The Social Network: Receptor Kinases and Cell Fate Determination in Plants

  • Anthony Bryan
  • Adriana Racolta
  • Frans Tax
  • Sarah Liljegren
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 13)

Abstract

Cell signaling plays a key role in the determination of cell fate in plants. In many developmental processes, receptor kinases have been identified as necessary for the formation of specific cell types. Many receptor kinase mutants with similar phenotypes have been characterized, and there is abundant experimental evidence for genetic redundancy. In addition, multiple examples of potentially sequential or parallel pathways have been uncovered. In a few instances, mutations in different receptor kinases cause opposite phenotypes. Taken together, these results imply that networks of receptor kinases, rather than single receptors, are necessary for cells to understand their postions with respect to other cells and ultimately to make decisions about their roles. In most cases, it is not yet clear whether receptor kinase networks are characterized by physical interactions between the kinases, by parallel pathways, by receptor kinases controling the localization of other receptor kinases, or by other as yet uncharacterized regulatory mechanisms. Some of the same receptor kinases function in multiple developmental processes and cell types, implying that these networks may be reiterative during development. In this chapter, we will focus on receptor kinase mediated mechanisms that establish and maintain cell fates in two broad contexts: (1) the determination of radial identity, particularly epidermal cell fate and the radial layers of the anther and (2) activation of cell separation within organ abscission zones, an enactment of cell fate that also spans radial layers.

References

  1. Abe M, Takahashi T, Komeda Y (2001) Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. Plant J 26:487–494PubMedCrossRefGoogle Scholar
  2. Abe M, Katsumata H, Komeda Y, Takahashi T (2003) Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130:635–643PubMedCrossRefGoogle Scholar
  3. 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
  4. Baroux C, Blanvillain R, Moore IR, Gallois P (2001) Transactivation of BARNASE under the AtLTP1 promoter affects the basal pole of the embryo and shoot development of the adult plant in Arabidopsis. Plant J 28:503–515PubMedCrossRefGoogle Scholar
  5. Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409PubMedCrossRefGoogle Scholar
  6. Bernhardt C, Zhao M, Gonzalez A, Lloyd A, Schiefelbein J (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132:291–298PubMedCrossRefGoogle Scholar
  7. Binder BM, Patterson SE (2009) Ethylene-dependent and -independent regulation of abscission. Stewart Postharv Rev 5:1–10CrossRefGoogle Scholar
  8. Bleecker AB, Patterson SE (1997) Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9:1169–1179PubMedCrossRefGoogle Scholar
  9. Burr CB, Leslie ME, Orlowski SK, Chen I, Wright CE, Daniels MJ, Liljegren SJ (2011) CAST AWAY, a membrane-associated receptor kinase, inhibits organ abscission in Arabidopsis. Plant Physiol 156:1837–1850Google Scholar
  10. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, Aalen RB (2003) INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15:2296–2307PubMedCrossRefGoogle Scholar
  11. 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
  12. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng J-C, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351PubMedCrossRefGoogle Scholar
  13. 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
  14. Cho SK, Larue CT, Chevalier D, Wang H, Jinn T-L, Zhang S, Walker JC (2008) Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:15629–15634PubMedCrossRefGoogle Scholar
  15. Choe S, Noguchi T, Fujioka S, Takatsuto S, Tissier CP, Gregory BD, Ross AS, Tanaka A, Yoshida S, Tax FE, Feldmann KA (1999) The Arabidopsis dwf7/ste1 mutant is defective in the Δ7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11:207–222PubMedCrossRefGoogle Scholar
  16. Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451PubMedCrossRefGoogle Scholar
  17. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedCrossRefGoogle Scholar
  18. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361PubMedCrossRefGoogle Scholar
  19. 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
  20. DeYoung BJ, Clark SE (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180:895–904Google Scholar
  21. Di Cristina M, Sessa G, Dolan L, Linstead P, Baima S, Ruberti I, Morelli G (1996) The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10:393–402PubMedCrossRefGoogle Scholar
  22. Dolan L, Janmaat K, Willemsin V, Linstead P, Poethig S, Roberts K, Sheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84PubMedGoogle Scholar
  23. Feng X, Dickinson HG (2010) Tapetal cell fate, lineage and proliferation in the Arabidopsis anther. Development 137:2409–2416PubMedCrossRefGoogle Scholar
  24. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153PubMedCrossRefGoogle Scholar
  25. Galway ME, Masucci JD, Lloyd AM, Walbot V, Davis RW, Schiefelbein JW (1994) The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166:740–754PubMedCrossRefGoogle Scholar
  26. Ge X, Chang F, Ma H (2010) Signaling and transcriptional control of reproductive development in Arabidopsis. Curr Biol 20:R988–R997PubMedCrossRefGoogle Scholar
  27. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229PubMedCrossRefGoogle Scholar
  28. González-García M-P, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-García S, Russinova E, Caño-Delgado AI (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138:849–859PubMedCrossRefGoogle Scholar
  29. Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848PubMedCrossRefGoogle Scholar
  30. Hord CLH, 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
  31. Hord CLH, Yu-Jin Sun Y-J, Pillitteri LJ, Torii KU, Wang H, Zhang S, Ma H (2008) Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol Plant 1:645–658PubMedCrossRefGoogle Scholar
  32. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386PubMedCrossRefGoogle Scholar
  33. 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
  34. Jinn TL, Stone JM, Walker JC (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108–117PubMedGoogle Scholar
  35. Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7:e1000090PubMedCrossRefGoogle Scholar
  36. Kuppusamy KT, Chen AY, Nemhauser JL (2009) Steroids are required for epidermal cell fate establishment in Arabidopsis roots. Proc Natl Acad Sci USA 106:8073–8076PubMedCrossRefGoogle Scholar
  37. 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 433:167–171Google Scholar
  38. Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, Nagasaka R, Tominaga R, Koshino-Kimura Y, Kato T et al (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132:5387–5398PubMedCrossRefGoogle Scholar
  39. Kwak S-H, Schiefelbein J (2008) A feedback mechanism controlling SCRAMBLED receptor accumulation and cell-type pattern in Arabidopsis. Curr Biol 18:1949–1954PubMedCrossRefGoogle Scholar
  40. Kwak S-H, Shen R, Schiefelbein J (2005) Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307:1111–1113PubMedCrossRefGoogle Scholar
  41. Laux T, Würschum T, Breuninger H (2004) Genetic regulation of embryonic pattern formation. Plant Cell 16:S190–S202PubMedCrossRefGoogle Scholar
  42. Lee MM, Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99:473–483PubMedCrossRefGoogle Scholar
  43. Lee MM, Schiefelbein J (2002) Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14:611–618PubMedCrossRefGoogle Scholar
  44. Leslie ME, Lewis ML, Liljegren SJ (2007) Organ abscission. In: Roberts J, Gonzalez-Carranza Z (eds) Plant cell separation and adhesion. Blackwell, Oxford, UK, pp 106–136CrossRefGoogle Scholar
  45. Leslie ME, Lewis MW, Youn J-Y, Daniels MJ, Liljegren SJ (2010) The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137:467–476PubMedCrossRefGoogle Scholar
  46. Lewis MW, Leslie ME, Fulcher EH, Darnielle L, Healy PN, Youn J-Y, Liljegren SJ (2010) The SERK1 receptor-like kinase regulates organ separation in Arabidopsis flowers. Plant J 62:817–828PubMedCrossRefGoogle Scholar
  47. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase gene involved in brassinosteroid signal transduction. Cell 90:929–938PubMedCrossRefGoogle Scholar
  48. Liljegren SJ, Leslie ME, Darnielle L, Lewis MW, Taylor SM, Luo R, Geldner N, Chory J, Randazzo PA, Yanofsky MF, Ecker JR (2009) Regulation of membrane trafficking and organ separation by the NEVERSHED ARF-GAP protein. Development 136:1909–1918PubMedCrossRefGoogle Scholar
  49. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434PubMedCrossRefGoogle Scholar
  50. Ma H, Sundaresan V (2010) Development of flowering plant gametophytes. Curr Top Dev Biol 91:379–412PubMedCrossRefGoogle Scholar
  51. Mansfield SG, Briarty LG (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 69:461–476CrossRefGoogle Scholar
  52. Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, Schiefelbein JW (1996) The homeobox gene GLABRA 2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122:1253–1260PubMedGoogle Scholar
  53. McKim SM, Stenvik G-S, Butenko MA, Kristiansen W, Cho SK, Hepworth SR, Aalen RB, Haughn GW (2008) The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development 135:1537–1546PubMedCrossRefGoogle Scholar
  54. 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
  55. Nakaya M, Tsukaya H, Murakami N, Kato M (2002) Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant Cell Physiol 43:239–244PubMedCrossRefGoogle Scholar
  56. Nanda K, Gupta SC (1978) Studies in the Bignoniaceae. II. Ontogeny of the dimorphic anther tapetum in Tecoma. Am J Bot 65:400–405CrossRefGoogle Scholar
  57. Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:1460–1471CrossRefGoogle Scholar
  58. Nodine MD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev Cell 12:943–956PubMedCrossRefGoogle Scholar
  59. Nodine MD, Bryan AC, Racolta A, Jerosky KV, Tax FE (2011) A few standing for many: embryo receptor-like kinases. Trends Plant Sci 16:211–217PubMedCrossRefGoogle Scholar
  60. Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559–565PubMedCrossRefGoogle Scholar
  61. Roberts JA, Whitelaw CA, Gonzalez-Carranza ZH, McManus MT (2000) Cell separation processes in plants–models, mechanisms and manipulation. Ann Bot 86:223–235CrossRefGoogle Scholar
  62. Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu Y-C, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322CrossRefGoogle Scholar
  63. Saulsberry A, Martin PR, O’Brien T, Sieburth LE, Pickett FB (2002) The induced sector Arabidopsis apical embryonic fate map. Development 129:3403–3410PubMedGoogle Scholar
  64. Savaldi-Goldstein S, Peto C, Chory J (2007) The epidermis both drives and restricts plant shoot growth. Nature 446:199–202PubMedCrossRefGoogle Scholar
  65. Schiefelbein J, Kwak S-H, Wieckowski Y, Barron C, Bruex A (2009) The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot 60:1515–1521PubMedCrossRefGoogle Scholar
  66. Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16:S46–S60PubMedCrossRefGoogle Scholar
  67. Shiu S-H, 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
  68. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234PubMedCrossRefGoogle Scholar
  69. Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131:1491–1501PubMedCrossRefGoogle Scholar
  70. Sorensen A, Guerineau F, Canales-Holzeis C, Dickinson HG, Scott RJ (2002) A novel extinction screen in Arabidopsis thaliana identifies mutant plants defective in early microsporangial development. Plant J 29:581–594PubMedCrossRefGoogle Scholar
  71. Stenvik G-E, Butenko MA, Urbanowicz BR, Rose JK, Aalen RB (2006) Overexpression of INFLORESCENCE DEFICIENT IN ABSCISSION activates cell separation in vestigial abscission zones in Arabidopsis. Plant Cell 18:1467–1476PubMedCrossRefGoogle Scholar
  72. Stenvik G-E, Tandstad NM, Guo Y, Shi C-L, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA (2008) The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20:1805–1817PubMedCrossRefGoogle Scholar
  73. Swain S, Kay P, Ogawa M (2011) Preventing unwanted breakups: using polygalacturonases to regulate cell separation. Plant Signal Behav 6:93–97PubMedCrossRefGoogle Scholar
  74. Takada S, Jürgens G (2007) Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134:1141–1150PubMedCrossRefGoogle Scholar
  75. Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y (2002) ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol 43:419–428PubMedCrossRefGoogle Scholar
  76. Tanaka H, Watanabe M, Sasabe M, Hilroe 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
  77. Tsuwamoto R, Fukuoka H, Takahata Y (2008) GASSHO1 and GASSHO2 encoding a putative leucine-rich repeat transmembrane-type receptor kinase are essential for the normal development of the epidermal surface in Arabidopsis embryos. Plant J 54:30–42PubMedCrossRefGoogle Scholar
  78. van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1995) Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378:62–65PubMedCrossRefGoogle Scholar
  79. Viotti C, Bubeck J, Stierhof Y-D, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jürgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–1357PubMedCrossRefGoogle Scholar
  80. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116PubMedCrossRefGoogle Scholar
  81. Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, Goto K, Marks MD, Shimura Y, Okada K (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129:5409–5419PubMedCrossRefGoogle Scholar
  82. 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
  83. Weijers D, van Hamburg J-P, van Rijn E, Hooykaas PJJ, Offringa R (2003) Diptheria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development. Plant Physiol 133:1882–1892PubMedCrossRefGoogle Scholar
  84. Wijeratne AJ, Zhang W, Sun Y, Liu W, Albert R, Zheng Z, Oppenheimer DG, Zhao D, Ma H (2007) Differential gene expression in Arabidopsis wild-type and mutant anthers: insights into anther cell differentiation and regulatory networks. Plant J 52:14–29PubMedCrossRefGoogle Scholar
  85. 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
  86. Yang W-C, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13:2108–2117PubMedCrossRefGoogle Scholar
  87. 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
  88. Yang SL, Jiang L, Puah CS, Xie LF, Zhang XQ, Chen LQ, Yang WC, Ye D (2005) Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with EXCESS MICROSPOROCYTES/EXTRA SPOROGENOUS CELLS. Plant Physiol 139:186–191PubMedCrossRefGoogle Scholar
  89. Zhao D-Z, Wang G-F, Speal B, Ma H (2002) The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat recepter protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031PubMedCrossRefGoogle Scholar
  90. Zhao D (2009) Control of anther cell differentiation: a teamwork of receptor-like kinases. Sex Plant Reprod 22:221–228Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Anthony Bryan
    • 1
  • Adriana Racolta
    • 1
  • Frans Tax
    • 1
  • Sarah Liljegren
    • 2
  1. 1.Department of Molecular and Cellular BiologyUniversity of ArizonaTucsonUSA
  2. 2.Department of BiologyUniversity of North CarolinaChapel HillUSA

Personalised recommendations