Spatiotemporal signalling in plant development

Nature Reviews Genetics

Volumn 14, Issue 9, 2013, Pages 631-644

  Sparks, Erin ^a   Wachsman, Guy ^a   Benfey, Philip N ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; DOUBLE STRANDED RNA; MICRORNA; PHYTOHORMONE; SINGLE STRANDED RNA; SMALL INTERFERING RNA; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR;

APICAL MERISTEM; AUXIN TRANSPORT; CELL DIFFERENTIATION; CELL PROLIFERATION; ENDOPLASMIC RETICULUM; METABOLISM; PLANT DEVELOPMENT; PLANT GENE; PLANT STRUCTURES; PRIORITY JOURNAL; REVIEW; SHOOT; SIGNAL TRANSDUCTION; SMALL RIBOSOMAL SUBUNIT;

GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; MICRORNAS; PEPTIDES; PLANT DEVELOPMENT; PLANT GROWTH REGULATORS; PLANTS; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84882298592     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3541     Document Type: Review

References (143)

1. Bradshaww, A. D. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13, 115-155 (1965).
2. Lease, K. A. & Walker, J. C. The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol. 142, 831-838 (2006).
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).
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).
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).
6. Shiu, S.-H. & Bleecker, A. B. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. Signal. 2001, re22 (2001).
7. Torii, K. U. Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int. Rev. Cytol. 234, 1-46 (2004).
8. Cock, J. M. & McCormick, S. A large family of genes that share homology with CLAVATA3. Plant Physiol. 126, 939-942 (2001).
9. Oelkers, K. et al. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 8, 1 (2008).
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).
11. Fletcher, J. C. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911-1914 (1999).
12. Ogawa, M., Shinohara, H., Sakagami, Y. & Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294-294 (2008).
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).
14. Kinoshita, A. et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911-3920 (2010).
15. Kayes, J. M. & Clark, S. E. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125, 3843-3851 (1998).
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).
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).
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).
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).
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).
21. Mayer, K. F. et al. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815 (1998).
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).
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).
24. Brandman, O. & Meyer, T. Feedback loops shape cellular signals in space and time. Science 322, 390-395 (2008).
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).
26. Reddy, G. V. Live-imaging stem-cell homeostasis in the Arabidopsis shoot apex. Curr. Opin. Plant Biol. 11, 88-93 (2008).
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).
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).
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).
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).
31. Haecker, A. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131, 657-668 (2004).
32. Sarkar, A. K. et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811-814 (2007).
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).
34. Hobe, M., Müller, 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).
35. Stahl, Y. et al. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23, 362-371 (2013).
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).
37. Meng, L., Buchanan, B. B., Feldman, L. J. & Luan, 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).
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).
39. Moore, K. L. The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278, 24243-24246 (2003).
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).
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).
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).
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).
44. Lucas, W. J. et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980-1983 (1995).
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).
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).
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).
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).
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).
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).
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).
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).
54. Wu, X. et al. Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130, 3735-3745 (2003).
55. Gallagher, K. L., Paquette, A. J., Nakajima, K. & Benfey, P. N. Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14, 1847-1851 (2004).
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).
57. Vatén, A. et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21, 1144-1155 (2011).
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).
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).
60. Yadav, R. K. et al. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25, 2025-2030 (2011).
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).
62. Voinnet, O. & Baulcombe, D. C. Systemic signalling in gene silencing. Nature 389, 553 (1997).
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).
64. Yoo, B.-C. et al. A systemic small RNA signaling system in plants. Plant Cell 16, 1979-2000 (2004).
65. Dunoyer, P. et al. Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912-916 (2010).
66. Dunoyer, P. et al. An endogenous, systemic RNAi pathway in plants. EMBO J. 29, 1699-1712 (2010).
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).
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).
69. Skopelitis, D. S., Husbands, A. Y. & Timmermans, M. C. P. Plant small RNAs as morphogens. Curr. Opin. Cell Biol. 24, 217-224 (2012).
70. Carlsbecker, A. et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316-321 (2010).
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).
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).
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).
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).
75. Zhu, H. et al. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145, 242-256 (2011).
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).
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).
78. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445 (2005).
79. Kepinski, S. & Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451 (2005).
80. Ueguchi Tanaka, M. et al. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437, 693-698 (2005).
81. Yan, J. et al. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21, 2220-2236 (2009).
82. Fu, Z. Q. et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228-232 (2012).
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).
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).
85. Santner, A. & Estelle, M. Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071-1078 (2009).
86. Ljung, K. Auxin metabolism and homeostasis during plant development. Development 140, 943-950 (2013).
87. Normanly, J. Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb. Perspect. Biol. 2, a001594 (2010).
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).
89. Petrášek, J. & Friml, J. Auxin transport routes in plant development. Development 136, 2675-2688 (2009).
90. Wisniewska, J. et al. Polar PIN localization directs auxin flow in plants. Science 312, 883 (2006).
91. Ljung, K. Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17, 1090-1104 (2005).
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).
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).
94. Sairanen, I. et al. Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24, 4907-4916 (2013).
95. Staswick, P. E. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol. 150, 1310-1321 (2009).
96. Cooke, T. J., Poli, D., Sztein, A. E. & Cohen, J. D. Evolutionary patterns in auxin action. Plant Mol. Biol. 49, 319-338 (2002).
97. Dharmasiri, S. et al. AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312, 1218-1220 (2006).
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).
99. Barbez, E. et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485, 119-122 (2012).
100. Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147-153 (2003).
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).
102. Mockaitis, K. & Estelle, M. Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24, 55-80 (2008).
103. Calderon-Villalobos, L. I., Tan, X., Zheng, N. & Estelle, M. Auxin perception-structural insights. Cold Spring Harb. Perspect. Biol. 2, a005546 (2010).
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).
105. Buchler, N. E. & Louis, M. Molecular titration and ultrasensitivity in regulatory networks. J. Mol. Biol. 384, 1106-1119 (2008).
106. Cross, F. R. & Buchler, N. E. Protein sequestration generates a flexible ultrasensitive response in a genetic network. Mol. Systems Biol. 5, 272 (2009).
107. Weijers, D. et al. Auxin Triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10, 265-270 (2006).
108. Schlereth, A. et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913-916 (2010).
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).
110. Alon, U. Network motifs: theory and experimental approaches. Nature Rev. Genet. 8, 450-461 (2007).
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).
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).
113. Alon, U. An Introduction to Systems Biology - Design Principles of Biological Circuits (Chapman & Hall/CRC Mathematical & Computational Biology, 2006).
114. Paponov, I. A. et al. Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol. Plant 1, 321-337 (2008).
115. Hagen, G. & Guilfoyle, T. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373-385 (2002).
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).
117. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Dimerization and DNA binding of auxin response factors. Plant J. 19, 309-319 (1999).
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).
119. Masel, J. & Siegal, ML. Robustness: mechanisms and consequences. Trends Genet. 25, 395-403 (2009).
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).
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).
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).
123. Turing, A. M. The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B 237, 37-72 (1952).
124. Matsubayashi, Y. & Sakagami, Y. Peptide hormones in plants. Annu. Rev. Plant Biol. 57, 649-674 (2006).
125. Lubeck, E. & Cai, L. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nature Methods 9, 743-748 (2012).
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).
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).
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).
129. Chailakhyan, M. K. About the mechanism of the photoperiodic response. Dokl. Akad. Nauk SSSR 1, 85-89 (in Russian) (1936).
130. Chailakhyan, M. K. New facts supporting the hormonal theory of plant development. Dokl. Akad. Nauk SSSR 4, 77-81 (in Russian) (1936).
131. Chailakhyan, M. K. in Hormonal Theory of Plant Development. 198 (Bull. Acad. Sci. U.R.S.S.,1937) (in Russian).
132. Zeevaart, J. A. D. Flower Formation As Studied By Grafting. (H. Veenman, 1958).
133. Lang, A. Physiology of flowering. Annu. Rev. Plant Physiol. 3, 265-306 (1952).
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).
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).
136. Corbesier, L. et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033 (2007).
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).
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).
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).
140. Kehr, J. in Short and Long Distance Signaling (eds Kragler, F. & Hülskamp, M.) 131-149 (Springer, 2011).
141. Ruiz-Medrano, R., Kragler, F. & Wolf, S. in Short and Long Distance Signaling (eds Kragler, F. & Hülskamp, M.) 151-177 (Springer, 2011).
142. Molnar, A. et al. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872-875 (2010).
143. Buhtz, A., Pieritz, J., Springer, F. & Kehr, J. Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol. 10, 64 (2010).