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Intercellular Signaling During Floral Development

  • Balaji Enugutti
  • Kay Schneitz
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 14)

Abstract

Flowers are central to sexual reproduction in higher plants and during evolution floral organs have acquired diverse morphologies to aid in this process. Cells need to communicate to allow floral morphogenesis to happen. The flow of information between plant cells occurs through signaling mechanisms that involve cell surface receptors, cell wall diffusible factors, and plasmodesmata. Transcription factors and small RNAs are now known to move between floral cells to regulate cell identity and morphogenesis. A growing number of cell surface receptor-like kinases have been identified that play a role in intercellular communication in the floral meristem (FM), the specification of the male germline, and the formation of the ovule integuments. In this chapter, we highlight some of the progress that has been made toward an understanding of these types of signaling mechanisms.

Keywords

Green Fluorescent Protein Floral Organ Shoot Apical Meristem Intercellular Communication Floral Meristem 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank members of our lab for fruitful discussions. We apologize to colleagues whose work we could not cite due to space restrictions. Work on signaling in floral organs in the Schneitz lab is funded by grants SCHN 723/1-3, SCHN 723/3-2, and SCHN 723/6-1 from the German Research Council (DFG) and by the Free State of Bavaria.

References

  1. Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouche N, Gasciolli V, Vaucheret H (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16:927–932PubMedCrossRefGoogle Scholar
  2. Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17:3337–3349PubMedCrossRefGoogle Scholar
  3. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013PubMedCrossRefGoogle Scholar
  4. Becraft PW, Stinard PS, McCarty DR (1996) CRINCLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409PubMedCrossRefGoogle Scholar
  5. Becraft PW, Kang SH, Suh SG (2001) The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol 127:486–496PubMedCrossRefGoogle Scholar
  6. Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152:166–176PubMedCrossRefGoogle Scholar
  7. Boudeau J, Miranda-Saavedra D, Barton GJ, Alessi DR (2006) Emerging roles of pseudokinases. Trends Cell Biol 16:443–452PubMedCrossRefGoogle Scholar
  8. Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996) Control of inforescence architecture in Antirrhinum. Nature 379:791–797PubMedCrossRefGoogle Scholar
  9. Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83PubMedCrossRefGoogle Scholar
  10. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619PubMedCrossRefGoogle Scholar
  11. Breuninger H, Lenhard M (2010) Control of tissue and organ growth in plants. Curr Top Dev Biol 91:185–220PubMedCrossRefGoogle Scholar
  12. Busch W, Miotk A, Ariel FD, Zhao Z, Forner J, Daum G, Suzaki T, Schuster C, Schultheiss SJ, Leibfried A, Haubeiss S, Ha N, Chan RL, Lohmann JU (2010) Transcriptional control of a plant stem cell niche. Dev Cell 18:849–861PubMedCrossRefGoogle Scholar
  13. Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727PubMedCrossRefGoogle Scholar
  14. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321PubMedCrossRefGoogle Scholar
  15. Carpenter R, Coen ES (1995) Transposon induced chimeras show that floricaula, a meristem identity gene, acts non-autonomously between cell layers. Development 121:19–26PubMedGoogle Scholar
  16. Cartolano M, Efremova N, Kuckenberg M, Raman S, Schwarz-Sommer Z (2009) Enhanced AGAMOUS expression in the centre of the Arabidopsis flower causes ectopic expression over its outer expression boundaries. Planta 230:857–862PubMedCrossRefGoogle Scholar
  17. Castells E, Casacuberta JM (2007) Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants. J Exp Bot 58:3503–3511PubMedCrossRefGoogle Scholar
  18. Causier B, Schwarz-Sommer Z, Davies B (2010) Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 21:73–79PubMedCrossRefGoogle Scholar
  19. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896PubMedCrossRefGoogle Scholar
  20. Chapman LA, Goring DR (2010) Pollen-pistil interactions regulating successful fertilization in the Brassicaceae. J Exp Bot 61:1987–1999PubMedCrossRefGoogle Scholar
  21. Chevalier D, Batoux M, Fulton L, Pfister K, Yadav RK, Schellenberg M, Schneitz K (2005) STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc Natl Acad Sci USA 102:9074–9079PubMedCrossRefGoogle Scholar
  22. Chitwood DH, Timmermans MC (2010) Small RNAs are on the move. Nature 467:415–419PubMedCrossRefGoogle Scholar
  23. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554PubMedCrossRefGoogle Scholar
  24. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585PubMedCrossRefGoogle Scholar
  25. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedCrossRefGoogle Scholar
  26. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361PubMedCrossRefGoogle Scholar
  27. Conti L, Bradley D (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19:767–778PubMedCrossRefGoogle Scholar
  28. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033PubMedCrossRefGoogle Scholar
  29. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425PubMedCrossRefGoogle Scholar
  30. de Felippes FF, Ott F, Weigel D (2011) Comparative analysis of non-autonomous effects of tasiRNAs and miRNAs in Arabidopsis thaliana. Nucleic Acids Res 39:2880–2889PubMedCrossRefGoogle Scholar
  31. De Smet I, Voß U, Jürgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173PubMedCrossRefGoogle Scholar
  32. DeYoung BJ, Clark S (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180:895–904PubMedCrossRefGoogle Scholar
  33. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16PubMedCrossRefGoogle Scholar
  34. Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002PubMedCrossRefGoogle Scholar
  35. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912–916PubMedCrossRefGoogle Scholar
  36. Efremova N, Perbal MC, Yephremov A, Hofmann WA, Saedler H, Schwarz-Sommer Z (2001) Epidermal control of floral organ identity by class B homeotic genes in Antirrhinum and Arabidopsis. Development 128:2661–2671PubMedGoogle Scholar
  37. Ehlers K, Kollmann R (2001) Primary and secondary plasmodesmata: structure, origin, and functioning. Protoplasma 216:1–30PubMedCrossRefGoogle Scholar
  38. Feng X, Dickinson HG (2007) Packaging the male germline in plants. Trends Genet 23:503–510PubMedCrossRefGoogle Scholar
  39. Feng X, Dickinson HG (2010a) Cell–cell interactions during patterning of the Arabidopsis anther. Biochem Soc Trans 38:571–576PubMedCrossRefGoogle Scholar
  40. Feng X, Dickinson HG (2010b) Tapetal cell fate, lineage and proliferation in the Arabidopsis anther. Development 137:2409–2416PubMedCrossRefGoogle Scholar
  41. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914PubMedCrossRefGoogle Scholar
  42. Fulton L, Batoux M, Vaddepalli P, Yadav RK, Busch W, Andersen SU, Jeong S, Lohmann JU, Schneitz K (2009) DETORQUEO, QUIRKY, and ZERZAUST represent novel components involved in organ development mediated by the receptor-like kinase STRUBBELIG in Arabidopsis thaliana. PLoS Genet 5:e1000355PubMedCrossRefGoogle Scholar
  43. Gagne JM, Clark SE (2010) The Arabidopsis stem cell factor POLTERGEIST is membrane localized and phospholipid stimulated. Plant Cell 22:729–743PubMedCrossRefGoogle Scholar
  44. Gifford ML, Dean S, Ingram GC (2003) The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development 130:4249–4258PubMedCrossRefGoogle Scholar
  45. Gifford ML, Robertson FC, Soares DC, Ingram GC (2005) ARABIDOPSIS CRINKLY4 function, internalization, and turnover are dependent on the extracellular crinkly repeat domain. Plant Cell 17:1154–1166PubMedCrossRefGoogle Scholar
  46. Gisel A, Barella S, Hempel FD, Zambryski PC (1999) Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126:1879–1889PubMedGoogle Scholar
  47. Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66:117–127PubMedCrossRefGoogle Scholar
  48. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA 106:16529–16534PubMedCrossRefGoogle Scholar
  49. Gross-Hardt R, Lenhard M, Laux T (2002) WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes Dev 16:1129–1138PubMedCrossRefGoogle Scholar
  50. Guo Y, Han L, Hymes M, Denver R, Clark SE (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J 63:889–900PubMedCrossRefGoogle Scholar
  51. Hématy K, Höfte H (2008) Novel receptor kinases involved in growth regulation. Curr Opin Plant Biol 11:321–328PubMedCrossRefGoogle Scholar
  52. Hord CL, Chen C, Deyoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–1680PubMedCrossRefGoogle Scholar
  53. Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997PubMedCrossRefGoogle Scholar
  54. Jackson D (2002) Double labeling of KNOTTED1 mRNA and protein reveals multiple potential sites of protein trafficking in the shoot apex. Plant Physiol 129:1423–1429PubMedCrossRefGoogle Scholar
  55. Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054PubMedCrossRefGoogle Scholar
  56. Jenik PD, Irish VF (2000) Regulation of cell proliferation patterns by homeotic genes during Arabidopsis floral development. Development 127:1267–1276PubMedGoogle Scholar
  57. Jenik PD, Irish VF (2001) The Arabidopsis floral homeotic gene APETALA3 differentially regulates intercellular signaling required for petal and stamen development. Development 128:13–23PubMedGoogle Scholar
  58. Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–1934PubMedGoogle Scholar
  59. Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci USA 105:2220–2225PubMedCrossRefGoogle Scholar
  60. Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851PubMedGoogle Scholar
  61. Kim JY (2005) Regulation of short-distance transport of RNA and protein. Curr Opin Plant Biol 8:45–52PubMedCrossRefGoogle Scholar
  62. Kinoshita T, Caño-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171PubMedCrossRefGoogle Scholar
  63. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–3920PubMedCrossRefGoogle Scholar
  64. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845–848PubMedCrossRefGoogle Scholar
  65. Kroiher M, Miller MA, Steele RE (2001) Deceiving appearances: signaling by “dead” and “fractured” receptor protein-tyrosine kinases. Bioessays 23:69–76PubMedCrossRefGoogle Scholar
  66. Kwak SH, Shen R, Schiefelbein J (2005) Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307:1111–1113PubMedCrossRefGoogle Scholar
  67. Leibfried A, To JP, Busch W, Stehling S, Kehle A, Demar M, Kieber JJ, Lohmann JU (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:1172–1175PubMedCrossRefGoogle Scholar
  68. Lenhard M, Bohnert A, Jürgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814PubMedCrossRefGoogle Scholar
  69. Li JM, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938PubMedCrossRefGoogle Scholar
  70. Lohmann JU, Hong RL, Hobe M, Busch M, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803PubMedCrossRefGoogle Scholar
  71. Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–1983PubMedCrossRefGoogle Scholar
  72. Lucas WJ, Ham BK, Kim JY (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503PubMedCrossRefGoogle Scholar
  73. Ma H, Sundaresan V (2010) Development of flowering plant gametophytes. Curr Top Dev Biol 91:379–412PubMedCrossRefGoogle Scholar
  74. Mathieu J, Warthmann N, Kuttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055–1060PubMedCrossRefGoogle Scholar
  75. Mayer FX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815PubMedCrossRefGoogle Scholar
  76. Melzer R, Wang YQ, Theissen G (2010) The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Semin Cell Dev Biol 21:118–128PubMedCrossRefGoogle Scholar
  77. Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S (2008) The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol 49:1752–1757PubMedCrossRefGoogle Scholar
  78. Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J 50:751–766PubMedCrossRefGoogle Scholar
  79. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–875PubMedCrossRefGoogle Scholar
  80. Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–946PubMedCrossRefGoogle Scholar
  81. Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311PubMedCrossRefGoogle Scholar
  82. Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1739PubMedCrossRefGoogle Scholar
  83. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294PubMedCrossRefGoogle Scholar
  84. Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632PubMedCrossRefGoogle Scholar
  85. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/i are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379PubMedCrossRefGoogle Scholar
  86. Perbal MC, Haughn G, Saedler H, Schwarz-Sommer Z (1996) Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122:3433–3441PubMedGoogle Scholar
  87. Reinhardt D, Frenz M, Mandel T, Kuhlemeier C (2003) Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem. Development 130:4073–4083PubMedCrossRefGoogle Scholar
  88. Rinne PL, van der Schoot C (1998) Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125:1477–1485PubMedGoogle Scholar
  89. Rinne PL, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J 26:249–264PubMedCrossRefGoogle Scholar
  90. Satina S, Blakeslee AF, Avery AG (1940) Demonstration of the three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras. Am J Bot 27:895–905CrossRefGoogle Scholar
  91. Savaldi-Goldstein S, Peto C, Chory J (2007) The epidermis both drives and restricts plant shoot growth. Nature 446:199–202PubMedCrossRefGoogle Scholar
  92. Schneitz K, Hülskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7:731–749CrossRefGoogle Scholar
  93. Schoof H, Lenhard M, Haecker A, Mayer KFX, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644PubMedCrossRefGoogle Scholar
  94. Sessions A, Yanofsky MF, Weigel D (2000) Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–781PubMedCrossRefGoogle Scholar
  95. Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768PubMedCrossRefGoogle Scholar
  96. Sieber P, Gheyeselinck J, Gross-Hardt R, Laux T, Grossniklaus U, Schneitz K (2004) Pattern formation during early ovule development in Arabidopsis thaliana. Dev Biol 273:321–334PubMedCrossRefGoogle Scholar
  97. Sieburth LE, Drews GN, Meyerowitz EM (1998) Non-autonomy of AGAMOUS function in flower development: use of a Cre/loxP method for mosaic analysis in Arabidopsis. Development 125:4303–4312PubMedGoogle Scholar
  98. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472PubMedCrossRefGoogle Scholar
  99. Steinwand BJ, Kieber JJ (2010) The role of receptor-like kinases in regulating cell wall function. Plant Physiol 153:479–484PubMedCrossRefGoogle Scholar
  100. Sundberg E, Ostergaard L (2009) Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb Perspect Biol 1:a001628PubMedCrossRefGoogle Scholar
  101. Szymkowiak EJ, Sussex IM (1992) The internal meristem layer (L3) determines floral meristem size and carpel number in tomato periclinal chimeras. Plant Cell 4:1089–1100PubMedGoogle Scholar
  102. Szymkowiak EJ, Sussex IM (1996) What chimeras can tell us about plant development. Annu Rev Plant Physiol Plant Mol Biol 47:351–376PubMedCrossRefGoogle Scholar
  103. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036PubMedCrossRefGoogle Scholar
  104. Tanaka H, Watanabe M, Sasabe M, Hiroe T, Tanaka T, Tsukaya H, Ikezaki M, Machida C, Machida Y (2007) Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development 134:1643–1652PubMedCrossRefGoogle Scholar
  105. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8:735–746PubMedGoogle Scholar
  106. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594PubMedCrossRefGoogle Scholar
  107. Urbanus SL, de Folter S, Shchennikova AV, Kaufmann K, Immink RG, Angenent GC (2009) In planta localisation patterns of MADS domain proteins during floral development in Arabidopsis thaliana. BMC Plant Biol 9:5PubMedCrossRefGoogle Scholar
  108. Urbanus SL, Martinelli AP, Dinh QD, Aizza LC, Dornelas MC, Angenent GC, Immink RG (2010) Intercellular transport of epidermis-expressed MADS domain transcription factors and their effect on plant morphology and floral transition. Plant J 63:60–72PubMedGoogle Scholar
  109. Vaddepalli P, Fulton L, Batoux M, Yadav RK, Schneitz K (2011) Structure-function analysis of STRUBBELIG, an Arabidopsis atypical receptor-like kinase involved in tissue morphogenesis. PLoS One 6:e19730PubMedCrossRefGoogle Scholar
  110. Van Norman JM, Breakfield NW, Benfey PN (2011) Intercellular communication during plant development. Plant Cell 23:855–864PubMedCrossRefGoogle Scholar
  111. Vincent CA, Carpenter R, Coen ES (2003) Interactions between gene activity and cell layers during floral development. Plant J 33:765–774PubMedCrossRefGoogle Scholar
  112. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687PubMedCrossRefGoogle Scholar
  113. Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y (2004) The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J 39:298–308PubMedCrossRefGoogle Scholar
  114. Werner D, Gerlitz N, Stadler R (2010) A dual switch in phloem unloading during ovule development in Arabidopsis. Protoplasma 248:225–235PubMedCrossRefGoogle Scholar
  115. Wollmann H, Mica E, Todesco M, Long JA, Weigel D (2010) On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137:3633–3642PubMedCrossRefGoogle Scholar
  116. Wu X, Dinneny JR, Crawford KM, Rhee Y, Citovsky V, Zambryski PC, Weigel D (2003) Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130:3735–3745PubMedCrossRefGoogle Scholar
  117. Xu SL, Rahman A, Baskin TI, Kieber JJ (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20:3065–3079PubMedCrossRefGoogle Scholar
  118. Yadav RK, Fulton L, Batoux M, Schneitz K (2008) The Arabidopsis receptor-like kinase STRUBBELIG mediates inter-cell-layer signaling during floral development. Dev Biol 323:261–270PubMedCrossRefGoogle Scholar
  119. Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804PubMedCrossRefGoogle Scholar
  120. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39PubMedCrossRefGoogle Scholar
  121. Yu LP, Miller AK, Clark SE (2003) POLTERGEIST encodes a protein phosphatase 2 C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Curr Biol 13:179–188PubMedCrossRefGoogle Scholar
  122. Zeevaart JAD (1976) Physiology of flower formation. Annu Rev Plant Physiol 27:321–348CrossRefGoogle Scholar
  123. Zhao DZ, Wang GF, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031PubMedCrossRefGoogle Scholar
  124. Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Herve P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54:375–387PubMedCrossRefGoogle Scholar
  125. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092PubMedCrossRefGoogle Scholar
  126. Zhu Y, Wang Y, Li R, Song X, Wang Q, Huang S, Jin J, Liu C, Lin J (2010) Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J 61:223–233PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Entwicklungsbiologie der Pflanzen, Wissenschaftszentrum WeihenstephanTechnische Universität MünchenFreisingGermany

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