Functional interaction between Cdc42 and the stress MAPK signaling pathway during the regulation of fission yeast polarized growth

  • Pilar PérezEmail author
  • Teresa Soto
  • Elisa Gómez-Gil
  • Jose CansadoEmail author


Cell polarization can be defined as the generation and maintenance of directional cellular organization. The spatial distribution and protein or lipid composition of the cell are not symmetric but organized in specialized domains which allow cells to grow and acquire a certain shape that is closely linked to their physiological function. The establishment and maintenance of polarized growth requires the coordination of diverse processes including cytoskeletal dynamics, membrane trafficking, and signaling cascade regulation. Some of the major players involved in the selection and maintenance of sites for polarized growth are Rho GTPases, which recognize the polarization site and transmit the signal to regulatory proteins of the cytoskeleton. Additionally, cytoskeletal organization, polarized secretion, and endocytosis are controlled by signaling pathways including those mediated by mitogen-activated protein kinases (MAPKs). Rho GTPases and the MAPK signaling pathways are strongly conserved from yeast to mammals, suggesting that the basic mechanisms of polarized growth have been maintained throughout evolution. For this reason, the study of how polarized growth is established and regulated in simple organisms such as the fission yeast Schizosaccharomyces pombe has contributed to broaden our knowledge about these processes in multicellular organisms. We review here the function of the Cdc42 GTPase and the stress activated MAPK (SAPK) signaling pathways during fission yeast polarized growth, and discuss the relevance of the crosstalk between both pathways.


GTPase Cdc42 MAPK Sty1 Polarized growth 



We thank D. M. Posner for language revision. This work was supported by grants BIO2015-69958-P and BFU2017-82423-P from the Ministry of Science, Innovation and Universities (MICIU) and grants CSI068P17 and Escalera de Excelencia CLU-2017-03 from the Regional Government of Castilla y León (JCyL/FEDER) and the European Regional Development Fund (ERDF). The authors wish to acknowledge the many other studies on fission yeast cell polarity and apologize for not citing every important contribution in this review due to space limitations.

Compliance with ethical standards

Conflict of interest

The authors declare that they have conflict of interest.


  1. Aicart-Ramos C, Valero RA, Rodriguez-Crespo I (2011) Protein palmitoylation and subcellular trafficking. Biochim Biophys Acta 1808:2981–2994CrossRefGoogle Scholar
  2. Alvarez-Tabarés I, Grallert A, Ortiz JM, Hagan IM (2007) Schizosaccharomyces pombe protein phosphatase 1 in mitosis, endocytosis and a partnership with Wsh3/Tea4 to control polarised growth. J Cell Sci 120:3589–3601CrossRefGoogle Scholar
  3. Arellano M, Durán A, Pérez P (1996) Rho 1 GTPase activates the (1-3)beta-D-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J 15:4584–4591CrossRefGoogle Scholar
  4. Arellano M, Valdivieso MH, Calonge TM, Coll PM, Duran A, Perez P (1999) Schizosaccharomyces pombe protein kinase C homologues, pck1p and pck2p, are targets of rho1p and rho2p and differentially regulate cell integrity. J Cell Sci 112:3569–3578Google Scholar
  5. Asp E, Nilsson D, Sunnerhagen P (2008) Fission yeast mitogen-activated protein kinase Sty1 interacts with translation factors. Eukaryot Cell 7:328–338CrossRefGoogle Scholar
  6. Attanapola SL, Alexander CJ, Mulvihill DP (2009) Ste20-kinase-dependent TEDS-site phosphorylation modulates the dynamic localisation and endocytic function of the fission yeast class I myosin, Myo1. J Cell Sci 122:3856–3861CrossRefGoogle Scholar
  7. Bähler J, Pringle JR (1998) Pom1p, a fission yeast protein kinase that provides positional information for both polarized growth and cytokinesis. Genes Dev 12:1356–1370CrossRefGoogle Scholar
  8. Bendezu FO, Martin SG (2011) Actin cables and the exocyst form two independent morphogenesis pathways in the fission yeast. Mol Biol Cell 22:44–53CrossRefGoogle Scholar
  9. Bendezu FO, Vincenzetti V, Vavylonis D, Wyss R, Vogel H, Martin SG (2015) Spontaneous Cdc42 polarization independent of GDI-mediated extraction and actin-based trafficking. PLoS Biol 13:e1002097CrossRefGoogle Scholar
  10. Berlanga JJ, Rivero D, Martin R, Herrero S, Moreno S, de Haro C (2010) Role of mitogen-activated protein kinase Sty1 in regulation of eukaryotic initiation factor 2alpha kinases in response to environmental stress in Schizosaccharomyces pombe. Eukaryot Cell 9:194–207CrossRefGoogle Scholar
  11. Bicho CC, Kelly DA, Snaith HA, Goryachev AB, Sawin KE (2010) A catalytic role for Mod5 in the formation of the Tea1 cell polarity landmark. Curr Biol 20:1752–1757CrossRefGoogle Scholar
  12. Bluthgen N, Legewie S (2008) Systems analysis of MAPK signal transduction. Essays in Biochem 45:95–107CrossRefGoogle Scholar
  13. Bos JL, Rehmann H, Wittinghofer A (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129:865–877CrossRefGoogle Scholar
  14. Buck V, Quinn J, Soto Pino T, Martin H, Saldanha J, Makino K, Morgan BA, Millar JB (2001) Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol Biol Cell 12:407–419CrossRefGoogle Scholar
  15. Cabib E, Drgonová J, Drgon T (1998) Role of small G proteins in yeast cell polarization and wall biosynthesis. Annu Rev Biochem 67:307–333CrossRefGoogle Scholar
  16. Calonge TM, Nakano K, Arellano M, Arai R, Katayama S, Toda T, Mabuchi I, Perez P (2000) Schizosaccharomyces pombe rho2p GTPase regulates cell wall alpha-glucan biosynthesis through the protein kinase pck2p. Mol Biol Cell 11:4393–4401Google Scholar
  17. Chang EC, Barr M, Wang Y, Jung V, Xu HP, Wigler MH (1994) Cooperative interaction of S. pombe proteins required for mating and morphogenesis. Cell Cycle 79:131–141Google Scholar
  18. Chang E, Bartholomeusz G, Pimental R, Chen J, Lai H, Wang LH, Yang P, Marcus S (1999) Direct binding and in vivo regulation of the fission yeast p21-activated kinase shk1 by the SH3 domain protein scd2. Mol Cell Biol 19:8066–8074CrossRefGoogle Scholar
  19. Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bahler J (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–229CrossRefGoogle Scholar
  20. Coffman VC, Sees JA, Kovar DR, Wu JQ (2013) The formins Cdc12 and For3 cooperate during contractile ring assembly in cytokinesis. J Cell Biol 203:101–114CrossRefGoogle Scholar
  21. Coll PM, Trillo Y, Ametzazurra A, Perez P (2003) Gef1p, a new guanine nucleotide exchange factor for Cdc42p, regulates polarity in Schizosaccharomyces pombe. Mol Biol Cell 14:313–323Google Scholar
  22. Das M, Wiley DJ, Medina S, Vincent HA, Larrea M, Oriolo A, Verde F (2007) Regulation of cell diameter, For3p localization, and cell symmetry by fission yeast Rho-GAP Rga4p. Mol Biol Cell 18:2090–2101CrossRefGoogle Scholar
  23. Das M, Drake T, Wiley DJ, Buchwald P, Vavylonis D, Verde F (2012) Oscillatory dynamics of Cdc42 GTPase in the control of polarized growth. Science 337:239–243CrossRefGoogle Scholar
  24. Das M, Nunez I, Rodriguez M, Wiley DJ, Rodriguez J, Sarkeshik A, Yates JR 3rd, Buchwald P, Verde F (2015) Phosphorylation-dependent inhibition of Cdc42 GEF Gef1 by 14-3-3 protein Rad24 spatially regulates Cdc42 GTPase activity and oscillatory dynamics during cell morphogenesis. Mol Biol Cell 26:3520–3534CrossRefGoogle Scholar
  25. Doi A, Kita A, Kanda Y, Uno T, Asami K, Satoh R, Nakano K, Sugiura R (2015) Geranylgeranyltransferase Cwg2-Rho4/Rho5 module is implicated in the Pmk1 MAP kinase-mediated cell wall integrity pathway in fission yeast. Genes Cells 20:310–323CrossRefGoogle Scholar
  26. Dudin O, Merlini L, Bendezu FO, Groux R, Vincenzetti V, Martin SG (2017) A systematic screen for morphological abnormalities during fission yeast sexual reproduction identifies a mechanism of actin aster formation for cell fusion. PLoS Genet 13:e1006721CrossRefGoogle Scholar
  27. Estravis M, Rincon SA, Santos B, Perez P (2011) Cdc42 regulates multiple membrane traffic events in fission yeast. Traffic 12:1744–1758CrossRefGoogle Scholar
  28. Estravis M, Rincon SA, Portales E, Perez P, Santos B (2017) Cdc42 activation state affects its localization and protein levels in fission yeast. MicrobiologyGoogle Scholar
  29. Etienne-Manneville S (2004) Cdc42--the Centre of polarity. J Cell Sci 117:1291–1300CrossRefGoogle Scholar
  30. Feierbach B, Chang F (2001) Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr Biol 11:1656–1665CrossRefGoogle Scholar
  31. Gachet Y, Hyams JS (2005) Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis. J Cell Sci 118:4231–4242CrossRefGoogle Scholar
  32. Gacto M, Soto T, Vicente-Soler J, Villa T, Cansado J (2003) Learning from yeasts: intracellular sensing of stress conditions. Int Microbio l6:211–219CrossRefGoogle Scholar
  33. Gallo Castro D, Martin SG (2018) Differential GAP requirement for Cdc42-GTP polarization during proliferation and sexual reproduction. J Cell Biol 217:4215–4229CrossRefGoogle Scholar
  34. Garcia Cortes JC, Ramos M, Osumi M, Perez P, Ribas JC (2016) The cell biology of fission yeast Septation. Microbiol Mol Biol Rev 80:779–791CrossRefGoogle Scholar
  35. Garcia P, Tajadura V, Sanchez Y (2009) The Rho1p exchange factor Rgf1p signals upstream from the Pmk1 mitogen-activated protein kinase pathway in fission yeast. Mol Biol Cell 20:721–731CrossRefGoogle Scholar
  36. Haupt A, Ershov D, Minc N (2018) A positive feedback between growth and polarity provides directional persistency and flexibility to the process of tip growth. Curr Biol 28:3342–3351 e3343CrossRefGoogle Scholar
  37. Hodge RG, Ridley AJ (2016) Regulating Rho GTPases and their regulators. Nat Rev Mol Cell Biol 17:496–510CrossRefGoogle Scholar
  38. Hoffman CS, Wood V, Fantes PA (2015) An ancient yeast for young geneticists: a primer on the Schizosaccharomyces pombe model system. Genetics 201:403–423CrossRefGoogle Scholar
  39. Huang Y, Chew TG, Ge W, Balasubramanian MK (2007) Polarity determinants Tea1p, Tea4p, and Pom1p inhibit division-septum assembly at cell ends in fission yeast. Dev Cell 12:987–996CrossRefGoogle Scholar
  40. Huisman SM, Brunner D (2011) Cell polarity in fission yeast: a matter of confining, positioning, and switching growth zones. Semin Cell Dev Biol 22:799–805CrossRefGoogle Scholar
  41. Kelly FD, Nurse P (2011) Spatial control of Cdc42 activation determines cell width in fission yeast. Mol Biol Cell 22:3801–3811CrossRefGoogle Scholar
  42. Kim H, Yang P, Catanuto P, Verde F, Lai H, Du H, Chang F, Marcus S (2003) The kelch repeat protein, Tea1, is a potential substrate target of the p21-activated kinase, Shk1, in the fission yeast, Schizosaccharomyces pombe. J Biol Chem 278:30074–30082Google Scholar
  43. Kokkoris K, Gallo Castro D, Martin SG (2014) The Tea4-PP1 landmark promotes local growth by dual Cdc42 GEF recruitment and GAP exclusion. J Cell Sci 127:2005–2016CrossRefGoogle Scholar
  44. Kovar DR, Sirotkin V, Lord M (2011) Three's company: the fission yeast actin cytoskeleton. Trends Cell Biol 21:177–187CrossRefGoogle Scholar
  45. Lawrence CL, Maekawa H, Worthington JL, Reiter W, Wilkinson CR, Jones N (2007) Regulation of Schizosaccharomyces pombe Atf1 protein levels by Sty1-mediated phosphorylation and heterodimerization with Pcr1. J Biol Chem 282, United States:5160–5170CrossRefGoogle Scholar
  46. Loo TH, Balasubramanian M (2008) Schizosaccharomyces pombe Pak-related protein, Pak1p/Orb2p, phosphorylates myosin regulatory light chain to inhibit cytokinesis. J Cell Biol 183:785–793CrossRefGoogle Scholar
  47. Lopez-Aviles S, Grande M, Gonzalez M, Helgesen AL, Alemany V, Sanchez-Piris M, Bachs O, Millar JB, Aligue R (2005) Inactivation of the Cdc25 phosphatase by the stress-activated Srk1 kinase in fission yeast. Mol Cell 17:49–59CrossRefGoogle Scholar
  48. Ma Y, Kuno T, Kita A, Asayama Y, Sugiura R (2006) Rho2 is a target of the farnesyltransferase Cpp1 and acts upstream of Pmk1 mitogen-activated protein kinase signaling in fission yeast. Mol Biol Cell 17:5028–5037CrossRefGoogle Scholar
  49. Marcus S, Polverino A, Chang E, Robbins D, Cobb MH, Wigler MH (1995) Shk1, a homolog of the Saccharomyces cerevisiae Ste20 and mammalian p65PAK protein kinases, is a component of a Ras/Cdc42 signaling module in the fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci U S A 92:6180–6184CrossRefGoogle Scholar
  50. Martin SG (2015) Spontaneous cell polarization: feedback control of Cdc42 GTPase breaks cellular symmetry. Bioessays 37:1193–1201CrossRefGoogle Scholar
  51. Martin SG, Berthelot-Grosjean M (2009) Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 459:852–856CrossRefGoogle Scholar
  52. Martin SG, McDonald WH, Yates JR 3rd, Chang F (2005) Tea4p links microtubule plus ends with the formin for3p in the establishment of cell polarity. Dev Cell 8:479–491CrossRefGoogle Scholar
  53. Martin V, Rodriguez-Gabriel MA, McDonald WH, Watt S, Yates JR 3rd, Bahler J, Russell P (2006) Cip1 and Cip2 are novel RNA-recognition-motif proteins that counteract Csx1 function during oxidative stress. Mol Biol Cell 17:1176–1183CrossRefGoogle Scholar
  54. Martin SG, Rincon SA, Basu R, Perez P, Chang F (2007) Regulation of the formin for3p by cdc42p and bud6p. Mol Biol Cell 18:4155–4167CrossRefGoogle Scholar
  55. Mata J, Nurse P (1997) Tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 89:939–949CrossRefGoogle Scholar
  56. Millar JB, Buck V, Wilkinson MG (1995) Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev 9:2117–2130CrossRefGoogle Scholar
  57. Morigasaki S, Ikner A, Tatebe H, Shiozaki K (2013) Response regulator-mediated MAPKKK heteromer promotes stress signaling to the Spc1 MAPK in fission yeast. Mol Biol Cell 24:1083–1092CrossRefGoogle Scholar
  58. Moseley JB, Mayeux A, Paoletti A, Nurse P (2009) A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 459:857–860CrossRefGoogle Scholar
  59. Mutavchiev DR, Leda M, Sawin KE (2016) Remodeling of the fission yeast Cdc42 cell-polarity module via the Sty1 p38 stress-activated protein kinase pathway. Curr Biol 26:2921–2928CrossRefGoogle Scholar
  60. Nakano K, Toya M, Yoneda A, Asami Y, Yamashita A, Kamasawa N, Osumi M, Yamamoto M (2011) Pob1 ensures cylindrical cell shape by coupling two distinct rho signaling events during secretory vesicle targeting. Traffic 12:726–739CrossRefGoogle Scholar
  61. Nguyen AN, Shiozaki K (1999) Heat-shock-induced activation of stress MAP kinase is regulated by threonine- and tyrosine-specific phosphatases. Genes Dev 13:1653–1663CrossRefGoogle Scholar
  62. Nguyen AN, Ikner AD, Shiozaki M, Warren SM, Shiozaki K (2002) Cytoplasmic localization of Wis1 MAPKK by nuclear export signal is important for nuclear targeting of Spc1/Sty1 MAPK in fission yeast. Mol Biol Cell 13:2651–2663CrossRefGoogle Scholar
  63. Opalko HE, Moseley JB (2017) Dynamic regulation of Cdr1 kinase localization and phosphorylation during osmotic stress. J Biol Chem 292:18457–18468CrossRefGoogle Scholar
  64. Perez P, Cansado J (2010) Cell integrity signaling and response to stress in fission yeast. Curr Protein Pept Sci 11:680–692CrossRefGoogle Scholar
  65. Perez P, Rincon SA (2010) Rho GTPases: regulation of cell polarity and growth in yeasts. Biochem J 426:243–253CrossRefGoogle Scholar
  66. Perez P, Portales E, Santos B (2015) Rho4 interaction with exocyst and septins regulates cell separation in fission yeast. Microbiology 161:948–959CrossRefGoogle Scholar
  67. Petersen J, Hagan IM (2005) Polo kinase links the stress pathway to cell cycle control and tip growth in fission yeast. Nature 435:507–512CrossRefGoogle Scholar
  68. Pollard TD (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Ann Rev Biophys Biomol Struct 36:451–477CrossRefGoogle Scholar
  69. Quinn J, Findlay VJ, Dawson K, Millar JB, Jones N, Morgan BA, Toone WM (2002) Distinct regulatory proteins control the graded transcriptional response to increasing H(2)O(2) levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 13:805–816CrossRefGoogle Scholar
  70. Revilla-Guarinos MT, Martin-Garcia R, Villar-Tajadura MA, Estravis M, Coll PM, Perez P (2016) Rga6 is a fission yeast rho GAP involved in Cdc42 regulation of polarized growth. Mol Biol Cell 27:1524–1535CrossRefGoogle Scholar
  71. Rincon SA, Santos B, Perez P (2006) Fission yeast Rho5p GTPase is a functional paralogue of Rho1p that plays a role in survival of spores and stationary-phase cells. Eukaryot Cell 5:435–446CrossRefGoogle Scholar
  72. Robertson AM, Hagan IM (2008) Stress-regulated kinase pathways in the recovery of tip growth and microtubule dynamics following osmotic stress in S. Pombe. J Cell Sci 121:4055–4068CrossRefGoogle Scholar
  73. Rodriguez-Gabriel MA, Burns G, McDonald WH, Martin V, Yates JR 3rd, Bahler J, Russell P (2003) RNA-binding protein Csx1 mediates global control of gene expression in response to oxidative stress. EMBO J 22:6256–6266CrossRefGoogle Scholar
  74. Salat-Canela C, Paulo E, Sánchez-Mir L, Carmona M, Ayté J, Oliva B, Hidalgo E (2017) Deciphering the role of the signal- and Sty1 kinase-dependent phosphorylation of the stress-responsive transcription factor Atf1 on gene activation. J Biol Chem 292:13635–13644CrossRefGoogle Scholar
  75. Sanchez-Marinas M, Gimenez-Zaragoza D, Martin-Ramos E, Llanes J, Cansado J, Pujol MJ, Bachs O, Aligue R (2018) Cmk2 kinase is essential for survival in arsenite by modulating translation together with RACK1 orthologue Cpc2 in Schizosaccharomyces pombe. Free Radic Biol Med 129:116–126Google Scholar
  76. Sanchez-Mir L, Franco A, Martin-Garcia R, Madrid M, Vicente-Soler J, Soto T, Gacto M, Perez P, Cansado J (2014a) Rho2 palmitoylation is required for plasma membrane localization and proper signaling to the fission yeast cell integrity MAPK pathway. Mol Cell Biol 34:2747–2759CrossRefGoogle Scholar
  77. Sanchez-Mir L, Soto T, Franco A, Madrid M, Viana RA, Vicente J, Gacto M, Perez P, Cansado J (2014b) Rho1 GTPase and PKC ortholog Pck1 are upstream activators of the cell integrity MAPK pathway in fission yeast. PLoS One 9:e88020CrossRefGoogle Scholar
  78. Santos B, Gutierrez J, Calonge TM, Perez P (2003) Novel rho GTPase involved in cytokinesis and cell wall integrity in the fission yeast Schizosaccharomyces pombe. Eukaryot Cell 2:521–533CrossRefGoogle Scholar
  79. Santos B, Martin-Cuadrado AB, Vazquez de Aldana CR, del Rey F, Perez P (2005) Rho4 GTPase is involved in secretion of glucanases during fission yeast cytokinesis. Eukaryot Cell 4:1639–1645CrossRefGoogle Scholar
  80. Sells MA, Barratt JT, Caviston J, Ottilie S, Leberer E, Chernoff J (1998) Characterization of Pak2p, a pleckstrin homology domain-containing, p21-activated protein kinase from fission yeast. J Biol Chem 273:18490–18498CrossRefGoogle Scholar
  81. Shiozaki K, Russell P (1996) Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev 10:2276–2288CrossRefGoogle Scholar
  82. Snaith HA, Samejima I, Sawin KE (2005) Multistep and multimode cortical anchoring of tea1p at cell tips in fission yeast. EMBO J 24:3690–3699CrossRefGoogle Scholar
  83. Soto T, Beltran FF, Paredes V, Madrid M, Millar JBA, Vicente-Soler J, Cansado J, Gacto M (2002) Cold induces stress-activated protein kinase-mediated response in the fission yeast Schizosaccharomyces pombe. Eur J Biochem 269:5056–5065Google Scholar
  84. Soto T, Nunez A, Madrid M, Vicente J, Gacto M, Cansado J (2007) Transduction of centrifugation-induced gravity forces through mitogen-activated protein kinase pathways in the fission yeast Schizosaccharomyces pombe. Microbiology 153:1519–1529Google Scholar
  85. Tatebe H, Shimada K, Uzawa S, Morigasaki S, Shiozaki K (2005) Wsh3/Tea4 is a novel cell-end factor essential for bipolar distribution of Tea1 and protects cell polarity under environmental stress in S. pombe. Curr Biol 15:1006–1015Google Scholar
  86. Tatebe H, Nakano K, Maximo R, Shiozaki K (2008) Pom1 DYRK regulates localization of the Rga4 GAP to ensure bipolar activation of Cdc42 in fission yeast. Curr Biol 18:322–330CrossRefGoogle Scholar
  87. Tay YD, Leda M, Goryachev AB, Sawin KE (2018) Local and global Cdc42 guanine nucleotide exchange factors for fission yeast cell polarity are coordinated by microtubules and the Tea1-Tea4-Pom1 axis. J Cell Sci 131.
  88. Terenna CR, Makushok T, Velve-Casquillas G, Baigl D, Chen Y, Bornens M, Paoletti A, Piel M, Tran PT (2008) Physical mechanisms redirecting cell polarity and cell shape in fission yeast. Curr Biol 18:1748–1753CrossRefGoogle Scholar
  89. Tiedje C, Sakwa I, Just U, Hofken T (2008) The Rho GDI Rdi1 regulates Rho GTPases by distinct mechanisms. Mol Biol Cell 19:2885–2896CrossRefGoogle Scholar
  90. Tran PT, Marsh L, Doye V, Inoué S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153:397–411CrossRefGoogle Scholar
  91. Tu H, Barr M, Dong DL, Wigler M (1997) Multiple regulatory domains on the Byr2 protein kinase. Mol Cell Biol 17:5876–5887CrossRefGoogle Scholar
  92. Vetter IR, Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294:1299–1304CrossRefGoogle Scholar
  93. Viana RA, Pinar M, Soto T, Coll PM, Cansado J, Pérez P (2013) Negative functional interaction between cell integrity MAPK pathway and Rho1 GTPase in fission yeast. Genetics 195:421–432CrossRefGoogle Scholar
  94. Vjestica A, Merlini L, Nkosi PJ, Martin SG (2018) Gamete fusion triggers bipartite transcription factor assembly to block re-fertilization. Nature 560:397–400CrossRefGoogle Scholar
  95. Wang H, Tang X, Balasubramanian MK (2003) Rho3p regulates cell separation by modulating exocyst function in Schizosaccharomyces pombe. Genetics 164:1323–1331Google Scholar
  96. Wedlich-Soldner R, Li R (2003) Spontaneous cell polarization: undermining determinism. Nat Cell Biol 5:267–270CrossRefGoogle Scholar
  97. Wennerberg K, Rossman KL, Der CJ (2005) The Ras superfamily at a glance. J Cell Sci 118:843–846CrossRefGoogle Scholar
  98. Wilkinson MG, Samuels M, Takeda T, Toone WM, Shieh JC, Toda T, Millar JB, Jones N (1996) The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. Genes Dev 10:2289–2301CrossRefGoogle Scholar
  99. Winter D, Podtelejnikov AV, Mann M, Li R (1997) The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches. Curr Biol 7:519–529CrossRefGoogle Scholar
  100. Wood E, Nurse P (2013) Pom1 and cell size homeostasis in fission yeast. Cell Cycle 12:3228–3236CrossRefGoogle Scholar
  101. Yang P, Qyang Y, Bartholomeusz G, Zhou X, Marcus S (2003) The novel Rho GTPase-activating protein family protein, Rga8, provides a potential link between Cdc42/p21-activated kinase and Rho signaling pathways in the fission yeast, Schizosaccharomyces pombe. J Biol Chem 278:48821–48830Google Scholar
  102. Yonetani A, Chang F (2010) Regulation of cytokinesis by the formin cdc12p. Curr Biol 20:561–566CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Instituto de Biología Funcional y GenómicaConsejo Superior de Investigaciones Científicas and Universidad de SalamancaSalamancaSpain
  2. 2.Yeast Physiology Group, Department of Genetics and Microbiology, Facultad de BiologíaUniversidad de MurciaMurciaSpain

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