hazak O, Brandt B, Cattaneo P, Santiago J, Rodriguez-Villalon A, Hothorn M, Hardtke CS (2017) Perception of root-active CLE peptides requires CORYNE function in the phloem vasculature. EMBO Rep 18:1367–1381
Heo JO, Blob B, Helariutta Y (2017) Differentiation of conductive cells: a matter of life and death. Curr Opin Plant Biol 35:23–29
Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci USA 105:15208–15213
Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629
Iakimova ET, Woltering EJ (2017) Xylogenesis in zinnia (Zinnia elegans) cell cultures: unravelling the regulatory steps in a complex developmental programmed cell death event. Planta 245:681–705
Ikematsu S, Tasaka M, Torii KU, Uchida N (2017) ERECTA-family receptor kinase genes redundantly prevent premature progression of secondary growth in the Arabidopsis hypocotyl. New Phytol 213:1697–1709
Kondo Y, Fukuda H (2015) The TDIF signaling network. Curr Opin Plant Biol 28:106–110
Kondo Y, Ito T, Nakagami H, Hirakawa Y, Saito M, Tamaki T, Shirasu K, Fukuda H (2014) Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF-TDR signalling. Nat Commun 5:3504
Kondo Y, Fujita T, Sugiyama M, Fukuda H (2015) A novel system for xylem cell differentiation in Arabidopsis thaliana. Mol Plant 8:612–621
Kondo Y, Nurani AM, Saito C, Ichihashi Y, Saito M, Yamazaki K, Mitsuda N, Ohme-Takagi M, Fukuda H (2016) Vascular cell induction culture system using Arabidopsis leaves (VISUAL) reveals the sequential differentiation of sieve element-like cells. Plant Cell 28:1250–1262
Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860
Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Václavíková K, Miyawaki K, Kakimoto T (2008) Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci USA 105:20027–20031
Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Tähtiharju S, Elo A, Decourteix M, Ljung K, Bhalerao R, Keinonen K, Albert VA, Helariutta Y (2008) Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA 105:20032–20037
Oda Y, Fukuda H (2012) Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science 337:1333–1336
Oda Y, Mimura T, Hasezawa S (2005) Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 137:1027–1036
Oda Y, Iida Y, Kondo Y, Fukuda H (2010) Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr Biol 20:1197–1202
Ohashi-Ito K, Oda Y, Fukuda H (2010) Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22:3461–3473
Ohashi-Ito K, Oguchi M, Kojima M, Sakakibara H, Fukuda H (2013) Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY. Development 140:765–769
Ohashi-Ito K, Saegusa M, Iwamoto K, Oda Y, Katayama H, Kojima M, Sakakibara H, Fukuda H (2014) A bHLH complex activates vascular cell division via cytokinin action in root apical meristem. Curr Biol 24:2053–2058
Pesquet E, Korolev AV, Calder G, Lloyd CW (2010) The microtubule-associated protein AtMAP70–5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 20:744–749
Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS (2011) Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23:1322–1336
Saito M, Nurani AM, Kondo Y, Fukuda H (2017) Tissue culture for xylem differentiation with Arabidopsis leaves. Methods Mol Biol 1544:59–65
Sawa S, Demura T, Horiguchi G, Kubo M, Fukuda H (2005) The ATE genes are responsible for repression of transdifferentiation into xylem cells in Arabidopsis. Plant Physiol 137:141–148
Truernit E, Bauby H, Belcram K, Barthélémy J, Palauqui JC (2012) OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139:1306–1315
Uchida N, Tasaka M (2013) Regulation of plant vascular stem cells by endodermis-derived EPFL-family peptide hormones and phloem-expressed ERECTA-family receptor kinases. J Exp Bot 64:5335–5343
Wallner ES, López-Salmerón V, Belevich I, Poschet G, Jung I, Grünwald K, Sevilem I, Jokitalo E, Hell R, Helariutta Y, Agustí J, Lebovka I, Greb T (2017) Strigolactone- and karrikin-independent SMXL proteins are central regulators of phloem formation. Curr Biol 27:1241–1247
Wu YY, Hou BH, Lee WC, Lu SH, Yang CJ, Vaucheret H, Chen HM (2017) DCL2- and RDR6-dependent transitive silencing of SMXL4 and SMXL5 in Arabidopsis dcl4 mutants causes defective phloem transport and carbohydrate over-accumulation. Plant J 90:1064–1078
Yamaguchi M, Goué N, Igarashi H, Ohtani M, Nakano Y, Mortimer JC, Nishikubo N, Kubo M, Katayama Y, Kakegawa K, Dupree P, Demura T (2010) VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 153:906–914
Acknowledgements
This work was supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (17H06476 to YK), and from the Japan Society for the Promotion of Science (17H05008 to YK).
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Kondo, Y. Reconstitutive approach for investigating plant vascular development. J Plant Res 131, 23–29 (2018). https://doi.org/10.1007/s10265-017-0998-1
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DOI: https://doi.org/10.1007/s10265-017-0998-1