Evolution of nuclear auxin signaling: Lessons from genetic studies with basal land plants

Journal of Experimental Botany

Volumn 69, Issue 2, 2018, Pages 291-301

  Kato, Hirotaka ^a   Nishihama, Ryuichi ^b   Weijers, Dolf ^a   Kohchi, Takayuki ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

ARF; AUX IAA; bryophytes; charophytes; evolution; TIR1 AFB; TPL

Indexed keywords

INDOLEACETIC ACID DERIVATIVE; PHYTOHORMONE;

CELL NUCLEUS; METABOLISM; MOLECULAR EVOLUTION; MOSS; PHYSIOLOGY; PLANT PHYSIOLOGY; SIGNAL TRANSDUCTION;

BRYOPHYTA; CELL NUCLEUS; EVOLUTION, MOLECULAR; INDOLEACETIC ACIDS; PLANT GROWTH REGULATORS; PLANT PHYSIOLOGICAL PHENOMENA; SIGNAL TRANSDUCTION;

EID: 85040638199     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erx267     Document Type: Review

References (147)

1. Allen E, Xie Z, Gustafson AM, Carrington JC. 2005. microRNAdirected phasing during trans-Acting siRNA biogenesis in plants. Cell 121, 207-221.
2. Amin SA, Hmelo LR, van Tol HM, et al. 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98-101.
3. Aoyama T, Hiwatashi Y, Shigyo M, Kofuji R, Kubo M, Ito M, Hasebe M. 2012. AP2-Type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139, 3120-3129.
4. Ashton NW, Grimsley NH, Cove DJ. 1979. Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta 144, 427-435.
5. Axtell MJ, Bartel DP. 2005. Antiquity of microRNAs and their targets in land plants. The Plant Cell 17, 1658-1673.
6. Axtell MJ, Snyder JA, Bartel DP. 2007. Common functions for diverse small RNAs of land plants. The Plant Cell 19, 1750-1769.
7. Bagwell CE, Piskorska M, Soule T, Petelos A, Yeager CM. 2014. A diverse assemblage of indole-3-Acetic acid producing bacteria associate with unicellular green algae. Applied Biochemistry and Biotechnology 173, 1977-1984.
8. Banks JA, Nishiyama T, Hasebe M, et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960-963.
9. Barnes CR, Land WJG. 1908. Bryological papers. II. The origin of the cupule of Marchantia. Botanical Gazette 46, 401-409.
10. Bennett TA, Liu MM, Aoyama T, et al. 2014. Plasma membranetargeted PIN proteins drive shoot development in a moss. Current Biology 24, 2776-2785.
11. Boer DR, Freire-Rios A, van den Berg WA, et al. 2014. Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156, 577-589.
12. Bowman JL. 2013. Walkabout on the long branches of plant evolution. Current Opinion in Plant Biology 16, 70-77.
13. Bowman JL. 2016. A brief history of Marchantia from Greece to genomics. Plant & Cell Physiology 57, 210-229.
14. Breuninger H, Thamm A, Streubel S, Sakayama H, Nishiyama T, Dolan L. 2016. Diversification of a transcription factor family led to the evolution of antagonistically acting genetic regulators of root hair growth. Current Biology 26, 1622-1628.
15. Bui LT, Cordle AR, Irish EE, Cheng CL. 2015. Transient and stable transformation of Ceratopteris richardii gametophytes. BMC Research Notes 8, 214.
16. Calderón Villalobos LI, Lee S, De Oliveira C, et al. 2012. A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nature Chemical Biology 8, 477-485.
17. Causier B, Ashworth M, Guo W, Davies B. 2012a. The TOPLESS interactome: A framework for gene repression in Arabidopsis. Plant Physiology 158, 423-438.
18. Causier B, Lloyd J, Stevens L, Davies B. 2012b. TOPLESS co-repressor interactions and their evolutionary conservation in plants. Plant Signaling & Behavior 7, 325-328.
19. Chandler JW. 2016. Auxin response factors. Plant, Cell & Environment 39, 1014-1028.
20. Cho H, Ryu H, Rho S, et al. 2014. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nature Cell Biology 16, 66-76.
21. Cooke TJ, Poli D, Sztein AE, Cohen JD. 2002. Evolutionary patterns in auxin action. Plant Molecular Biology 49, 319-338.
22. Coudert Y, Palubicki W, Ljung K, Novak O, Leyser O, Harrison CJ. 2015. Three ancient hormonal cues co-ordinate shoot branching in a moss. eLife 4, e06808.
23. Darwin C. 1880. The power of movement in plants. London: John Murray.
24. De AK, Dey N, Adak MK. 2016. Bio indices for 2, 4-D sensitivity between two plant species: Azolla pinnata R.Br. and Vernonia cinerea L. with their cellular responses. Physiology and Molecular Biology of Plants 22, 371-380.
25. De Rybel B, Möller B, Yoshida S, Grabowicz I, Barbier de Reuille P, Boeren S, Smith RS, Borst JW, Weijers D. 2013. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Developmental Cell 24, 426-437.
26. de Vries J, Fischer AM, Roettger M, Rommel S, Schluepmann H, Bräutigam A, Carlsbecker A, Gould SB. 2016. Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots. New Phytologist 209, 705-720.
27. Dharmasiri N, Dharmasiri S, Estelle M. 2005a. The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445.
28. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jörgens G, Estelle M. 2005b. Plant development is regulated by a family of auxin receptor F box proteins. Developmental Cell 9, 109-119.
29. Ding W, Yu Z, Tong Y, Huang W, Chen H, Wu P. 2009. A transcription factor with a bHLH domain regulates root hair development in rice. Cell Research 19, 1309-1311.
30. Eklund DM, Ishizaki K, Flores-Sandoval E, et al. 2015. Auxin produced by the indole-3-pyruvic acid pathway regulates development and gemmae dormancy in the liverwort Marchantia polymorpha. The Plant Cell 27, 1650-1669.
31. Finet C, Berne-Dedieu A, Scutt CP, Marlétaz F. 2013. Evolution of the ARF gene family in land plants: old domains, new tricks. Molecular Biology and Evolution 30, 45-56.
32. Flores-Sandoval E, Dierschke T, Fisher TJ, Bowman JL. 2015a. Efficient and inducible use of artificial MicroRNAs in Marchantia polymorpha. Plant & Cell Physiology 57, 281-290.
33. Flores-Sandoval E, Eklund DM, Bowman JL. 2015b. A simple auxin transcriptional response system regulates multiple morphogenetic processes in the liverwort Marchantia polymorpha. PLoS Genetics 11, e1005207.
34. Floyd SK, Bowman JL. 2007. The ancestral developmental tool kit of land plants. International Journal of Plant Sciences 168, 1-35.
35. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jörgens G. 2003. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147-153.
36. Fu SF, Wei JY, Chen HW, Liu YY, Lu HY, Chou JY. 2015. Indole-3-Acetic acid: A widespread physiological code in interactions of fungi with other organisms. Plant Signaling & Behavior 10, e1048052.
37. Fujita T, Sakaguchi H, Hiwatashi Y, Wagstaff SJ, Ito M, Deguchi H, Sato T, Hasebe M. 2008. Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots. Evolution & Development 10, 176-186.
38. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M. 2001. Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414, 271-276.
39. Guilfoyle TJ, Hagen G. 2001. Auxin response factors. Journal of Plant Growth Regulation 20, 281-291.
40. Guseman JM, Hellmuth A, Lanctot A, Feldman TP, Moss BL, Klavins E, Calderón Villalobos LI, Nemhauser JL. 2015. Auxininduced degradation dynamics set the pace for lateral root development. Development 142, 905-909.
41. Hamann T, Mayer U, Jörgens G. 1999. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126, 1387-1395.
42. Hardtke CS, Berleth T. 1998. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. The EMBO Journal 17, 1405-1411.
43. Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E. 2000. The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. The Plant Cell 12, 757-770.
44. Harrison CJ, Roeder AH, Meyerowitz EM, Langdale JA. 2009. Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Current Biology 19, 461-471.
45. Havens KA, Guseman JM, Jang SS, Pierre-Jerome E, Bolten N, Klavins E, Nemhauser JL. 2012. A synthetic approach reveals extensive tunability of auxin signaling. Plant Physiology 160, 135-142.
46. Hori K, Maruyama F, Fujisawa T, et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications 5, 3978.
47. Horstman A, Willemsen V, Boutilier K, Heidstra R. 2014. AINTEGUMENTA-LIKE proteins: hubs in a plethora of networks. Trends in Plant Science 19, 146-157.
48. Jang G, Dolan L. 2011. Auxin promotes the transition from chloronema to caulonema in moss protonema by positively regulating PpRSL1 and PpRSL2 in Physcomitrella patens. New Phytologist 192, 319-327.
49. Jang G, Yi K, Pires ND, Menand B, Dolan L. 2011. RSL genes are sufficient for rhizoid system development in early diverging land plants. Development 138, 2273-2281.
50. Jiao Y, Wickett NJ, Ayyampalayam S, et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97-100.
51. Ju C, Van der Poel B, Cooper ED, Thierer JH, Gibbons TR, Delwiche CF, Chang C. 2015. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nature Plants 1, 1-7.
52. Karas B, Amyot L, Johansen C, Sato S, Tabata S, Kawaguchi M, Szczyglowski K. 2009. Conservation of Lotus and Arabidopsis basic helix-loop-helix proteins reveals new players in root hair development. Plant Physiology 151, 1175-1185.
53. Kato H, Ishizaki K, Kouno M, Shirakawa M, Bowman JL, Nishihama R, Kohchi T. 2015. Auxin-mediated transcriptional system with a minimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha. PLoS Genetics 11, e1005084.
54. Kato H, Kouno M, Takeda M, Suzuki H, Ishizaki K, Nishihama R, Kohchi T. 2017. The roles of the sole activator-Type auxin response factor in pattern formation of Marchantia polymorpha. Plant & Cell Physiology, in press. doi:10.1093/pcp/pcx095.
55. Kelley DR, Arreola A, Gallagher TL, Gasser CS. 2012. ETTIN (ARF3) physically interacts with KANADI proteins to form a functional complex essential for integument development and polarity determination in Arabidopsis. Development 139, 1105-1109.
56. Kepinski S, Leyser O. 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451.
57. Kim J, Harter K, Theologis A. 1997. Protein-protein interactions among the Aux/IAA proteins. Proceedings of the National Academy of Sciences, USA 94, 11786-11791.
58. Kofuji R, Hasebe M. 2014. Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Current Opinion in Plant Biology 17, 13-21.
59. Kohlenbach HW. 1957. Die Bedeutung des heretoauxins för die entwicklung der Dorsiventralität der Brutkörperkeimlinge von Marchantia polymorpha L. Biologisches Zentralblatt 76, 70-125.
60. Krogan NT, Ckurshumova W, Marcos D, Caragea AE, Berleth T. 2012. Deletion of MP/ARF5 domains III and IV reveals a requirement for Aux/IAA regulation in Arabidopsis leaf vascular patterning. The New Phytologist 194, 391-401.
61. Labeeuw L, Khey J, Bramucci AR, Atwal H, de la Mata AP, Harynuk J, Case RJ. 2016. Indole-3-Acetic acid is produced by Emiliania huxleyi coccolith-bearing cells and triggers a physiological response in bald cells. Frontiers in Microbiology 7, 828.
62. Landberg K, Pederson ER, Viaene T, Bozorg B, Friml J, Jönsson H, Thelander M, Sundberg E. 2013. The moss Physcomitrella patens reproductive organ development is highly organized, affected by the two SHI/STY genes and by the level of active auxin in the SHI/STY expression domain. Plant Physiology 162, 1406-1419.
63. Lau S, Shao N, Bock R, Jörgens G, De Smet I. 2009. Auxin signaling in algal lineages: fact or myth? Trends in Plant Science 14, 182-188.
64. Lavy M, Prigge MJ, Tao S, Shain S, Kuo A, Kirchsteiger K, Estelle M. 2016. Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. eLife 5, e13325.
65. Leyser HM, Pickett FB, Dharmasiri S, Estelle M. 1996. Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. The Plant Journal 10, 403-413.
66. Lin PC, Lu CW, Shen BN, et al. 2016. Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-seq and degradome analyses. Plant & Cell Physiology 57, 339-358.
67. Liscum E, Reed JW. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Molecular Biology 49, 387-400.
68. Mallory AC, Bartel DP, Bartel B. 2005. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. The Plant Cell 17, 1360-1375.
69. Masucci JD, Schiefelbein JW. 1994. The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin-And ethylene-Associated process. Plant Physiology 106, 1335-1346.
70. Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG, Dolan L. 2007. An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316, 1477-1480.
71. Mittag J, Šola I, Rusak G, Ludwig-Möller J. 2015. Physcomitrella patens auxin conjugate synthetase (GH3) double knockout mutants are more resistant to Pythium infection than wild type. Journal of Plant Physiology 183, 75-83.
72. Möller B, Schenck D, Löthen H. 2010. Exploring the link between auxin receptors, rapid cell elongation and organ tropisms. Plant Signaling & Behavior 5, 601-603.
73. Möller BK, Ten Hove CA, Xiang D, Williams N, López LG, Yoshida S, Smit M, Datla R, Weijers D. 2017. Auxin response cellautonomously controls ground tissue initiation in the early Arabidopsis embryo. Proceedings of the National Academy of Sciences, USA 114, E2533-E2539.
74. Muthukumar B, Joyce BL, Elless MP, Stewart CN Jr. 2013. Stable transformation of ferns using spores as targets: Pteris vittata and Ceratopteris thalictroides. Plant Physiology 163, 648-658.
75. Muto H, Watahiki MK, Nakamoto D, Kinjo M, Yamamoto KT. 2007. Specificity and similarity of functions of the Aux/IAA genes in auxin signaling of Arabidopsis revealed by promoter-exchange experiments among MSG2/IAA19, AXR2/IAA7, and SLR/IAA14. Plant Physiology 144, 187-196.
76. Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW. 2000. AXR2 encodes a member of the Aux/IAA protein family. Plant Physiology 123, 563-574.
77. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439.
78. OMalley RC, Huang SS, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR. 2016. Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165, 1280-1292.
79. Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY. 2014. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife 3, e03031.
80. Okushima Y, Overvoorde PJ, Arima K, et al. 2005. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. The Plant Cell 17, 444-463.
81. Overvoorde PJ, Okushima Y, Alonso JM, et al. 2005. Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. The Plant Cell 17, 3282-3300.
82. Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K. 2009. The evolution of nuclear auxin signalling. BMC Evolutionary Biology 9, 126.
83. Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M. 2009. Complex regulation of the TIR1/AFB family of auxin receptors. Proceedings of the National Academy of Sciences, USA 106, 22540-22545.
84. Pérez-Pérez JM, Candela H, Robles P, López-Torrejón G, del Pozo JC, Micol JL. 2010. A role for AUXIN RESISTANT3 in the coordination of leaf growth. Plant & Cell Physiology 51, 1661-1673.
85. Pfluger J, Zambryski P. 2004. The role of SEUSS in auxin response and floral organ patterning. Development 131, 4697-4707.
86. Pierre-Jerome E, Moss BL, Lanctot A, Hageman A, Nemhauser JL. 2016. Functional analysis of molecular interactions in synthetic auxin response circuits. Proceedings of the National Academy of Sciences, USA 113, 11354-11359.
87. Pires ND, Yi K, Breuninger H, Catarino B, Menand B, Dolan L. 2013. Recruitment and remodeling of an ancient gene regulatory network during land plant evolution. Proceedings of the National Academy of Sciences, USA 110, 9571-9576.
88. Piya S, Shrestha SK, Binder B, Stewart CN Jr, Hewezi T. 2014. Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Frontiers in Plant Science 5, 744.
89. Plackett AR, Rabbinowitsch EH, Langdale JA. 2015. Protocol: genetic transformation of the fern Ceratopteris richardii through microparticle bombardment. Plant Methods 11, 37.
90. Plavskin Y, Nagashima A, Perroud PF, Hasebe M, Quatrano RS, Atwal GS, Timmermans MC. 2016. Ancient trans-Acting siRNAs confer robustness and sensitivity onto the auxin response. Developmental Cell 36, 276-289.
91. Prigge MJ, Greenham K, Zhang Y, Santner A, Castillejo C, Mutka AM, OMalley RC, Ecker JR, Kunkel BN, Estelle M. 2016. The arabidopsis auxin receptor F-box proteins AFB4 and AFB5 are required for response to the synthetic auxin picloram. G3: Genes Genomes Genetics 6, 1383-1390.
92. Prigge MJ, Lavy M, Ashton NW, Estelle M. 2010. Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxinsignaling pathway. Current Biology 20, 1907-1912.
93. Proust H, Honkanen S, Jones VA, Morieri G, Prescott H, Kelly S, Ishizaki K, Kohchi T, Dolan L. 2016. RSL class I genes controlled the development of epidermal structures in the common ancestor of land plants. Current Biology 26, 93-99.
94. Rademacher EH, Lokerse AS, Schlereth A, et al. 2012. Different auxin response machineries control distinct cell fates in the early plant embryo. Developmental Cell 22, 211-222.
95. Rademacher EH, Möller B, Lokerse AS, Llavata-Peris CI, van den Berg W, Weijers D. 2011. A cellular expression map of the Arabidopsis AUXIN RESPONSE FACTOR gene family. The Plant Journal 68, 597-606.
96. Ramos JA, Zenser N, Leyser O, Callis J. 2001. Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. The Plant Cell 13, 2349-2360.
97. Rensing SA. 2017. Why we need more non-seed plant models. New Phytologist, in press. doi:10.1111/nph.14464.
98. Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, Van de Peer Y, Reski R. 2007. An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evolutionary Biology 7, 130.
99. Rensing SA, Lang D, Zimmer AD, et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69.
100. Rousseau J. 1950. Action de lacide indol beta-Acétique sur les propagules de Marchantia polymorpha et Lunularia cruciata. Comptes Rendus Hebdomadaires des Séances de lAcadémie des Sciences 230, 675-676.
101. Rousseau J. 1951a. Action de lacide alpha napthaléne acétique sur les corbeilles á propagules de Marchantia polymorpha L. et de Lunularia cruciata Adans. Comptes Rendus Hebdomadaires des Séances de lAcadémie des Sciences 232, 107-108.
102. Rousseau J. 1951b. Action des acides 2.4-dichloro-phénoxy-Acétique et 2.5-dichloro-Thio-Acétique sur les propagules de Marchantia polymorpha L. Comptes Rendus Hebdomadaires des Séances de lAcadémie des Sciences 232, 749-751.
103. Rousseau J. 1953. Action des hetero-Auxines sur les chapeaux du Marchantia polymorpha L. Bulletin de la Société Botanique de France 100, 179-180.
104. Sakakibara K, Nishiyama T, Sumikawa N, Kofuji R, Murata T, Hasebe M. 2003. Involvement of auxin and a homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130, 4835-4846.
105. Sanders HL, Langdale JA. 2013. Conserved transport mechanisms but distinct auxin responses govern shoot patterning in Selaginella kraussiana. New Phytologist 198, 419-428.
106. Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jörgens G, Weijers D. 2010. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913-916.
107. Shimamura M. 2016. Marchantia polymorpha: Taxonomy, phylogeny and morphology of a model system. Plant & Cell Physiology 57, 230-256.
108. Shimizu-Mitao Y, Kakimoto T. 2014. Auxin sensitivities of all Arabidopsis Aux/IAAs for degradation in the presence of every TIR1/AFB. Plant & Cell Physiology 55, 1450-1459.
109. Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP. 2007. The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. The Plant Cell 19, 2440-2453.
110. Simonini S, Deb J, Moubayidin L, Stephenson P, Valluru M, Freire-Rios A, Sorefan K, Weijers D, Friml J, Østergaard L. 2016. A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis. Genes & Development 30, 2286-2296.
111. Sørensen I, Fei Z, Andreas A, Willats WG, Domozych DS, Rose JK. 2014. Stable transformation and reverse genetic analysis of Penium margaritaceum: A platform for studies of charophyte green algae, the immediate ancestors of land plants. The Plant Journal 77, 339-351.
112. Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I, Kohchi T. 2014. CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant & Cell Physiology 55, 475-481.
113. Szemenyei H, Hannon M, Long JA. 2008. TOPLESS mediates auxindependent transcriptional repression during Arabidopsis embryogenesis. Science 319, 1384-1386.
114. Sztein AE, Cohen JD, Cooke TJ. 2000. Evolutionary patterns in the auxin metabolism of green plants. International Journal of Plant Sciences 161, 849-859.
115. Tam TH, Catarino B, Dolan L. 2015. Conserved regulatory mechanism controls the development of cells with rooting functions in land plants. Proceedings of the National Academy of Sciences, USA 112, E3959-E3968.
116. Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT. 2004. MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. The Plant Cell 16, 379-393.
117. ten Hove CA, Lu KJ, Weijers D. 2015. Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142, 420-430.
118. Tian Q, Reed JW. 1999. Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126, 711-721.
119. Timme RE, Bachvaroff TR, Delwiche CF. 2012. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7, e29696.
120. Tsuzuki M, Nishihama R, Ishizaki K, Kurihara Y, Matsui M, Bowman JL, Kohchi T, Hamada T, Watanabe Y. 2016. Profiling and characterization of small RNAs in the liverwort, Marchantia polymorpha, belonging to the first diverged land plants. Plant & Cell Physiology 57, 359-372.
121. Turmel M, Otis C, Lemieux C. 2006. The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Molecular Biology and Evolution 23, 1324-1338.
122. Turnaev II, Gunbin KV, Afonnikov DA. 2015. Plant auxin biosynthesis did not originate in charophytes. Trends in Plant Science 20, 463-465.
123. Ulmasov T, Hagen G, Guilfoyle TJ. 1997. ARF1, a transcription factor that binds to auxin response elements. Science 276, 1865-1868.
124. Ulmasov T, Hagen G, Guilfoyle TJ. 1999a. Activation and repression of transcription by auxin response factors. Proceedings of the National Academy of Sciences, USA 96, 5844-5849.
125. Ulmasov T, Hagen G, Guilfoyle TJ. 1999b. Dimerization and DNA binding of auxin response factors. The Plant Journal 19, 309-319.
126. Varaud E, Brioudes F, Szécsi J, Leroux J, Brown S, Perrot-Rechenmann C, Bendahmane M. 2011. AUXIN RESPONSE FACTOR8 regulates Arabidopsis petal growth by interacting with the bHLH transcription factor BIGPETALp. The Plant Cell 23, 973-983.
127. Vernoux T, Brunoud G, Farcot E, et al. 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Molecular Systems Biology 7, 508.
128. Viaene T, Landberg K, Thelander M, et al. 2014. Directional auxin transport mechanisms in early diverging land plants. Current Biology 24, 2786-2791.
129. Wang C, Liu Y, Li SS, Han GZ. 2015. Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiology 167, 872-886.
130. Wang JJ, Guo HS. 2015. Cleavage of INDOLE-3-ACETIC ACID INDUCIBLE28 mRNA by microRNA847 upregulates auxin signaling to modulate cell proliferation and lateral organ growth in Arabidopsis. The Plant Cell 27, 574-590.
131. Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY. 2005. Control of root cap formation by microRNA-Targeted auxin response factors in Arabidopsis. The Plant Cell 17, 2204-2216.
132. Weijers D, Benkova E, Jäger KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jörgens G. 2005. Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. The EMBO Journal 24, 1874-1885.
133. Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jörgens G. 2006. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Developmental Cell 10, 265-270.
134. Wickett NJ, Mirarab S, Nguyen N, et al. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences, USA 111, E4859-E4868.
135. Williams L, Carles CC, Osmont KS, Fletcher JC. 2005. A database analysis method identifies an endogenous trans-Acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proceedings of the National Academy of Sciences, USA 102, 9703-9708.
136. Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B. 2011. Origin of land plants: do conjugating green algae hold the key? BMC Evolutionary Biology 11, 104.
137. Wu MF, Tian Q, Reed JW. 2006. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211-4218.
138. Xia R, Xu J, Arikit S, Meyers BC. 2015. Extensive families of miRNAs and PHAS loci in Norway spruce demonstrate the origins of complex phasiRNA networks in seed plants. Molecular Biology and Evolution 32, 2905-2918.
139. Xia R, Xu J, Meyers BC. 2017. The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants. The Plant Cell 29, 1232-1247.
140. Yang J, Tian L, Sun MX, Huang XY, Zhu J, Guan YF, Jia QS, Yang ZN. 2013. AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiology 162, 720-731.
141. Yi K, Menand B, Bell E, Dolan L. 2010. A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nature Genetics 42, 264-267.
142. Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P, Smith RS, Weijers D. 2014. Genetic control of plant development by overriding a geometric division rule. Developmental Cell 29, 75-87.
143. Yu H, Zhang Y, Moss BL, Bargmann BO, Wang R, Prigge M, Nemhauser JL, Estelle M. 2015. Untethering the TIR1 auxin receptor from the SCF complex increases its stability and inhibits auxin response. Nature Plants 1, 14030.
144. Yue J, Hu X, Huang J. 2014. Origin of plant auxin biosynthesis. Trends in Plant Science 19, 764-770.
145. Zhang Q, Li J, Sang Y, Xing S, Wu Q, Liu X. 2015. Identification and characterization of microRNAs in Ginkgo biloba var. epiphylla Mak. PLoS ONE 10, e0127184.
146. Zhang S, van Duijn B. 2014. Cellular auxin transport in algae. Plants 3, 58-69.
147. Zižková E, Kubeš M, Dobrev PI, Přibyl P, Šimura J, Zahajská L, Záveská Drábková L, Novák O, Motyka V. 2017. Control of cytokinin and auxin homeostasis in cyanobacteria and algae. Annals of Botany 119, 151-166.