Dynamics of MONOPTEROS and PIN‐FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana
Abstract
Summary: Genetic evidence links the Arabidopsis MONOPTEROS (MP) and PIN‐FORMED1 (PIN1) genes to the patterning of leaf veins. To elucidate their potential functions and interactions in this process, we have assessed the dynamics of MP and PIN1 expression during vascular patterning in Arabidopsis leaf primordia. Both genes undergo a dynamic process of gradual refinement of expression into files one to two cells wide before overt vascular differentiation. The subcellular distribution of PIN1 is also gradually refined from a non‐polar distribution in isodiametric cells to strongly polarized in elongated procambial cells and provides an indication of overall directions of auxin flow. We found evidence that MP expression can be activated by auxin exposure and that PIN1 as well as DR5::GUS expression is defective in mp mutant leaves. Taken together the results suggest a feedback regulatory loop that involves auxin, MP and PIN1 and provide novel experimental support for the canalization‐of‐auxin‐flow hypothesis.
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Expression of PIN proteins precedes vascular development.
“the expression of PIN proteins precedes vascular development (Sauer et al., 2006; Scarpella et al., 2006; Wenzel et al., 2007)”
From Shaping plant architecture (2015) · cites this paper as Wenzel et al., 2007
Cites
Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation
Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., & Friml, J. (2003) · Cell · doi:10.1016/s0092-8674(03)00924-3 · Cited by 2,637 · see citing works
Ulmasov, T., Murfett, J., Hagen, G., & Guilfoyle, T. J. (1997) · The Plant Cell · doi:10.1105/tpc.9.11.1963 · Cited by 2,044 · see citing works
The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots
Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I. A., Friml, J., Heidstra, R., Aida, M., Palme, K. J., & Scheres, B. (2005) · Nature · doi:10.1038/nature03184 · Cited by 2,023 · see citing works
Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis
Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., & Jürgens, G. (2003) · Nature · doi:10.1038/nature02085 · Cited by 1,896 · see citing works
Regulation of Polar Auxin Transport by AtPIN1 in <i>Arabidopsis</i> Vascular Tissue
Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A., & Palme, K. (1998) · Science · doi:10.1126/science.282.5397.2226 · Cited by 1,530 · see citing works
Regulation of phyllotaxis by polar auxin transport
Reinhardt, D., Pesce, E.-R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., & Kuhlemeier, C. (2003) · Nature · doi:10.1038/nature02081 · Cited by 1,523 · see citing works
Hardtke, C. S., & Berleth, T. (1998) · The EMBO Journal · doi:10.1093/emboj/17.5.1405 · Cited by 1,064 · see citing works
Arabidopsis AUX1 Gene: A Permease-Like Regulator of Root Gravitropism
Bennett, M. J., Marchant, A., Green, H. G., May, S. T., Ward, S. P., Millner, P. A., Walker, A. R., Schulz, B., & Feldmann, K. A. (1996) · Science · doi:10.1126/science.273.5277.948 · Cited by 1,043 · see citing works
PIN Proteins Perform a Rate-Limiting Function in Cellular Auxin Efflux
Petrášek, J., Mravec, J., Bouchard, R., Blakeslee, J. J., Abas, M., Seifertová, D., Wiśniewska, J., Tadele, Z., Kubeš, M., Čovanová, M., et al. (2006) · Science · doi:10.1126/science.1123542 · Cited by 922 · see citing works
Polar PIN Localization Directs Auxin Flow in Plants
Wiśniewska, J., Xu, J., Seifertová, D., Brewer, P. B., Růžička, K., Blilou, I., Rouquié, D., Benková, E., Scheres, B., & Friml, J. (2006) · Science · doi:10.1126/science.1121356 · Cited by 883 · see citing works
Control of leaf vascular patterning by polar auxin transport
Scarpella, E., Marcos, D., Friml, J., & Berleth, T. (2006) · Genes & Development · doi:10.1101/gad.1402406 · Cited by 799 · see citing works
A PINOID-Dependent Binary Switch in Apical-Basal PIN Polar Targeting Directs Auxin Efflux
Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O., Benjamins, R., Ouwerkerk, P. B. F., Ljung, K., Sandberg, G., et al. (2004) · Science · doi:10.1126/science.1100618 · Cited by 789 · see citing works
Auxin inhibits endocytosis and promotes its own efflux from cells
Paciorek, T., Zažímalová, E., Ruthardt, N., Petrášek, J., Stierhof, Y.-D., Kleine-Vehn, J., Morris, D. A., Emans, N., Jürgens, G., Geldner, N., et al. (2005) · Nature · doi:10.1038/nature03633 · Cited by 772 · see citing works
Coordinated Polar Localization of Auxin Efflux Carrier PIN1 by GNOM ARF GEF
Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C. L., Paris, S., Gälweiler, L., Palme, K. J., & Jürgens, G. (1999) · Science · doi:10.1126/science.286.5438.316 · Cited by 761 · see citing works
Auxin transport — shaping the plant
Friml, J. (2003) · Current Opinion in Plant Biology · doi:10.1016/s1369526602000031 · Cited by 746 · see citing works
Growth and development of the axr1 mutants of Arabidopsis.
Lincoln, C., Britton, J. H., & Estelle, M. (1990) · The Plant Cell · doi:10.1105/tpc.2.11.1071 · Cited by 688 · see citing works
Biological pattern formation: from basic mechanisms to complex structures
Koch, A.-J., & Meinhardt, H. (1994) · Reviews of Modern Physics · doi:10.1103/revmodphys.66.1481 · Cited by 664 · see citing works
The Control of the Patterned Differentiation of Vascular Tissues
Sachs, T. (1981) · Advances in Botanical Research · doi:10.1016/s0065-2296(08)60351-1 · Cited by 656 · see citing works
Vieten, A., Vanneste, S., Wiśniewska, J., Benková, E., Benjamins, R., Beeckman, T., Luschnig, C., & Friml, J. (2005) · Development · doi:10.1242/dev.02027 · Cited by 636 · see citing works
Dimerization and DNA binding of auxin response factors
Ulmasov, T., Hagen, G., & Guilfoyle, T. J. (1999) · The Plant Journal · doi:10.1046/j.1365-313x.1999.00538.x · Cited by 586 · see citing works
Noh, B., Murphy, A. S., & Spalding, E. P. (2001) · The Plant Cell · doi:10.1105/tpc.010350 · Cited by 560 · see citing works
Auxin as a positional signal in pattern formation in plants.
Uggla, C., Möritz, T., Sandberg, G., & Sundberg, B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.17.9282 · Cited by 510 · see citing works
Przemeck, G. K. H., Mattsson, J., Hardtke, C. S., Sung, Z. R., & Berleth, T. (1996) · Planta · doi:10.1007/bf00208313 · Cited by 502 · see citing works
Self-citationResponses of plant vascular systems to auxin transport inhibition
Mattsson, J., Sung, Z. R., & Berleth, T. (1999) · Development · doi:10.1242/dev.126.13.2979 · Cited by 471 · see citing works
Self-citationAuxin Signaling in Arabidopsis Leaf Vascular Development
Mattsson, J., Ckurshumova, W., & Berleth, T. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.013623 · Cited by 445 · see citing works
Self-citationA Molecular Framework for Plant Regeneration
Xu, J., Hofhuis, H. F., Heidstra, R., Sauer, M., Friml, J., & Scheres, B. (2006) · Science · doi:10.1126/science.1121790 · Cited by 391 · see citing works
Hamann, T., Mayer, U., & Jürgens, G. (1999) · Development · doi:10.1242/dev.126.7.1387 · Cited by 386 · see citing works
Noh, B. (2001) · The Plant Cell · doi:10.1105/tpc.13.11.2441 · Cited by 366 · see citing works
Auxin Is Required for Leaf Vein Pattern in Arabidopsis
Sieburth, L. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.121.4.1179 · Cited by 293 · see citing works
Hobbie, L. J., McGovern, M., Hurwitz, L. R., Pierro, A., Liu, N. Y., Bandyopadhyay, A., & Estelle, M. A. (2000) · Development · doi:10.1242/dev.127.1.23 · Cited by 239 · see citing works
M OLECULAR G ENETICS OF A UXIN S IGNALING
Leyser, O. (2002) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.53.100301.135227 · Cited by 223 · see citing works
Murphy, A. S., Hoogner, K. R., Peer, W. A., & Taiz, L. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.010519 · Cited by 210 · see citing works
Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis
Rolland‐Lagan, A., & Prusinkiewicz, P. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02581.x · Cited by 198 · see citing works
Koizumi, K., Sugiyama, M., & Fukuda, H. (2000) · Development · doi:10.1242/dev.127.15.3197 · Cited by 188 · see citing works
The Induction of Vascular Tissues by Auxin and Cytokinin
Aloni, R. (1995) · Springer eBooks · doi:10.1007/978-94-011-0473-9_25 · Cited by 186 · see citing works
The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins
Boutté, Y., Crosnier, M., Carraro, N., Traas, J. A., & Satiat‐Jeunemaître, B. (2006) · Journal of Cell Science · doi:10.1242/jcs.02847 · Cited by 150 · see citing works
Auxin Distribution and Plant Pattern Formation: How Many Angels Can Dance on the Point of PIN?
Leyser, O. (2005) · Cell · doi:10.1016/j.cell.2005.06.005 · Cited by 129 · see citing works
Kang, J., & Dengler, N. G. (2002) · Planta · doi:10.1007/s00425-002-0847-9 · Cited by 123 · see citing works
The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo
Treml, B. S., Winderl, S., Radykewicz, R., Herz, M., Schweizer, G., Hutzler, P., Glawischnig, E., & Ruiz, R. A. T. (2005) · Development · doi:10.1242/dev.01969 · Cited by 117 · see citing works
Apical–basal polarity: why plant cells don't standon their heads
Friml, J., Benfey, P. N., Benková, E., Bennett, M. J., Berleth, T., Geldner, N., Grebe, M., Heisler, M. G., Hejátko, J., Jürgens, G., et al. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2005.11.010 · Cited by 34 · see citing works
Zachgo, S., Jacquemot-Perbal, M.-C., Saedler, H., & Schwarz‐Sommer, Z. (2000) · The Plant Journal · doi:10.1046/j.1365-313x.2000.00826.x · Cited by 28 · see citing works
Flagged first, then by citations
2 of the 43 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Guilfoyle, T. J., & Hagen, G. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.08.014 · Cited by 1,257 · see citing works
The Plant Vascular System: Evolution, Development and Functions F
Lucas, W. J., Groover, A. T., Lichtenberger, R., Furuta, K. M., Yadav, S. R., Helariutta, Y., He, X., Fukuda, H., Kang, J., Brady, S. M., et al. (2013) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12041 · Cited by 769 · see citing works
Auxin Receptors and Plant Development: A New Signaling Paradigm
Mockaitis, K., & Estelle, M. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123214 · Cited by 651 · see citing works
In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning
Greco, M., Chiappetta, A. A. C., Bruno, L., & Bitonti, M. B. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err313 · Cited by 533 · see citing works
Transcriptional Responses to the Auxin Hormone
Weijers, D., & Wagner, D. (2016) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-043015-112122 · Cited by 533 · see citing works
Auxin Transporters--Why So Many?
Zazimalova, E., Murphy, A. S., Yang, H., Hoyerova, K., & Hosek, P. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001552 · Cited by 400 · see citing works
Xylem hydraulic physiology: The functional backbone of terrestrial plant productivity
Brodribb, T. J. (2009) · Plant Science · doi:10.1016/j.plantsci.2009.06.001 · Cited by 303 · see citing works
Stem cell function during plant vascular development
Miyashima, S., Sebastián, J., Lee, J., & Helariutta, Y. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.301 · Cited by 295 · see citing works
WOX4 Imparts Auxin Responsiveness to Cambium Cells in Arabidopsis
Suer, S., Agustí, J., Sánchez, P., Schwarz, M., & Greb, T. (2011) · The Plant Cell · doi:10.1105/tpc.111.087874 · Cited by 291 · see citing works
WOX4 Promotes Procambial Development
Ji, J., Strable, J., Shimizu, R., Koenig, D., Sinha, N. R., & Scanlon, M. J. (2009) · PLANT PHYSIOLOGY · doi:10.1104/pp.109.149641 · Cited by 282 · see citing works
Regulation of preprocambial cell state acquisition by auxin signaling inArabidopsisleaves
Donner, T. J., Sherr, I., & Scarpella, E. (2009) · Development · doi:10.1242/dev.037028 · Cited by 272 · see citing works
Auxin influx carriers stabilize phyllotactic patterningPreprint
Bainbridge, K., Guyomarc’h, S., Bayer, E., Swarup, R., Bennett, M. J., Mandel, T., & Kuhlemeier, C. J. (2008) · Genes & Development · doi:10.1101/gad.462608 · Cited by 272 · see citing works
Control of Leaf and Vein Development by AuxinPreprint
Scarpella, E., Barkoulas, M., & Tsiantis, M. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001511 · Cited by 264 · see citing works
Xylem tissue specification, patterning, and differentiation mechanisms
Schuetz, M., Smith, R. A., & Ellis, B. E. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers287 · Cited by 258 · see citing works
Self-citationTeichmann, T., & Muhr, M. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00233 · Cited by 228 · see citing works
“Biosynthesis and plasma membrane localization of PIN proteins are elevated by auxin (Paciorek et al., 2005) and the expression of PIN proteins precedes vascular development (Sauer et al., 2006; Scarpella et al., 2006; Wenzel et al., 2007).”
BackgroundMechanical Regulation of Auxin-Mediated Growth
Nakayama, N., Smith, R. S., Mandel, T., Robinson, S., Kimura, S., Boudaoud, A., & Kuhlemeier, C. J. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.050 · Cited by 227 · see citing works
Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation
Ilegems, M., Douet, V., Meylan-Bettex, M., Uyttewaal, M., Brand, L., Bowman, J. L., & Stieger, P. A. (2010) · Development · doi:10.1242/dev.047662 · Cited by 213 · see citing works
Plant grafting: insights into tissue regeneration
Melnyk, C. W. (2016) · Regeneration · doi:10.1002/reg2.71 · Cited by 207 · see citing works
Sehr, E. M., Agustí, J., Lehner, R., Farmer, E. E., Schwarz, M., & Greb, T. (2010) · The Plant Journal · doi:10.1111/j.1365-313x.2010.04283.x · Cited by 205 · see citing works
Auxin patterns<i>Solanum lycopersicum</i>leaf morphogenesis
Koenig, D., Bayer, E., Kang, J., Kuhlemeier, C., & Sinha, N. (2009) · Development · doi:10.1242/dev.033811 · Cited by 201 · see citing works
Wójcik, A. M., Wójcikowska, B., & Gaj, M. D. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041333 · Cited by 197 · see citing works
Zhiponova, M., Vanhoutte, I., Boudolf, V., Betti, C., Dhondt, S., Coppens, F., Mylle, E., Maes, S., González‐García, M. P., Caño‐Delgado, A. I., et al. (2012) · New Phytologist · doi:10.1111/nph.12036 · Cited by 193 · see citing works
Xylem development – from the cradle to the grave
Růžička, K., Ursache, R., Hejátko, J., & Helariutta, Y. (2015) · New Phytologist · doi:10.1111/nph.13383 · Cited by 186 · see citing works
Ibañes, M., Fàbregas, N., Chory, J., & Caño‐Delgado, A. I. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906416106 · Cited by 177 · see citing works
The Hormonal Regulation of Flower Development
Chandler, J. (2010) · Journal of Plant Growth Regulation · doi:10.1007/s00344-010-9180-x · Cited by 175 · see citing works
Embryonic Patterning in Arabidopsis thaliana
Jenik, P. D., Gillmor, C. S., & Lukowitz, W. (2007) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.22.011105.102609 · Cited by 174 · see citing works
Wójcikowska, B., & Gaj, M. D. (2017) · Plant Cell Reports · doi:10.1007/s00299-017-2114-3 · Cited by 162 · see citing works
The role of plant hormones during grafting
Nanda, A. K., & Melnyk, C. W. (2017) · Journal of Plant Research · doi:10.1007/s10265-017-0994-5 · Cited by 158 · see citing works
Agustí, J., Lichtenberger, R., Schwarz, M., Nehlin, L., & Greb, T. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001312 · Cited by 146 · see citing works
Patterning the axis in plants – auxin in control
Smet, I. D., & Jürgens, G. (2007) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2007.04.012 · Cited by 145 · see citing works
Patterning of Leaf Vein Networks by Convergent Auxin Transport Pathways
Sawchuk, M. G., Edgar, A. J., & Scarpella, E. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003294 · Cited by 141 · see citing works
Thermospermine is Not a Minor Polyamine in the Plant Kingdom
Takano, A., Kakehi, J.-I., & Takahashi, T. (2012) · Plant and Cell Physiology · doi:10.1093/pcp/pcs019 · Cited by 140 · see citing works
JAGGED Controls Arabidopsis Petal Growth and Shape by Interacting with a Divergent Polarity Field
Sauret-Gueto, S., Schiessl, K., Bangham, A., Sablowski, R. W. M., & Coen, E. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001550 · Cited by 137 · see citing works
Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis
Bhatia, N., Bozorg, B., Larsson, A., Ohno, C. K., Jönsson, H., & Heisler, M. G. (2016) · Current Biology · doi:10.1016/j.cub.2016.09.044 · Cited by 136 · see citing works
Hu, J. H., Su, H., Cao, H., Wei, H., Fu, X., Jiang, X., Song, Q., He, X., Xu, C., & Luo, K. (2022) · The Plant Cell · doi:10.1093/plcell/koac107 · Cited by 132 · see citing works
Habets, M. E. J., & Offringa, R. (2014) · New Phytologist · doi:10.1111/nph.12831 · Cited by 130 · see citing works
Krogan, N. T., Ckurshumova, W., Marcos, D., Caragea, A. E., & Berleth, T. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2012.04064.x · Cited by 127 · see citing works
Palovaara, J., Hallberg, H., Stasolla, C., & Hakman, I. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2010.03336.x · Cited by 119 · see citing works
de Almeida, M., de Almeida, C. V., Graner, E. M., Brondani, G. E., & de Abreu-Tarazi, M. F. (2012) · Plant Cell Reports · doi:10.1007/s00299-012-1264-6 · Cited by 114 · see citing works
Genetic Networks in Plant Vascular Development
Ruonala, R., Ko, D., & Helariutta, Y. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024525 · Cited by 109 · see citing works
PHABULOSA Mediates an Auxin Signaling Loop to Regulate Vascular Patterning in Arabidopsis
Müller, C. J., Valdés, A. E., Wang, G., Ramachandran, P., Beste, L., Uddenberg, D., & Carlsbecker, A. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01204 · Cited by 106 · see citing works
Canalization without flux sensors: a traveling-wave hypothesis
Merks, R. M. H., de Peer, Y. V., Inzé, D., & Beemster, G. T. S. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.08.004 · Cited by 104 · see citing works
Wang, Y., Deng, D., Shi, Y., Miao, N., Bian, Y., & Yin, Z. (2011) · Molecular Biology Reports · doi:10.1007/s11033-011-0991-z · Cited by 102 · see citing works
Transcriptional regulation of vascular cell fates
Ohashi‐Ito, K., & Fukuda, H. (2010) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2010.08.011 · Cited by 100 · see citing works
Negative Feedback Regulation of Auxin Signaling by ATHB8/ACL5–BUD2 Transcription Module
Baima, S., Forte, V., Possenti, M., Peñalosa, A., Leoni, G., Salvi, S., Felici, B., Ruberti, I., & Morelli, G. (2014) · Molecular Plant · doi:10.1093/mp/ssu051 · Cited by 98 · see citing works
Tryptophan-dependent auxin biosynthesis is required for HD-ZIP III-mediated xylem patterning
Ursache, R., Miyashima, S., Chen, Q., Vatén, A., Nakajima, K., Carlsbecker, A., Zhao, Y., Helariutta, Y., & Dettmer, J. (2014) · Development · doi:10.1242/dev.103473 · Cited by 97 · see citing works
Hormone interactions during vascular development
Dettmer, J., Elo, A., & Helariutta, Y. (2008) · Plant Molecular Biology · doi:10.1007/s11103-008-9374-9 · Cited by 96 · see citing works
The Diverse Roles of Auxin in Regulating Leaf Development
Xiong, Y., & Jiao, Y. (2019) · Plants · doi:10.3390/plants8070243 · Cited by 96 · see citing works
A gain-of-function mutation inIAA18altersArabidopsisembryonic apical patterning
Ploense, S. E., Wu, M., Nagpal, P., & Reed, J. W. (2009) · Development · doi:10.1242/dev.025932 · Cited by 95 · see citing works
Vascular cambium regeneration and vessel formation in wounded inflorescence stems of Arabidopsis
Mazur, E., Benková, E., & Friml, J. (2016) · Scientific Reports · doi:10.1038/srep33754 · Cited by 90 · see citing works
Transcription Factors VND1-VND3 Contribute to Cotyledon Xylem Vessel Formation
Tan, T. T., Endo, H., Sano, R., Kurata, T., Yamaguchi, M., Ohtani, M., & Demura, T. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.00461 · Cited by 90 · see citing works
Plant vascular development: mechanisms and environmental regulation
Agustí, J., & Blázquez, M. A. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03496-w · Cited by 89 · see citing works
Irrepressible MONOPTEROS / ARF 5 promotes de novo shoot formation
Ckurshumova, W., Смирнова, Т. А., Marcos, D., Zayed, Y., & Berleth, T. (2014) · New Phytologist · doi:10.1111/nph.13014 · Cited by 89 · see citing works
An Atypical bHLH Transcription Factor Regulates Early Xylem Development Downstream of Auxin
Ohashi‐Ito, K., Matsukawa, M., & Fukuda, H. (2013) · Plant and Cell Physiology · doi:10.1093/pcp/pct013 · Cited by 89 · see citing works
Molecular Control of Cell Specification and Cell Differentiation During Procambial Development
Furuta, K. M., Hellmann, E., & Helariutta, Y. (2014) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050213-040306 · Cited by 85 · see citing works
Gibberellins promote polar auxin transport to regulate stem cell fate decisions in cambium
Mäkilä, R., Wybouw, B., Smetana, O., Vainio, L., Solé-Gil, A., Lyu, M., Ye, L., Wang, X., Riccardo, S., Jenness, M. K., et al. (2023) · Nature Plants · doi:10.1038/s41477-023-01360-w · Cited by 84 · see citing works
Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves
Gardiner, J., Sherr, I., & Scarpella, E. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.093006jg · Cited by 84 · see citing works
(Pro)cambium formation and proliferation: two sides of the same coin?
Jouannet, V., Brackmann, K., & Greb, T. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.10.010 · Cited by 82 · see citing works
Regulation of vascular cell division
Campbell, L., & Turner, S. R. (2016) · Journal of Experimental Botany · doi:10.1093/jxb/erw448 · Cited by 81 · see citing works
Molecular Mechanisms for Vascular Development and Secondary Cell Wall Formation
Yang, J. H., & Wang, H. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00356 · Cited by 80 · see citing works
Genomewide identification and expression analysis of the ARF gene family in apple
Luo, X., Sun, M., Xu, R., Shu, H., Wang, J., & Zhang, S. (2014) · Journal of Genetics · doi:10.1007/s12041-014-0462-0 · Cited by 79 · see citing works
Coordination of tissue cell polarity by auxin transport and signaling
Verna, C., Ravichandran, S. J., Sawchuk, M. G., Linh, N. M., & Scarpella, E. (2019) · eLife · doi:10.7554/elife.51061 · Cited by 78 · see citing works
Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY
Ohashi‐Ito, K., Oguchi, M., Kojima, M., Sakakibara, H., & Fukuda, H. (2013) · Development · doi:10.1242/dev.087924 · Cited by 77 · see citing works
Zhou, F., Roy, B., & von Arnim, A. G. (2010) · BMC Plant Biology · doi:10.1186/1471-2229-10-193 · Cited by 75 · see citing works
Feedback from Lateral Organs Controls Shoot Apical Meristem Growth by Modulating Auxin Transport
Shi, B., Guo, X., Wang, Y., Xiong, Y., Wang, J., Hayashi, K., Lei, J., Zhang, L., & Jiao, Y. (2018) · Developmental Cell · doi:10.1016/j.devcel.2017.12.021 · Cited by 74 · see citing works
The evolution of plant development in a paleontological context
Boyce, C. K. (2009) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2009.10.001 · Cited by 73 · see citing works
Slewinski, T. L., Baker, R. F., Stubert, A., & Braun, D. M. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.202473 · Cited by 73 · see citing works
Mechanical Stress Induces Remodeling of Vascular Networks in Growing Leaves
Bar‐Sinai, Y., Julien, J.-D., Sharon, E., Armon, S., Nakayama, N., Adda-Bedia, M., & Boudaoud, A. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004819 · Cited by 71 · see citing works
Du, Q., & Wang, H. (2015) · Plant Signaling & Behavior · doi:10.1080/15592324.2015.1078955 · Cited by 70 · see citing works
Gardiner, J., Donner, T. J., & Scarpella, E. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22516 · Cited by 70 · see citing works
Shifts in leaf vein density through accelerated vein formation in C4Flaveria (Asteraceae)
McKown, A. D., & Dengler, N. G. (2009) · Annals of Botany · doi:10.1093/aob/mcp210 · Cited by 69 · see citing works
Baylis, T., Cierlik, I., Sundberg, E., & Mattsson, J. (2013) · New Phytologist · doi:10.1111/nph.12084 · Cited by 69 · see citing works
Self-citationCracking the Kranz enigma with systems biology
Fouracre, J. P., Ando, S., & Langdale, J. A. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru015 · Cited by 68 · see citing works
Quantitative analysis of venation patterns of Arabidopsis leaves by supervised image analysis
Dhondt, S., Haerenborgh, D. V., Cauwenbergh, C. V., Merks, R. M. H., Philips, W. R., Beemster, G. T. S., & Inzé, D. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04803.x · Cited by 67 · see citing works
Auxin influx importers modulate serration along the leaf margin
Kasprzewska, A., Carter, R., Swarup, R., Bennett, M. J., Monk, N., Hobbs, J. K., & Fleming, A. J. (2015) · The Plant Journal · doi:10.1111/tpj.12921 · Cited by 67 · see citing works
Auxin canalization and vascular tissue formation by TIR1/AFB‐mediated auxin signaling in Arabidopsis
Mazur, E., Kulik, I., Hajný, J., & Friml, J. (2020) · New Phytologist · doi:10.1111/nph.16446 · Cited by 65 · see citing works
Vascular Cambium: The Source of Wood Formation
Wang, D., Chen, Y., Li, W., Li, Q., Lu, M., Zhou, G., & Chai, G. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.700928 · Cited by 65 · see citing works
Hormone interactions in xylem development: a matter of signals
Milhinhos, A., & Miguel, C. M. G. (2013) · Plant Cell Reports · doi:10.1007/s00299-013-1420-7 · Cited by 64 · see citing works
The Role of Elastic Stresses on Leaf Venation Morphogenesis
Laguna, M. F., Bohn, S., & Jagla, E. A. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000055 · Cited by 63 · see citing works
Quantifying leaf venation patterns: two‐dimensional maps
Rolland‐Lagan, A., Amin, M., & Pakulska, M. M. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03678.x · Cited by 63 · see citing works
Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana
Kang, J., Mizukami, Y., Wang, H., Fowke, L. C., & Dengler, N. G. (2007) · Planta · doi:10.1007/s00425-007-0567-2 · Cited by 61 · see citing works
Auxin-mediated regulation of vascular patterning in Arabidopsis thaliana leaves
Biedroń, M., & Banasiak, A. (2018) · Plant Cell Reports · doi:10.1007/s00299-018-2319-0 · Cited by 61 · see citing works
Refahi, Y., Zardilis, A., Michelin, G., Wightman, R., Leggio, B., Legrand, J., Faure, E., Vachez, L., Armezzani, A., Risson, A.-E., et al. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.01.019 · Cited by 59 · see citing works
Connecting the plant vasculature to friend or foe
Melnyk, C. W. (2016) · New Phytologist · doi:10.1111/nph.14218 · Cited by 59 · see citing works
Vascular Pattern Formation in Plants
Scarpella, E., & Helariutta, Y. (2010) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(10)91008-9 · Cited by 59 · see citing works
Current status and trends in forest genomics
Borthakur, D., Busov, V. B., Cao, H. X., Du, Q., Gailing, O., Işik, F., Ko, J., Li, C., Li, Q., Niu, S., et al. (2022) · Forestry Research · doi:10.48130/fr-2022-0011 · Cited by 58 · see citing works
Developmental regulation of leaf venation patterns: monocot versus eudicots and the role of auxin
Perico, C., Tan, S., & Langdale, J. A. (2022) · New Phytologist · doi:10.1111/nph.17955 · Cited by 57 · see citing works
Control of vein network topology by auxin transport
Verna, C., Sawchuk, M. G., Linh, N. M., & Scarpella, E. (2015) · BMC Biology · doi:10.1186/s12915-015-0208-3 · Cited by 56 · see citing works
SlPIN1 regulates auxin efflux to affect flower abscission process
Shi, Z., Jiang, Y., Han, X., Liu, X., Cao, R., Qi, M., Xu, T., & Li, T. (2017) · Scientific Reports · doi:10.1038/s41598-017-15072-7 · Cited by 56 · see citing works
A Single-Nucleus Atlas of Seed-to-Seed Development in ArabidopsisPreprint
Lee, T. A., Nobori, T., Illouz‐Eliaz, N., Xu, J., Jow, B., Nery, J. R., & Ecker, J. R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.23.533992 · Cited by 55 · see citing works
Garrett, J. J. T., Meents, M. J., Blackshaw, M. T., Blackshaw, L. C., Hou, H., Styranko, D. M., Kohalmi, S. E., & Schultz, E. A. (2012) · Planta · doi:10.1007/s00425-012-1607-0 · Cited by 54 · see citing works
Drought recovery in plants triggers a cell-state-specific immune activation
Illouz‐Eliaz, N., Yu, J., Swift, J., Lande, K., Jow, B., Partida-Garcia, L., Tuang, Z. K., Lee, T. A., Yaaran, A., Castanon, R., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-63467-2 · Cited by 53 · see citing works
The vascular cambium: molecular control of cellular structure
Risopatron, J. P. M., Sun, Y., & Jones, B. J. (2010) · PROTOPLASMA · doi:10.1007/s00709-010-0211-z · Cited by 52 · see citing works
Shirakawa, M., Ueda, H., Shimada, T., Nishiyama, C., & Hara‐Nishimura, I. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp076 · Cited by 52 · see citing works
MultipleMONOPTEROS-Dependent Pathways Are Involved in Leaf Initiation
Schuetz, M., Berleth, T., & Mattsson, J. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.119396 · Cited by 51 · see citing works
Self-citationKonishi, M., Donner, T. J., Scarpella, E., & Yanagisawa, S. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru418 · Cited by 50 · see citing works
Novel phytohormones involved in long-range signaling
Mouchel, C. F., & Leyser, O. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.08.005 · Cited by 50 · see citing works
Context, Specificity, and Self-Organization in Auxin ResponsePreprint
Bianco, M. D., & Kepinski, S. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001578 · Cited by 46 · see citing works
Pahari, S., Cormark, R. D., Blackshaw, M. T., Liu, C., Erickson, J. L., & Schultz, E. A. (2014) · Development · doi:10.1242/dev.099333 · Cited by 44 · see citing works
Tsugeki, R., Ditengou, F. A., Sumi, Y., Teale, W., Palme, K. J., & Okada, K. (2009) · The Plant Cell · doi:10.1105/tpc.109.068841 · Cited by 44 · see citing works
- Authors
- Wenzel, C. L., Schuetz, M., Yu, Q., & Mattsson, J.
- Affiliations
- Simon Fraser University (CA)
- Corresponding author
- Mattsson, Jim
- Venue
- The Plant Journal
- Publisher
- Wiley
- Published
- 2007-01-08
- Volume
- 49
- Issue
- 3
- Pages
- 387-398
- ISSN
- 0960-7412 (ISSN-L)
- 1365-313X
- OpenAlex
- W1601614441
- Cited by
- 267
- References
- 43
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 15 · 2023: 12 · 2022: 13 · 2021: 21 · 2020: 16 · 2019: 10 · 2018: 5 · 2017: 16 · 2016: 17 · 2015: 11 · 2014: 19 · 2013: 13 · 2012: 18
- FWCI
- 22.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Plant Journal (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- MONOPTEROS, vascular patterning, auxin transport, procambium, gene expression dynamics, Arabidopsis thaliana
- MeSH terms
- DNA-Binding Proteins, Indoleacetic Acids, Mutation, Transcription Factors, Arabidopsis, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Plant Leaves, Plant Epidermis, Body Patterning, Membrane Transport Proteins, Arabidopsis Proteins, Green Fluorescent Proteins
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