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  • Review Article
  • Published:

Spatiotemporal signalling in plant development

Key Points

  • Plants are sessile organisms and have developed unique signalling mechanisms that allow the integration of external cues in order to continuously modulate developmental processes.

  • The integration of multiple signalling pathways is important for plant development. These pathways include short- and long-range signals that give rise to a whole-organism response.

  • Short-range signals, such as peptides, transcription factors and noncoding small RNAs, are used to provide local communication between plant cells that are constrained by a cell wall.

  • Long-range signals, such as phytohormones, use diverse regulatory and integration mechanisms to elicit a broad range of signal outputs.

Abstract

Plants, being sessile organisms, need to respond to changing environments, and as a result they have evolved unique signalling mechanisms that allow rapid communication between different parts of the plant. The signalling mechanisms that direct plant development include long-range effectors, such as phytohormones, and molecules with a local intra-organ range, such as peptides, transcription factors and some small RNAs. In this Review, we highlight recent advances in understanding plant signalling mechanisms and discuss how different classes of signalling networks can integrate with gene regulatory networks and contribute to plant development. In some cases, we also address the evolutionary context of mechanisms and discuss possible links between the lifestyle of plants and selection for different signalling mechanisms.

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Figure 1: Schematic representation of Arabidopsis thaliana meristems and types of signalling.
Figure 2: Routes of intercellular movement.
Figure 3: Peptide signalling in meristem maintenance.
Figure 4: Transcription factor and small non-coding RNA movement in the root meristem.
Figure 5: Dynamics of auxin responses.

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References

  1. Bradshaww, A. D. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13, 115–155 (1965).

    Article  Google Scholar 

  2. Lease, K. A. & Walker, J. C. The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol. 142, 831–838 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Murphy, E., Smith, S. & De Smet, I. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24, 3198–3217 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Matsubayashi, Y. MBSJ MCC Young Scientist Award 2010. Recent progress in research on small post-translationally modified peptide signals in plants. Genes Cells 17, 1–10 (2012).

    Article  CAS  PubMed  Google Scholar 

  5. Hirakawa, Y. et al. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl Acad. Sci. USA 105, 15208–15213 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Shiu, S.-H. & Bleecker, A. B. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. Signal. 2001, re22 (2001).

    Article  CAS  Google Scholar 

  7. Torii, K. U. Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int. Rev. Cytol. 234, 1–46 (2004).

    Article  CAS  PubMed  Google Scholar 

  8. Cock, J. M. & McCormick, S. A large family of genes that share homology with CLAVATA3. Plant Physiol. 126, 939–942 (2001).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Oelkers, K. et al. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 8, 1 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Clark, S. E., Running, M. P. & Meyerowitz, E. M. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057–2067 (1995).

    CAS  Google Scholar 

  11. Fletcher, J. C. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911–1914 (1999).

    Article  CAS  PubMed  Google Scholar 

  12. Ogawa, M., Shinohara, H., Sakagami, Y. & Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294–294 (2008).

    Article  CAS  PubMed  Google Scholar 

  13. Guo, Y., Han, L., Hymes, M., Denver, R. & Clark, S. E. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889–900 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Kinoshita, A. et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911–3920 (2010).

    Article  CAS  PubMed  Google Scholar 

  15. Kayes, J. M. & Clark, S. E. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125, 3843–3851 (1998).

    CAS  PubMed  Google Scholar 

  16. Jeong, S., Trotochaud, A. E. & Clark, S. E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11, 1925–1934 (1999).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Nimchuk, Z. L., Tarr, P. T. & Meyerowitz, E. M. An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell 23, 851–854 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Chevalier, D. et al. STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc. Natl Acad. Sci. USA 102, 9074–9079 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Castells, E. & Casacuberta, J. M. Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants. J. Exp. Bot. 58, 3503–3511 (2007).

    Article  CAS  PubMed  Google Scholar 

  20. Laux, T., Mayer, K. F., Berger, J. & Jürgens, G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87–96 (1996).

    CAS  PubMed  Google Scholar 

  21. Mayer, K. F. et al. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815 (1998).

    Article  CAS  PubMed  Google Scholar 

  22. Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. & Simon, R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617–619 (2000).

    Article  CAS  PubMed  Google Scholar 

  23. Schoof, H. et al. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644 (2000).

    Article  CAS  PubMed  Google Scholar 

  24. Brandman, O. & Meyer, T. Feedback loops shape cellular signals in space and time. Science 322, 390–395 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Muller, R., Bleckmann, A. & Simon, R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Sci. Signal. 20, 934 (2008).

    Google Scholar 

  26. Reddy, G. V. Live-imaging stem-cell homeostasis in the Arabidopsis shoot apex. Curr. Opin. Plant Biol. 11, 88–93 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. Clark, S. E., Williams, R. W. & Meyerowitz, E. M. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575–585 (1997).

    Article  CAS  PubMed  Google Scholar 

  28. Trotochaud, A. E., Hao, T., Wu, G., Yang, Z. & Clark, S. E. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11, 393–406 (1999).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Williams, R. W., Wilson, J. M. & Meyerowitz, E. M. A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc. Natl Acad. Sci. USA 94, 10467–10472 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Song, S.-K., Lee, M. M. & Clark, S. E. POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells. Development 133, 4691–4698 (2006).

    Article  CAS  PubMed  Google Scholar 

  31. Haecker, A. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131, 657–668 (2004).

    Article  CAS  PubMed  Google Scholar 

  32. Sarkar, A. K. et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. Stahl, Y., Wink, R. H., Ingram, G. C. & Simon, R. A. Signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19, 909–914 (2009).

    Article  CAS  PubMed  Google Scholar 

  34. Hobe, M., M. ller, R., Gr newald, M., Brand, U. & Simon, R. D. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev. Genes Evol. 213, 371–381 (2003).

    Article  CAS  PubMed  Google Scholar 

  35. Stahl, Y. et al. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23, 362–371 (2013).

    Article  CAS  PubMed  Google Scholar 

  36. Matsuzaki, Y., Ogawa-Ohnishi, M., Mori, A. & Matsubayashi, Y. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329, 1065–1067 (2010). This article takes a unique approach to identifying peptide signals involved in plant development by examining a mutant of a protein that modifies peptide signals.

    Article  CAS  PubMed  Google Scholar 

  37. Meng, L., Buchanan, B. B., Feldman, L. J. & L. uan, S. CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. Proc. Natl Acad. Sci. USA 109, 1760–1765 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Komori, R., Amano, Y., Ogawa-Ohnishi, M. & Matsubayashi, Y. Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl Acad. Sci. USA 106, 15067–15072 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Moore, K. L. The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278, 24243–24246 (2003).

    Article  CAS  PubMed  Google Scholar 

  40. Matsubayashi, Y. & Sakagami, Y. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc. Natl Acad. Sci. USA 93, 7623–7627 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Amano, Y., Tsubouchi, H., Shinohara, H., Ogawa, M. & Matsubayashi, Y. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl Acad. Sci. USA 104, 18333–18338 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Zhou, W. et al. Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22, 3692–3709 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Song, S.-K., Hofhuis, H., Lee, M. M. & Clark, S. E. Key divisions in the early Arabidopsis embryo require POL and PLL1 phosphatases to establish the root stem cell organizer and vascular axis. Dev. Cell 15, 98–109 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Lucas, W. J. et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980–1983 (1995).

    Article  CAS  PubMed  Google Scholar 

  45. Jackson, D., Veit, B. & Hake, S. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120, 405–413 (1994).

    CAS  Google Scholar 

  46. Lee, J.-Y. et al. Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc. Natl Acad. Sci. USA 103, 6055–6060 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Rim, Y. et al. Analysis of Arabidopsis transcription factor families revealed extensive capacity for cell-to-cell movement as well as discrete trafficking patterns. Mol. Cell 32, 519–526 (2011).

    Article  CAS  Google Scholar 

  48. Gallagher, K. L. & Benfey, P. N. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J. 57, 785–797 (2009).

    Article  CAS  PubMed  Google Scholar 

  49. Kim, I., Kobayashi, K., Cho, E. & Zambryski, P. C. Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc. Natl Acad. Sci. USA 102, 11945–11950 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Crawford, K. M. & Zambryski, P. C. Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol. 125, 1802–1812 (2001).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Kim, I., Cho, E., Crawford, K., Hempel, F. D. & Zambryski, P. C. Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc. Natl Acad. Sci. USA 102, 2227–2231 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lee, J.-Y. & Zhou, J. in Short and Long Distance Signaling (eds Kragler, F. & Hülskamp, M.) 61–86 (Springer New York, 2011).

  53. Sessions, A., Yanofsky, M. F. & Weigel, D. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289, 779–782 (2000).

    Article  CAS  PubMed  Google Scholar 

  54. Wu, X. et al. Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130, 3735–3745 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Gallagher, K. L., Paquette, A. J., Nakajima, K. & Benfey, P. N. Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14, 1847–1851 (2004).

    Article  CAS  PubMed  Google Scholar 

  56. Nakajima, K., Sena, G., Nawy, T. & Benfey, P. N. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307–311 (2001).

    Article  CAS  PubMed  Google Scholar 

  57. Vatén, A. et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21, 1144–1155 (2011).

    Article  CAS  PubMed  Google Scholar 

  58. Koizumi, K., Wu, S., MacRae-Crerar, A. & Gallagher, K. L. An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr. Biol. 21, 1559–1564 (2011). One of the first identifications of a cofactor that facilitates the movement of transcription factors through the plasmodesmata.

    Article  CAS  PubMed  Google Scholar 

  59. Harries, P. A., Schoelz, J. E. & Nelson, R. S. Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol. Plant Microbe Interact. 23, 1381–1393 (2010).

    Article  CAS  PubMed  Google Scholar 

  60. Yadav, R. K. et al. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25, 2025–2030 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Palauqui, J. C., Elmayan, T., Pollien, J. M. & Vaucheret, H. Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J. 16, 4738–4745 (1997).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Voinnet, O. & Baulcombe, D. C. Systemic signalling in gene silencing. Nature 389, 553 (1997).

    Article  CAS  PubMed  Google Scholar 

  63. Axtell, M. J., Westholm, J. O. & Lai, E. C. Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 12, 221 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Yoo, B.-C. et al. A systemic small RNA signaling system in plants. Plant Cell 16, 1979–2000 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Dunoyer, P. et al. Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912–916 (2010).

    Article  CAS  PubMed  Google Scholar 

  66. Dunoyer, P. et al. An endogenous, systemic RNAi pathway in plants. EMBO J. 29, 1699–1712 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Brosnan, C. A. & Voinnet, O. Cell-to-cell and long-distance siRNA movement in plants: mechanisms and biological implications. Curr. Opin. Plant Biol. 14, 580–587 (2011).

    Article  CAS  PubMed  Google Scholar 

  68. Himber, C., Dunoyer, P., Moissiard, G., Ritzenthaler, C. & Voinnet, O. Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J. 22, 4523–4533 (2003).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Skopelitis, D. S., Husbands, A. Y. & Timmermans, M. C. P. Plant small RNAs as morphogens. Curr. Opin. Cell Biol. 24, 217–224 (2012).

    Article  CAS  PubMed  Google Scholar 

  70. Carlsbecker, A. et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316–321 (2010). This study identified mobile sRNAs, miR165 and miR166, that are required for specific cell fates in the vasculature.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Miyashima, S., Koi, S., Hashimoto, T. & Nakajima, K. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138, 2303–2313 (2011).

    Article  CAS  PubMed  Google Scholar 

  72. Moussian, B., Schoof, H., Haecker, A., Jürgens, G. & Laux, T. Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J. 17, 1799–1809 (1998).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Tucker, M. R. et al. Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo. Development 135, 2839–2843 (2008).

    Article  CAS  PubMed  Google Scholar 

  74. Liu, Q. et al. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis . Plant J. 58, 27–40 (2009).

    Article  CAS  PubMed  Google Scholar 

  75. Zhu, H. et al. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145, 242–256 (2011). This study identified a unique role for an ARGONAUTE protein, AGO10, which acts as a decoy in the shoot meristem to sequester miR165 and miR166 from the meristem and maintain pluripotency.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Ji, L. et al. ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet. 7, e1001358 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Knauer, S. et al. A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev. Cell 24, 125–132 (2013).

    Article  CAS  PubMed  Google Scholar 

  78. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445 (2005).

    Article  CAS  PubMed  Google Scholar 

  79. Kepinski, S. & Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451 (2005). These two studies reported the identification of TIR1 as the auxin receptor.

    Article  CAS  PubMed  Google Scholar 

  80. Ueguchi Tanaka, M. et al. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437, 693–698 (2005).

    Article  CAS  PubMed  Google Scholar 

  81. Yan, J. et al. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21, 2220–2236 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Fu, Z. Q. et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228–232 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Santner, A., Calderon-Villalobos, L. I. A. & Estelle, M. Plant hormones are versatile chemical regulators of plant growth. Nature Chem. Biol. 5, 301–307 (2009).

    Article  CAS  Google Scholar 

  84. Lumba, S., Cutler, S. & McCourt, P. Plant nuclear hormone receptors: a role for small molecules in protein-protein interactions. Annu. Rev. Cell Dev. Biol. 26, 445–469 (2010).

    Article  CAS  PubMed  Google Scholar 

  85. Santner, A. & Estelle, M. Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071–1078 (2009).

    Article  CAS  PubMed  Google Scholar 

  86. Ljung, K. Auxin metabolism and homeostasis during plant development. Development 140, 943–950 (2013).

    Article  CAS  PubMed  Google Scholar 

  87. Normanly, J. Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb. Perspect. Biol. 2, a001594 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Grieneisen, V. A., Xu, J., Marée, A. F. M., Hogeweg, P. & Scheres, B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449, 1008–1013 (2007).

    Article  CAS  PubMed  Google Scholar 

  89. Petrášek, J. & Friml, J. Auxin transport routes in plant development. Development 136, 2675–2688 (2009).

    Article  CAS  PubMed  Google Scholar 

  90. Wisniewska, J. et al. Polar PIN localization directs auxin flow in plants. Science 312, 883 (2006).

    Article  CAS  PubMed  Google Scholar 

  91. Ljung, K. Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17, 1090–1104 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Petersson, S. V. et al. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21, 1659–1668 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Ludwig-Muller, J. Auxin conjugates: their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757–1773 (2011).

    Article  CAS  PubMed  Google Scholar 

  94. Sairanen, I. et al. Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24, 4907–4916 (2013).

    Article  CAS  Google Scholar 

  95. Staswick, P. E. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol. 150, 1310–1321 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Cooke, T. J., Poli, D., Sztein, A. E. & Cohen, J. D. Evolutionary patterns in auxin action. Plant Mol. Biol. 49, 319–338 (2002).

    Article  CAS  PubMed  Google Scholar 

  97. Dharmasiri, S. et al. AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312, 1218–1220 (2006).

    Article  CAS  PubMed  Google Scholar 

  98. Yang, Y., Hammes, U. Z., Taylor, C. G., Schachtman, D. P. & Nielsen, E. High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123–1127 (2006).

    Article  CAS  PubMed  Google Scholar 

  99. Barbez, E. et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485, 119–122 (2012).

    Article  CAS  PubMed  Google Scholar 

  100. Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 (2003).

    Article  CAS  PubMed  Google Scholar 

  101. Benkova, E., Michniewicz, M., Sauer, M. & Teichmann, T. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003).

    Article  CAS  PubMed  Google Scholar 

  102. Mockaitis, K. & Estelle, M. Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24, 55–80 (2008).

    Article  CAS  PubMed  Google Scholar 

  103. Calderon-Villalobos, L. I., Tan, X., Zheng, N. & Estelle, M. Auxin perception-structural insights. Cold Spring Harb. Perspect. Biol. 2, a005546 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Remington, D. L., Vision, T. J., Guilfoyle, T. J. & Reed, J. W. Contrasting modes of diversification in the Aux/IAA & ARF gene families. Plant Physiol. 135, 1738–1752 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Buchler, N. E. & Louis, M. Molecular titration and ultrasensitivity in regulatory networks. J. Mol. Biol. 384, 1106–1119 (2008).

    Article  CAS  PubMed  Google Scholar 

  106. Cross, F. R. & Buchler, N. E. Protein sequestration generates a flexible ultrasensitive response in a genetic network. Mol. Systems Biol. 5, 272 (2009).

    Article  Google Scholar 

  107. Weijers, D. et al. Auxin Triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10, 265–270 (2006).

    Article  CAS  PubMed  Google Scholar 

  108. Schlereth, A. et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913–916 (2010).

    Article  CAS  PubMed  Google Scholar 

  109. Rademacher, E. H. et al. Different auxin response machineries control distinct cell fates in the early plant embryo. Dev. Cell 22, 211–222 (2012).

    Article  CAS  PubMed  Google Scholar 

  110. Alon, U. Network motifs: theory and experimental approaches. Nature Rev. Genet. 8, 450–461 (2007).

    Article  CAS  PubMed  Google Scholar 

  111. Tiwari, S. B., Hagen, G. & Guilfoyle, T. The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15, 533–543 (2003).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Activation and repression of transcription by auxin-response factors. Proc. Natl Acad. Sci. USA 96, 5844–5849 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Alon, U. An Introduction to Systems Biology — Design Principles of Biological Circuits (Chapman & Hall/CRC Mathematical & Computational Biology, 2006).

    Google Scholar 

  114. Paponov, I. A. et al. Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol. Plant 1, 321–337 (2008).

    Article  CAS  PubMed  Google Scholar 

  115. Hagen, G. & Guilfoyle, T. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373–385 (2002).

    Article  CAS  PubMed  Google Scholar 

  116. Middleton, A. M., King, J. R., Bennett, M. J. & Owen, M. R. Mathematical modelling of the Aux/IAA negative feedback loop. Bull. Math. Biol. 72, 1383–1407 (2010).

    Article  CAS  PubMed  Google Scholar 

  117. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Dimerization and DNA binding of auxin response factors. Plant J. 19, 309–319 (1999).

    Article  CAS  PubMed  Google Scholar 

  118. Cooper, T. F., Morby, A. P., Gunn, A. & Schneider, D. Effect of random and hub gene disruptions on environmental and mutational robustness in Escherichia coli. BMC Genomics 7, 237 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Masel, J. & Siegal, M. L. Robustness: mechanisms and consequences. Trends Genet. 25, 395–403 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Hill, A. V. The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J. Physiol. 40, 1–7 (1910).

    Article  Google Scholar 

  121. Hill, A. V. The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J. Physiol. 40, 1–7 (1910).

    Article  Google Scholar 

  122. Chen, H., Xu, Z., Mei, C., Yu, D. & Small, S. A. System of repressor gradients spatially organizes the boundaries of bicoid-dependent target genes. Cell 149, 618–629 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Turing, A. M. The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B 237, 37–72 (1952).

    Article  Google Scholar 

  124. Matsubayashi, Y. & Sakagami, Y. Peptide hormones in plants. Annu. Rev. Plant Biol. 57, 649–674 (2006).

    Article  CAS  PubMed  Google Scholar 

  125. Lubeck, E. & Cai, L. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nature Methods 9, 743–748 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Sachs, J. Handbuch der experimental-physiologie der Pflanzen: Untersuchungen uber die allgemeinen Lebensbedingungen er Pflanzen und die Functionen ihrer Organe. (W. Engelmann, 1865) (in German).

    Book  Google Scholar 

  127. Garner, W. W. & Allard, H. A. Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. Mon. Wea. Rev. 48, 415–415 (1920).

    Article  Google Scholar 

  128. Melchers, G. Die Wirkung von Genen, tiefen Temperaturen und blühenden Propfpartnern auf die Blühreife von Hyoscyamus. Biol. Zbl. 57, 568–614 (in German) (1937) .

    Google Scholar 

  129. Chailakhyan, M. K. About the mechanism of the photoperiodic response. Dokl. Akad. Nauk SSSR 1, 85–89 (in Russian) (1936).

    Google Scholar 

  130. Chailakhyan, M. K. New facts supporting the hormonal theory of plant development. Dokl. Akad. Nauk SSSR 4, 77–81 (in Russian) (1936).

    Google Scholar 

  131. Chailakhyan, M. K. in Hormonal Theory of Plant Development. 198 (Bull. Acad. Sci. U.R.S.S.,1937) (in Russian).

    Google Scholar 

  132. Zeevaart, J. A. D. Flower Formation As Studied By Grafting. (H. Veenman, 1958).

    Google Scholar 

  133. Lang, A. Physiology of flowering. Annu. Rev. Plant Physiol. 3, 265–306 (1952).

    Article  Google Scholar 

  134. Lifschitz, E. et al. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl Acad. Sci. USA 103, 6398–6403 (2006). This study made the first correlation between tomato SINGLE FLOWER TRUSS (SFT; the orthologue of FLOWERING LOCUS T in A. thaliana ) and the florigen signal originating from the leaf.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Notaguchi, M. et al. Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol. 49, 1645–1658 (2008).

    Article  PubMed  Google Scholar 

  136. Corbesier, L. et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030–1033 (2007).

    Article  CAS  PubMed  Google Scholar 

  137. Lin, M. K. et al. FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19, 1488–1506 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Tamaki, S., Matsuo, S., Wong, H. L., Yokoi, S. & Shimamoto, K. Hd3a protein is a mobile flowering signal in rice. Science 316, 1033–1036 (2007).

    Article  CAS  PubMed  Google Scholar 

  139. Shalit, A. et al. The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc. Natl Acad. Sci. USA 106, 8392–8397 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  140. Kehr, J. in Short and Long Distance Signaling (eds Kragler, F. & Hülskamp, M.) 131–149 (Springer, 2011).

    Google Scholar 

  141. Ruiz-Medrano, R., Kragler, F. & Wolf, S. in Short and Long Distance Signaling (eds Kragler, F. & Hülskamp, M.) 151–177 (Springer, 2011).

    Google Scholar 

  142. Molnar, A. et al. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872–875 (2010).

    Article  CAS  PubMed  Google Scholar 

  143. Buhtz, A., Pieritz, J., Springer, F. & Kehr, J. Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol. 10, 64 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

Work in the Benfey laboratory is funded by the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3405) to P.N.B., as well as by grants from the US National Institutes of Health (R01-GM043778), the US National Science Foundation and the Defense Advanced Research Projects Agency.

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Glossary

Phytohormones

Signal molecules produced in plants that elicit diverse effects depending on context.

Meristems

Groups of dividing cells (in the root and shoot), which include the stem cells that give rise to new tissues and organs.

Organizing centre

A group of meristem cells in the shoot that have low mitotic activity and that are required for the maintenance of the stem cells.

Quiescent centre

A group of meristem cells in the root that have low mitotic activity and that are required for maintenance of the stem cells.

Initial cells

Progenitor cells of a tissue or an organ.

Cell wall

A structure composed of cellulose, hemicellulose and pectin that surrounds plant cells (and some other organisms such as fungi), contributes towards the overall firmness of the organism and prevents cellular movement.

Kinase-dead

Contains a kinase domain identified by its sequence, but without kinase activity; that is, the ability to add phosphate to a substrate.

Morphogen

A signal gradient that has a single source that results in differential output (that is, cell fate) as a readout of the local concentration.

Florigen

A universal mobile signal, originating from leaves, that is necessary for the initiation of flowering in plants.

Hypophysis

The most proximal cell of the suspensor that will initiate the columella and quiescent centre.

Suspensor

A cell population that connects the embryo proper to the endosperm feeding tissue. It forms as a result of asymmetric division of the zygote and functions similarly to the placenta in animals.

Feedforward loops

(FFLs). Gene network motifs in which a protein, X (usually a transcription factor), regulates a target gene, Z, directly as well as indirectly through another regulator, Y. The input of X and Y can be either positive or negative. X and Y might both be required (AND gate) or either one might be sufficient on its own (OR gate).

Hill function

A function used in biochemistry to describe cooperative binding. It usually reflects the enhanced efficiency of ligand binding as a result of other ligand molecules that are already bound to a receptor.

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Sparks, E., Wachsman, G. & Benfey, P. Spatiotemporal signalling in plant development. Nat Rev Genet 14, 631–644 (2013). https://doi.org/10.1038/nrg3541

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