The Relationship between Auxin Transport and Maize Branching
Open accessAbstract
Maize (Zea mays) plants make different types of vegetative or reproductive branches during development. Branches develop from axillary meristems produced on the flanks of the vegetative or inflorescence shoot apical meristem. Among these branches are the spikelets, short grass-specific structures, produced by determinate axillary spikelet-pair and spikelet meristems. We investigated the mechanism of branching in maize by making transgenic plants expressing a native expressed endogenous auxin efflux transporter (ZmPIN1a) fused to yellow fluorescent protein and a synthetic auxin-responsive promoter (DR5rev) driving red fluorescent protein. By imaging these plants, we found that all maize branching events during vegetative and reproductive development appear to be regulated by the creation of auxin response maxima through the activity of polar auxin transporters. We also found that the auxin transporter ZmPIN1a is functional, as it can rescue the polar auxin transport defects of the Arabidopsis (Arabidopsis thaliana) pin1-3 mutant. Based on this and on the groundbreaking analysis in Arabidopsis and other species, we conclude that branching mechanisms are conserved and can, in addition, explain the formation of axillary meristems (spikelet-pair and spikelet meristems) that are unique to grasses. We also found that BARREN STALK1 is required for the creation of auxin response maxima at the flanks of the inflorescence meristem, suggesting a role in the initiation of polar auxin transport for axillary meristem formation. Based on our results, we propose a general model for branching during maize inflorescence development.
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Cites
Floral dip: a simplified method for Agrobacterium ‐mediated transformation of Arabidopsis thaliana
Clough, S. J., & Bent, A. F. (1998) · The Plant Journal · doi:10.1046/j.1365-313x.1998.00343.x · Cited by 22,014 · see citing works
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
A monomeric red fluorescent protein
Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A., & Tsien, R. Y. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082243699 · Cited by 2,346 · 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
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
Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis
Friml, J., Wiśniewska, J., Benková, E., Mendgen, K., & Palme, K. (2002) · Nature · doi:10.1038/415806a · Cited by 1,426 · see citing works
An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root
Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T. J., Malamy, J. E., Benfey, P. N., Leyser, O., Bechtold, N., Weisbeek, P. J., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)81535-4 · Cited by 1,367 · see citing works
Heisler, M. G., Ohno, C., Das, P., Sieber, P., Reddy, G. V., Long, J. A., & Meyerowitz, E. M. (2005) · Current Biology · doi:10.1016/j.cub.2005.09.052 · Cited by 1,189 · see citing works
Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs
Reinhardt, D., Mandel, T., & Kuhlemeier, C. (2000) · The Plant Cell · doi:10.1105/tpc.12.4.507 · Cited by 1,024 · see citing works
Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation.
Okada, K., Ueda, J., Komaki, M., Bell, C. J., & Shimura, Y. (1991) · The Plant Cell · doi:10.1105/tpc.3.7.677 · Cited by 1,017 · 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
Jackson, D., Veit, B. E., & Hake, S. (1994) · Development · doi:10.1242/dev.120.2.405 · Cited by 754 · see citing works
Self-citationAntagonistic Regulation of PIN Phosphorylation by PP2A and PINOID Directs Auxin Flux
Michniewicz, M., Zago, M. K., Abas, L., Weijers, D., Schweighofer, A., Meskiene, I., Heisler, M. G., Ohno, C., Zhang, J., Huang, F., et al. (2007) · Cell · doi:10.1016/j.cell.2007.07.033 · Cited by 678 · see citing works
A plausible model of phyllotaxis
Smith, R. S., Guyomarc’h, S., Mandel, T., Reinhardt, D., Kuhlemeier, C. J., & Prusinkiewicz, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510457103 · Cited by 623 · see citing works
An auxin-driven polarized transport model for phyllotaxis
Jönsson, H., Heisler, M. G., Shapiro, B. E., Meyerowitz, E. M., & Mjolsness, E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509839103 · Cited by 616 · see citing works
Leaf polarity and meristem formation in <i>Arabidopsis</i>
McConnell, J. R., & Barton, M. K. (1998) · Development · doi:10.1242/dev.125.15.2935 · Cited by 592 · see citing works
Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation
Okada, K., Ueda, J., Komaki, M., Bell, C. J., & Shimura, Y. (1991) · The Plant Cell · doi:10.2307/3869249 · Cited by 542 · see citing works
The evolutionary dynamics of plant duplicate genes
Moore, R. C., & Purugganan, M. D. (2005) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2004.12.001 · Cited by 537 · see citing works
Xu, M., Zhu, L., Shou, H., & Wu, P. (2005) · Plant and Cell Physiology · doi:10.1093/pcp/pci183 · Cited by 485 · see citing works
Morphogenesis in pinoid mutants of Arabidopsis thaliana
Bennett, S. R. M., Alvarez, J. P., Bossinger, G., & Smyth, D. R. (1995) · The Plant Journal · doi:10.1046/j.1365-313x.1995.8040505.x · Cited by 424 · see citing works
The PIN auxin efflux facilitators: evolutionary and functional perspectives
Paponov, I. A., Teale, W., Trebar, M., Blilou, I., & Palme, K. J. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2005.02.009 · Cited by 403 · see citing works
Architecture of floral branch systems in maize and related grasses
Vollbrecht, E., Springer, P. S., Goh, L., Buckler, E. S., & Martienssen, R. A. (2005) · Nature · doi:10.1038/nature03892 · Cited by 392 · see citing works
The role of barren stalk1 in the architecture of maize
Gallavotti, A., Zhao, Q., Kyozuka, J., Meeley, R. B., Ritter, M. K., Doebley, J. F., Enrico Pè, M., & Schmidt, R. J. (2004) · Nature · doi:10.1038/nature03148 · Cited by 365 · see citing works
Self-citationde Reuille, P. B., Bohn-Courseau, I., Ljung, K., Morin, H., Carraro, N., Godin, C., & Traas, J. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510130103 · Cited by 346 · see citing works
The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1Preprint
Chuck, G., Meeley, R. B., & Hake, S. (1998) · Genes & Development · doi:10.1101/gad.12.8.1145 · Cited by 342 · see citing works
Taguchi‐Shiobara, F., Yuan, Z., Hake, S., & Jackson, D. P. (2001) · Genes & Development · doi:10.1101/gad.208501 · Cited by 330 · see citing works
Self-citationORGAN INITIATION AND THE DEVELOPMENT OF UNISEXUAL FLOWERS IN THE TASSEL AND EAR OF ZEA MAYS
Cheng, P. C., GREYSON, R. I., & Walden, D. B. (1983) · American Journal of Botany · doi:10.1002/j.1537-2197.1983.tb06411.x · Cited by 272 · see citing works
The association of culm anatomy with lodging susceptibility in modern spring wheat genotypes
Kelbert, A. J., Spaner, D., Briggs, K. G., & King, J. R. (2004) · Euphytica · doi:10.1023/b:euph.0000030670.36730.a4 · Cited by 259 · see citing works
High-Throughput Fluorescent Tagging of Full-Length Arabidopsis Gene Products in Planta
Tian, G.-W., Mohanty, A., Chary, S. N., Li, S., Paap, B. K., Drakakaki, G., Kopec, C. D., Li, J., Ehrhardt, D. W., Jackson, D. P., et al. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.040139 · Cited by 236 · see citing works
Self-citationPaz, M. M., Shou, H., Guo, Z., Zhang, Z., Banerjee, A. K., & Wang, K. (2004) · Euphytica · doi:10.1023/b:euph.0000030669.75809.dc · Cited by 235 · see citing works
Genetics and Evolution of Inflorescence and Flower Development in Grasses
Bommert, P., Satoh‐Nagasawa, N., Jackson, D. P., & Hirano, H. (2005) · Plant and Cell Physiology · doi:10.1093/pcp/pci504 · Cited by 210 · see citing works
Self-citationMcSteen, P., Malcomber, S., Skirpan, A., Lunde, C., Wu, X., Kellogg, E., & Hake, S. (2007) · Plant Physiology · doi:10.1104/pp.107.098558 · Cited by 186 · see citing works
A floret by any other name: control of meristem identity in maize
McSteen, P., Laudencia‐Chingcuanco, D., & Colasanti, J. (2000) · Trends in Plant Science · doi:10.1016/s1360-1385(99)01541-1 · Cited by 158 · see citing works
Carraro, N., Forestan, C., Canova, S., Traas, J. A., & Varotto, S. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.080119 · Cited by 155 · see citing works
Scanlon, M. J. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.026880 · Cited by 154 · see citing works
<i>barren inflorescence2</i> regulates axillary meristem development in the maize inflorescence
McSteen, P., & Hake, S. (2001) · Development · doi:10.1242/dev.128.15.2881 · Cited by 148 · see citing works
Disruption of Auxin Transport Is Associated with Aberrant Leaf Development in Maize
Tsiantis, M., Brown, M. I. N., Skibinski, G., & Langdale, J. A. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.121.4.1163 · Cited by 110 · see citing works
The maize mutant <i>barren stalk1</i> is defective in axillary meristem development
Ritter, M. K., Padilla, C. M., & Schmidt, R. J. (2002) · American Journal of Botany · doi:10.3732/ajb.89.2.203 · Cited by 90 · cited 4× · see citing works
“…et al., 2007), and BA1 encodes a basic helix-loop-helix transcription factor (Gallavotti et al., 2004). ba1 mutants completely lack all axillary meristems, resulting in a complete sterile plant essentially composed of a stalk and several leaves (Ritter et al., 2002; Gallavotti et al., 2004).”
BackgroundInfluentialSelf-citationFloral displays: genetic control of grass inflorescences
Kellogg, E. A. (2006) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2006.11.009 · Cited by 87 · see citing works
The role of auxin transport during inflorescence development in maize (<i>Zea mays</i>, Poaceae)
Wu, X., & McSteen, P. (2007) · American Journal of Botany · doi:10.3732/ajb.94.11.1745 · Cited by 76 · see citing works
Irish, E. E. (1997) · American Journal of Botany · doi:10.2307/2446611 · Cited by 75 · see citing works
Barazesh, S., & McSteen, P. (2008) · Genetics · doi:10.1534/genetics.107.084079 · Cited by 62 · see citing works
Branching Out: The ramosa Pathway and the Evolution of Grass Inflorescence Morphology
McSteen, P. (2006) · The Plant Cell · doi:10.1105/tpc.105.040196 · Cited by 51 · see citing works
Combinatorial control of meristem identity in maize inflorescences
Kaplinsky, N. J., & Freeling, M. (2003) · Development · doi:10.1242/dev.00336 · Cited by 30 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Neuffer M, Coe E, Wessler S (1997) Mutants of maize. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Cited by
Sorted by citations
Marín, E., Jouannet, V., Herz, A., Lokerse, A. S., Weijers, D., Vaucheret, H., Nussaume, L., Crespi, M. D., & Maizel, A. (2010) · The Plant Cell · doi:10.1105/tpc.109.072553 · Cited by 597 · see citing works
A dynamic gene expression atlas covering the entire life cycle of rice
Wang, L., Xie, W., Chen, Y., Tang, W., Yang, J., Ye, R., Liu, L., Lin, Y., Xu, C., Xiao, J., et al. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2009.04100.x · Cited by 353 · see citing works
Doehlemann, G., van der Linde, K., Daniela, A., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D. P., & Kahmann, R. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000290 · Cited by 348 · see citing works
Self-citationThe maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size
Bommert, P., Je, B. I., Goldshmidt, A., & Jackson, D. P. (2013) · Nature · doi:10.1038/nature12583 · Cited by 298 · see citing works
Self-citationUnraveling the KNOTTED1 regulatory network in maize meristemsPreprint
Bolduc, N., Yılmaz, A., Mejía‐Guerra, M. K., Morohashi, K., O’Connor, D., Erich Grotewold, A., & Hake, S. (2012) · Genes & Development · doi:10.1101/gad.193433.112 · Cited by 295 · see citing works
Phillips, K. A., Skirpan, A. L., Liu, X., Christensen, A., Slewinski, T. L., Hudson, C., Barazesh, S., Cohen, J. D., Malcomber, S., & McSteen, P. (2011) · The Plant Cell · doi:10.1105/tpc.110.075267 · Cited by 286 · see citing works
Gallavotti, A., Barazesh, S., Malcomber, S. T., Hall, D. H., Jackson, D. P., Schmidt, R. J., & McSteen, P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805596105 · Cited by 275 · see citing works
Self-citationTwo-Step Regulation of LAX PANICLE1 Protein Accumulation in Axillary Meristem Formation in Rice
Oikawa, T., & Kyozuka, J. (2009) · The Plant Cell · doi:10.1105/tpc.108.065425 · Cited by 251 · see citing works
Molecular Control of Grass Inflorescence Development
Zhang, D., & Yuan, Z. (2014) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050213-040104 · Cited by 235 · see citing works
Leitner, J. J., Petrášek, J., Tomanov, K., Retzer, K., Pařezová, M., Korbei, B., Bachmair, A., Zažı́malová, E., & Luschnig, C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200824109 · Cited by 213 · see citing works
Developmental Roles of AUX1/LAX Auxin Influx Carriers in Plants
Swarup, R., & Bhosale, R. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.01306 · Cited by 211 · see citing works
The Stem Cell Niche in Leaf Axils Is Established by Auxin and Cytokinin in <i>Arabidopsis</i>
Wang, Y., Wang, J., Shi, B., Yu, T., Qi, J., Meyerowitz, E. M., & Jiao, Y. (2014) · The Plant Cell · doi:10.1105/tpc.114.123083 · Cited by 207 · 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
Hormonal regulation of branching in grasses
McSteen, P. (2009) · Plant Physiology · doi:10.1104/pp.108.129056 · Cited by 193 · see citing works
Auxin signaling modules regulate maize inflorescence architecture
Galli, M., Liu, Q., Moss, B. L., Malcomber, S. T., Li, W., Gaines, C., Federici, S., Roshkovan, J., Meeley, R. B., Nemhauser, J. L., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516473112 · Cited by 182 · see citing works
Self-citationAuxin and Monocot DevelopmentPreprint
McSteen, P. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001479 · Cited by 182 · see citing works
Eubel, H., Meyer, E. H., Taylor, N. L., Bussell, J. D., O’Toole, N., Heazlewood, J. L., Castleden, I. R., Small, I., Smith, S. M., & Millar, A. H. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.129999 · Cited by 178 · see citing works
Wang, Q., Kohlen, W., Rossmann, S., Vernoux, T., & Theres, K. (2014) · The Plant Cell · doi:10.1105/tpc.114.123059 · Cited by 172 · see citing works
“However, recent reports have demonstrated that auxin response maxima promote the initiation of AMs during maize inflorescence development (Gallavotti et al., 2008).”
BackgroundThe role of auxin in shaping shoot architecture
Gallavotti, A. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert141 · Cited by 177 · see citing works
Self-citationMaternal auxin supply contributes to early embryo patterning in Arabidopsis
Robert, H. S., Park, C., Gutièrrez, C. L., Wójcikowska, B., Pěnčík, A., Novák, O., Chen, J., Grunewald, W., Dresselhaus, T., Friml, J., et al. (2018) · Nature Plants · doi:10.1038/s41477-018-0204-z · Cited by 175 · see citing works
Root architecture and root and tuber crop productivity
Villordon, A. Q., Ginzberg, I., & Firon, N. (2014) · Trends in Plant Science · doi:10.1016/j.tplants.2014.02.002 · Cited by 169 · see citing works
Post-embryonic root organogenesis in cereals: branching out from model plants
Orman-Ligeza, B., Parizot, B., Gantet, P., Beeckman, T., Bennett, M. J., & Draye, X. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.04.010 · Cited by 166 · see citing works
Dong, Z., Jiang, C., Chen, X., Zhang, T., Ding, L., Song, W., Luo, H., Lai, J., Chen, H., Liu, R., et al. (2013) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.227314 · Cited by 164 · see citing works
Coming into bloom: the specification of floral meristems
Liu, C., Thong, Z., & Yu, H. Q. (2009) · Development · doi:10.1242/dev.033076 · Cited by 162 · see citing works
Unraveling the Evolution of Auxin Signaling
Smet, I. D., Voß, U., Lau, S., Wilson, M. H., Shao, N., Timme, R., Swarup, R., Kerr, I. D., Hodgman, C. T., Bock, R., et al. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.168161 · Cited by 161 · see citing works
The role of auxin transporters in monocots development
Balzan, S., Johal, G. S., & Carraro, N. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00393 · Cited by 156 · see citing works
Regulatory modules controlling maize inflorescence architecturePreprint
Eveland, A. L., Goldshmidt, A., Pautler, M., Morohashi, K., Liseron-Monfils, C., Lewis, M. W., Kumari, S., Hiraga, S., Yang, F., Unger‐Wallace, E., et al. (2013) · Genome Research · doi:10.1101/gr.166397.113 · Cited by 156 · see citing works
Self-citationMatthes, M. S., Best, N. B., Robil, J. M., Malcomber, S. T., Gallavotti, A., & McSteen, P. (2018) · Molecular Plant · doi:10.1016/j.molp.2018.12.012 · Cited by 154 · see citing works
Self-citationA simple and versatile cell wall staining protocol to study plant reproduction
Musielak, T., Schenkel, L., Kolb, M., Henschen, A., & Bayer, M. J. (2015) · Plant Reproduction · doi:10.1007/s00497-015-0267-1 · Cited by 153 · see citing works
On the mechanisms of development in monocot and eudicot leaves
Conklin, P. A., Strable, J., Li, S., & Scanlon, M. J. (2018) · New Phytologist · doi:10.1111/nph.15371 · Cited by 144 · see citing works
A serine/threonine protein kinase encoding gene KERNEL NUMBER PER ROW6 regulates maize grain yield
Jia, H., Li, M., Li, W., Liu, L., Jian, Y., Yang, Z., Shen, X., Ning, Q., Du, Y., Zhao, R., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14746-7 · Cited by 147 · see citing works
Self-citationYoshida, A., Ohmori, Y., Kitano, H., Taguchi‐Shiobara, F., & Hirano, H. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04872.x · Cited by 145 · see citing works
Doehlemann, G., Reißmann, S., Daniela, A., Fleckenstein, M. A., & Kahmann, R. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07728.x · Cited by 145 · see citing works
A Division in PIN-Mediated Auxin Patterning during Organ Initiation in Grasses
O’Connor, D., Runions, A., Sluis, A., Bragg, J. N., Vogel, J. P., Prusinkiewicz, P., & Hake, S. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003447 · Cited by 143 · see citing works
The Maize PIN Gene Family of Auxin Transporters
Forestan, C., Farinati, S., & Varotto, S. (2012) · Frontiers in Plant Science · doi:10.3389/fpls.2012.00016 · Cited by 139 · see citing works
Lee, B., Johnston, R., Yang, Y., Gallavotti, A., Kojima, M., Travençolo, B. A. N., Costa, L. D. F., Sakakibara, H., & Jackson, D. P. (2009) · PLANT PHYSIOLOGY · doi:10.1104/pp.109.137034 · Cited by 136 · see citing works
Self-citationScarecrow Plays a Role in Establishing Kranz Anatomy in Maize Leaves
Slewinski, T. L., Anderson, A. A., Zhang, C., & Turgeon, R. (2012) · Plant and Cell Physiology · doi:10.1093/pcp/pcs147 · Cited by 129 · see citing works
Axillary meristem initiation — a way to branch out
Wang, Y., & Jiao, Y. (2017) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2017.09.001 · Cited by 129 · see citing works
Nizampatnam, N. R., Schreier, S. J., Damodaran, S., Adhikari, S., & Subramanian, S. (2015) · The Plant Journal · doi:10.1111/tpj.12965 · Cited by 121 · see citing works
A multi-omics integrative network map of maize
Han, L., Zhong, W., Qian, J., Jin, M., Tian, P., Zhu, W., Zhang, H., Sun, Y., Feng, J., Liu, X., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01262-1 · Cited by 120 · see citing works
Johnston, R., Wang, M., Sun, Q., Sylvester, A. W., Hake, S., & Scanlon, M. J. (2014) · The Plant Cell · doi:10.1105/tpc.114.132688 · Cited by 119 · see citing works
Rios, A. F., Tanaka, K., Crespo, I., van der Wijk, E., Sizentsova, Y., Levitsky, V. G., Lindhoud, S., Fontana, M., Hohlbein, J., Boer, R., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2009554117 · Cited by 119 · see citing works
Lu, C., Chen, M., Liu, R., Zhang, L., Hou, X., Liu, S., Ding, X., Jiang, Y., Xu, J., Zhang, J., et al. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00716 · Cited by 111 · see citing works
<i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems
Wang, Q., Hasson, A., Rossmann, S., & Theres, K. (2016) · New Phytologist · doi:10.1111/nph.13641 · Cited by 106 · see citing works
A Conserved Mechanism of Bract Suppression in the Grass Family
Whipple, C., Hall, D. H., DeBlasio, S. L., Taguchi‐Shiobara, F., Schmidt, R. J., & Jackson, D. P. (2010) · The Plant Cell · doi:10.1105/tpc.109.073536 · Cited by 106 · see citing works
Self-citationParallel Proteomic and Phosphoproteomic Analyses of Successive Stages of Maize Leaf Development
Facette, M. R., Shen, Z., Björnsdóttir, F. R., Briggs, S. P., & Smith, L. G. (2013) · The Plant Cell · doi:10.1105/tpc.113.112227 · Cited by 102 · see citing works
Sporisorium reilianumInfection Changes Inflorescence and Branching Architectures of Maize
Ghareeb, H., Becker, A., Iven, T., Feußner, I., & Schirawski, J. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.179499 · Cited by 101 · see citing works
Sun, X., Cahill, J., Hautegem, T. V., Feys, K., Whipple, C., Novák, O., Delbare, S., Versteele, C., Demuynck, K., Block, J. D., et al. (2017) · Nature Communications · doi:10.1038/ncomms14752 · Cited by 99 · see citing works
Genetic variation in YIGE1 contributes to ear length and grain yield in maize
Luo, Y., Zhang, M., Liu, Y., Liu, J., Li, W., Chen, G., Peng, Y., Jin, M., Wei, W., Jian, L., et al. (2021) · New Phytologist · doi:10.1111/nph.17882 · Cited by 97 · see citing works
Advancing Cell Biology and Functional Genomics in Maize Using Fluorescent Protein-Tagged Lines
Mohanty, A., Luo, A., DeBlasio, S. L., Ling, X., Yang, Y., Tuthill, D., Williams, K. E., Hill, D. R., Zadrozny, T., Chan, A. P.-Y., et al. (2009) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.130146 · Cited by 97 · see citing works
Self-citationBARREN STALK FASTIGIATE1 Is an AT-Hook Protein Required for the Formation of Maize Ears
Gallavotti, A., Malcomber, S. T., Gaines, C., Stanfield, S. W., Whipple, C., Kellogg, E. A., & Schmidt, R. J. (2011) · The Plant Cell · doi:10.1105/tpc.111.084590 · Cited by 97 · see citing works
Self-citationWang, L., Ming, L., Liao, K., Xia, C., Sun, S., Chang, Y., Wang, H., Fu, D., Xu, C., Wang, Z., et al. (2021) · Molecular Plant · doi:10.1016/j.molp.2021.04.013 · Cited by 92 · see citing works
A Maize Glutaredoxin Gene, Abphyl2, Regulates Shoot Meristem Size and Phyllotaxy
Yang, F., Bui, H., Pautler, M., Llaca, V., Johnston, R., Lee, B., Kolbe, A. R., Sakai, H., & Jackson, D. P. (2015) · The Plant Cell · doi:10.1105/tpc.114.130393 · Cited by 86 · see citing works
Self-citationForestan, C., & Varotto, S. (2011) · Molecular Plant · doi:10.1093/mp/ssr103 · Cited by 85 · see citing works
Wang, F., Yu, Z., Zhang, M., Wang, M., Lu, X., Liu, X., Li, Y., Zhang, X., Tan, B., Li, C., et al. (2021) · Plant Biotechnology Journal · doi:10.1111/pbi.13734 · Cited by 82 · see citing works
The Liguleless narrow mutation affects proximal-distal signaling and leaf growth
Moon, J., Candela, H., & Hake, S. (2012) · Development · doi:10.1242/dev.085787 · Cited by 80 · see citing works
Skirpan, A. L., Culler, A. H., Gallavotti, A., Jackson, D. P., Cohen, J. D., & McSteen, P. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp006 · Cited by 80 · see citing works
Self-citationA Genome-wide View of Transcriptome Dynamics During Early Spike Development in Bread Wheat
Li, Y., Fu, X., Zhao, M., Zhang, W., Li, B., An, D., Li, J., Zhang, A., Liu, R., & Liu, X. (2018) · Scientific Reports · doi:10.1038/s41598-018-33718-y · Cited by 79 · see citing works
Hormonal control of grass inflorescence development
Barazesh, S., & McSteen, P. (2008) · Trends in Plant Science · doi:10.1016/j.tplants.2008.09.007 · Cited by 78 · see citing works
Yang, J., Yuan, Z., Meng, Q., Huang, G., Périn, C., Bureau, C., Meunier, A., Ingouff, M., Bennett, M. J., Liang, W., et al. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00256 · Cited by 78 · see citing works
Yu, P., Eggert, K., Nicolaus Von Wirén, A., Li, C., & Hochholdinger, F. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.00888 · Cited by 75 · see citing works
Hormonal responses during early embryogenesis in maize
Chen, J., Lausser, A., & Dresselhaus, T. (2014) · Biochemical Society Transactions · doi:10.1042/bst20130260 · Cited by 74 · 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
Genetic regulation of maize flower development and sex determination
Li, Q., & Liu, B. (2016) · Planta · doi:10.1007/s00425-016-2607-2 · Cited by 73 · see citing works
Lituiev, D., Krohn, N. G., Muller, B. H., Jackson, D. P., Hellriegel, B., Dresselhaus, T., & Grossniklaus, U. (2013) · Development · doi:10.1242/dev.098301 · Cited by 70 · see citing works
Self-citationSterility Caused by Floral Organ Degeneration and Abiotic Stresses in Arabidopsis and Cereal Grains
Smith, A. R., & Zhao, D. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01503 · Cited by 70 · see citing works
Developmental and transcriptional responses of maize to drought stress under field conditions
Danilevskaya, O. N., Yu, G.-X., Meng, X., Xu, J., Stephenson, E., Estrada, S., Chilakamarri, S., Zastrow‐Hayes, G., & Thatcher, S. (2019) · Plant Direct · doi:10.1002/pld3.129 · Cited by 69 · see citing works
A Maize Thiamine Auxotroph Is Defective in Shoot Meristem Maintenance
Woodward, J. B., Abeydeera, N., Paul, D., Phillips, K. A., Rąpała‐Kozik, M., Freeling, M., Begley, T. P., Ealick, S. E., McSteen, P., & Scanlon, M. J. (2010) · The Plant Cell · doi:10.1105/tpc.110.077776 · Cited by 66 · see citing works
Sparse panicle1 is required for inflorescence development in Setaria viridis and maize
Huang, P., Jiang, H., Zhu, C., Barry, K., Jenkins, J. W., Sandor, L., Schmutz, J., Box, M. S., Kellogg, E. A., & Brutnell, T. P. (2017) · Nature Plants · doi:10.1038/nplants.2017.54 · Cited by 65 · see citing works
Auxin Efflux Carrier ZmPGP1 Mediates Root Growth Inhibition under Aluminum Stress
Zhang, M., Lu, X., Li, C., Zhang, B., Zhang, C., Zhang, X., & Ding, Z. (2018) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.01379 · Cited by 65 · see citing works
The transcription factor AtDOF4.2 regulates shoot branching and seed coat formation in Arabidopsis
Zou, H., Zhang, Y.-Q., Wei, W., Chen, H., Song, Q., Liu, Y.-F., Zhao, M.-Y., Wang, F., Zhang, B., Lin, Q. F., et al. (2012) · Biochemical Journal · doi:10.1042/bj20110060 · Cited by 62 · see citing works
The Maize Leaf: Another Perspective on Growth Regulation
Avramova, V., Sprangers, K., & Beemster, G. T. S. (2015) · Trends in Plant Science · doi:10.1016/j.tplants.2015.09.002 · Cited by 62 · see citing works
Deveshwar, P., Prusty, A., Sharma, S., & Tyagi, A. K. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.586462 · Cited by 61 · see citing works
Auxin polar transport in stamen formation and development: how many actors?
Cardarelli, M., & Cecchetti, V. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00333 · Cited by 61 · see citing works
Identification and expression analysis of PIN genes in rice
Miyashita, Y., Takasugi, T., & Ito, Y. (2010) · Plant Science · doi:10.1016/j.plantsci.2010.02.018 · Cited by 61 · see citing works
Patterning at the shoot apical meristem and phyllotaxis
Shi, B., & Vernoux, T. (2018) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2018.10.003 · Cited by 61 · see citing works
DR5 as a reporter system to study auxin response in Populus
Chen, Y., Yordanov, Y. S., Ma, C., Strauss, S. H., & Busov, V. B. (2013) · Plant Cell Reports · doi:10.1007/s00299-012-1378-x · 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
Xue, H., Veit, C., Abas, L., Tryfona, T., Maresch, D., Ricardi, M. M., Estevez, J. M., Strasser, R., & Seifert, G. J. (2017) · The Plant Journal · doi:10.1111/tpj.13591 · Cited by 57 · 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
Liu, Q., Galli, M., Liu, X., Federici, S., Buck, A., Cody, J. P., Labra, M., & Gallavotti, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907071116 · Cited by 55 · see citing works
Self-citationDown-expression of TaPIN1s Increases the Tiller Number and Grain Yield in Wheat
Yao, F. Q., Li, X. H., Wang, H., Song, Y. N., Li, Z. Q., Li, X. G., Gao, X., Zhang, X. S., & Bie, X. M. (2021) · BMC Plant Biology · doi:10.1186/s12870-021-03217-w · Cited by 54 · see citing works
Nishimura, T., Nakano, H., Hayashi, K., Niwa, C., & Koshiba, T. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp129 · Cited by 53 · see citing works
The barren stalk2 Gene Is Required for Axillary Meristem Development in Maize
Yao, H., Skirpan, A. L., Wardell, B., Matthes, M. S., Best, N. B., McCubbin, T., Durbak, A. R., Smith, T., Malcomber, S. T., & McSteen, P. (2019) · Molecular Plant · doi:10.1016/j.molp.2018.12.024 · Cited by 53 · see citing works
Bartlett, M. E., Williams, S. K., Taylor, Z., DeBlasio, S. L., Goldshmidt, A., Hall, D. H., Schmidt, R. J., Jackson, D. P., & Whipple, C. (2015) · The Plant Cell · doi:10.1105/tpc.15.00679 · Cited by 52 · see citing works
Self-citationGenetic control of branching patterns in grass inflorescences
Kellogg, E. A. (2022) · The Plant Cell · doi:10.1093/plcell/koac080 · Cited by 50 · see citing works
Meristem identity and phyllotaxis in inflorescence development
Bartlett, M. E., & Thompson, B. E. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00508 · Cited by 50 · see citing works
Translating auxin responses into ovules, seeds and yield: Insight from Arabidopsis and the cereals
Shirley, N. J., Aubert, M. K., Wilkinson, L. G., Bird, D. C., Lora, J., Yang, X., & Tucker, M. R. (2018) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12747 · Cited by 49 · see citing works
Laureyns, R., Joossens, J., Herwegh, D., Pevernagie, J., Pavie, B., Demuynck, K., Debray, K., Coussens, G., Pauwels, L., Hautegem, T. V., et al. (2021) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiab533 · Cited by 45 · see citing works
Divergent Roles for Maize PAN1 and PAN2 Receptor-Like Proteins in Cytokinesis and Cell Morphogenesis
Sutimantanapi, D., Pater, D., & Smith, L. G. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.232660 · Cited by 45 · see citing works
Stephenson, E., Estrada, S., Meng, X., Ourada, J., Muszynski, M. G., Habben, J. E., & Danilevskaya, O. N. (2019) · PLoS ONE · doi:10.1371/journal.pone.0203728 · Cited by 43 · see citing works
TALE and Shape: How to Make a Leaf Different
Giacomo, E. D., Iannelli, M. A., & Frugis, G. (2013) · Plants · doi:10.3390/plants2020317 · Cited by 43 · see citing works
Local auxin biosynthesis regulates brace root angle and lodging resistance in maize
Zheng, Z., Wang, B., Zhuo, C., Xie, Y., Zhang, X., Liu, Y., Zhang, G., Ding, H., Zhao, B., Tian, M., et al. (2023) · New Phytologist · doi:10.1111/nph.18733 · Cited by 41 · see citing works
Martinez, C. C., Koenig, D., Chitwood, D. H., & Sinha, N. R. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.08.011 · Cited by 41 · see citing works
Wang, X., Feng, J., White, P. J., Shen, J., & Cheng, L. (2019) · Annals of Botany · doi:10.1093/aob/mcz154 · Cited by 41 · see citing works
Tissue-specific transcriptomics reveal functional differences in floral development
Yang, H., Nukunya, K., Ding, Q., & Thompson, B. E. (2021) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiab557 · Cited by 39 · see citing works
Pressoir, G., Brown, P. J., Zhu, W., Upadyayula, N., Rocheford, T., Buckler, E. S., & Kresovich, S. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2009.03802.x · Cited by 38 · see citing works
What Has Been Seen Cannot Be Unseen—Detecting Auxin In Vivo
Pařízková, B., Pernisová, M., & Novák, O. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122736 · Cited by 38 · see citing works
Matsuda, S., Kajizuka, T., Kadota, A., Nishimura, T., & Koshiba, T. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err019 · Cited by 37 · see citing works
“In the monocot maize, ZmPIN1a, b, and c are involved in auxin transport during embryogenesis and vegetative development (Carraro et al., 2006; Gallavotti et al., 2008; Forestan et al., 2010).”
Hormonal control of medial–lateral growth and vein formation in the maize leaf
Robil, J. M., & McSteen, P. (2022) · New Phytologist · doi:10.1111/nph.18625 · Cited by 36 · see citing works
- Authors
- Gallavotti, A., Yang, Y., Schmidt, R. J., & Jackson, D.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Venue
- Plant Physiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-06-11
- Volume
- 147
- Issue
- 4
- Pages
- 1913-1923
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC2492655
- OpenAlex
- W2017000081
- Cited by
- 227
- References
- 49
- Citations by year
- 2026: 6 · 2025: 12 · 2024: 15 · 2023: 17 · 2022: 13 · 2021: 13 · 2020: 14 · 2019: 11 · 2018: 13 · 2017: 11 · 2016: 8 · 2015: 13 · 2014: 15 · 2013: 15 · 2012: 13
- FWCI
- 14.96
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- PLANT PHYSIOLOGY (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- National Science Foundation
- U.S. Department of Agriculture
- Iowa State University
- 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 › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
- Keywords
- polar auxin transport, auxin efflux transporters, axillary meristem, inflorescence development
- MeSH terms
- Biological Transport, Zea mays, Indoleacetic Acids, Models, Biological, Mutation, Phthalimides, Plant Proteins, Up-Regulation, Arabidopsis, Genes, Reporter, Meristem, Plants, Genetically Modified
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