Adaxial-abaxial polarity: The developmental basis of leaf shape diversity

Genesis

Volumn 52, Issue 1, 2014, Pages 1-18

  Fukushima, Kenji ^a,b   Hasebe, Mitsuyasu ^a,b  

^a The Graduate University for Advanced Studies   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

Bifacial leaf; Leaf type; Peltate leaf; Unifacial leaf

Indexed keywords

ARTICLE; LEAF STRUCTURE; MORPHOGENESIS; PLANT LEAF; PRIMORDIUM; PRIORITY JOURNAL; TISSUE DIFFERENTIATION;

MAGNOLIOPHYTA;

BIFACIAL LEAF; LEAF TYPE; PELTATE LEAF; UNIFACIAL LEAF;

ANGIOSPERMS; CELL POLARITY; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; PLANT LEAVES; PLANT PROTEINS;

EID: 84892894669     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22728     Document Type: Article

References (160)

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 16:927-932.
2. Albert VA, Williams SE, Chase MW. 1992. Carnivorous plants: Phylogeny and structural evolution. Science 257:1491-1495.
3. Allen E, Xie Z, Gustafson AM, Carrington JC. 2005. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207-221.
4. Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J, Fleck C, Lenhard M. 2007. Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev Cell 13:843-856.
5. Arber A. 1918. The phyllode theory of the monocotyledonous leaf, with special reference to anatomical evidence. Ann Bot os-32:465-501.
6. Arber A. 1921. The leaf structure of the Iridaceae, considered in relation to the phyllode theory. Ann Bot os-35:301-336.
7. Arber A. 1923. Leaves of the Gramineae. Bot Gaz 76:374-388.
8. Böcher TW. 1981. Evolutionary trends in Ericalean leaf structure. Biol Skr kgl danske Vidensk Selsk 23:1-64.
9. Becker A, Lange M. 2010. VIGS-genomics goes functional. Trends Plant Sci 15:1-4.
10. Bell AD, Bryan A. 2008. Plant form: An illustrated guide to flowering plant morphology. London: Timber Press.
11. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. 1998. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170-180.
12. Boke NH. 1940. Histogenesis and morphology of the phyllode in certain species of Acacia. Am J Bot 27:73-90.
13. Bonaccorso O, Lee JE, Puah L, Scutt CP, Golz JF. 2012. FILAMENTOUS FLOWER controls lateral organ development by acting as both an activator and a repressor. BMC Plant Biol 12:1471-2229.
14. Bowman J. 1994. ARABIDOPSIS: An atlas of morphology and development. New York: Springer.
15. Braybrook SA, Kuhlemeier C. 2010. How a plant builds leaves. Plant Cell 22:1006-1018.
16. Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA. 2000. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967-971.
17. Candela H, Johnston R, Gerhold A, Foster T, Hake S. 2008. The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves. Plant Cell 20:2073-2087.
18. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén 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 465:316-321.
19. Charlton WA. 1993. The rotated-lamina syndrome. I. Ulmaceae. Can J Bot 71:211-221.
20. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC. 2009. Pattern formation via small RNA mobility. Genes Dev 23:549-554.
21. Cho S-H, Yoo S-C, Zhang H, Pandeya D, Koh H-J, Hwang J-Y, Kim G-T, Paek N-C. 2013. The rice narrow leaf2 and narrow leaf3 loci encode WUSCHEL-related homeobox 3A (OsWOX3A) and function in leaf, spikelet, tiller and lateral root development. New Phytol 198:1071-1084.
22. Cunninghame ME, Lyndon RF. 1986. The relationship between the distribution of periclinal cell divisions in the shoot apex and leaf initiation. Ann Bot 57:737-746.
23. Dai M, Hu Y, Zhao Y, Liu H, Zhou DX. 2007. A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 144:380-390.
24. De Vries H. 1905. Species and varieties: Their origin by mutation. Chicago: The Open Court Publishing Co.
25. Dengler N, Kang J. 2001. Vascular patterning and leaf shape. Curr Opin Plant Biol 4:50-56.
26. DeWitte A, Twyford A, Thomas D, Kidner C, Van Huylenbroeck J. 2011. The origin of diversity in Begonia: Genome dynamism, population processes and phylogenetic patterns. In: Grillo O, Venora G, editors. The dynamical processes of biodiversity-Case studies of evolution and spatial distribution, Rijeka: InTech. pp 27-52.
27. Douglas RN, Wiley D, Sarkar A, Springer N, Timmermans MC, Scanlon MJ. 2010. ragged seedling2 Encodes an ARGONAUTE7-like protein required for mediolateral expansion, but not dorsiventrality, of maize leaves. Plant Cell 22:1441-1451.
28. 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 328:912-916.
29. Ellison AM, Gotelli NJ. 2002. Nitrogen availability alters the expression of carnivory in the northern pitcher plant, Sarracenia purpurea. Proc Natl Acad Sci USA 99:4409-4412.
30. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768-1774.
31. Esau K. 1977. Anatomy of Seed Plants. New York: Wiley.
32. Eshed Y, Baum SF, Bowman JL. 1999. Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199-209.
33. Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL. 2004. Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997-3006.
34. Finet C, Berne-Dedieu A, Scutt CP, Marletaz F. 2013. Evolution of the ARF gene family in land plants: Old domains, new tricks. Mol Biol Evol 30:45-56.
35. Finet C, Fourquin C, Vinauger M, Berne-Dedieu A, Chambrier P, Paindavoine S, Scutt CP. 2010. Parallel structural evolution of auxin response factors in the angiosperms. Plant J 63:952-959.
36. Franck D. 1976. The morphological interpretation of epiascidiate leaves-An historical perspective. Bot Rev 42:345-388.
37. Fu Y, Xu L, Xu B, Yang L, Ling Q, Wang H, Huang H. 2007. Genetic interactions between leaf polarity-controlling genes and ASYMMETRIC LEAVES1 and 2 in Arabidopsis leaf patterning. Plant Cell Physiol 48:724-735.
38. Garcia D, Collier SA, Byrne ME, Martienssen RA. 2006. Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933-938.
39. Givnish TJ, Vermeij GJ. 1976. Sizes and shapes of liane leaves. Am Nat 110:743-778.
40. Gleissberg S, Groot EP, Schmalz M, Eichert M, Kolsch A, Hutter S. 2005. Developmental events leading to peltate leaf structure in Tropaeolum majus (Tropaeolaceae) are associated with expression domain changes of a YABBY gene. Dev Genes Evol 215:313-319.
41. Golz JF, Roccaro M, Kuzoff R, Hudson A. 2004. GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131:3661-3670.
42. Groff PA, Kaplan DR. 1988. The relation of root systems to shoot systems in vascular plants. Bot Rev 54:387-422.
43. Hagemann W, Gleissberg S. 1996. Organogenetic capacity of leaves: The significance of marginal blastozones in angiosperms. Plant Syst Evol 199:121-152.
44. Hagerup O. 1946. Studies on the Empetraceae. Kgl danske Vidensk Selsk biol Medd 20:1-49.
45. Hillson CJ. 1979. Leaf development in Senecio rowleyanus (Compositae). Am J Bot 66:59-63.
46. Hofer J, Turner L, Moreau C, Ambrose M, Isaac P, Butcher S, Weller J, Dupin A, Dalmais M, Le Signor C, Bendahmane A, Ellis N. 2009. Tendril-less regulates tendril formation in pea leaves. Plant Cell 21:420-428.
47. Huang W, Pi L, Liang W, Xu B, Wang H, Cai R, Huang H. 2006. The proteolytic function of the Arabidopsis 26S proteasome is required for specifying leaf adaxial identity. Plant Cell 18:2479-2492.
48. Ishiwata A, Ozawa M, Nagasaki H, Kato M, Noda Y, Yamaguchi T, Nosaka M, Shimizu-Sato S, Nagasaki A, Maekawa M, Hirano H-Y, Sato Y. 2013. Two WUSCHEL-related homeobox genes, narrow leaf2 and narrow leaf3, control leaf width in rice. Plant Cell Physiol 54:779-792.
49. Iwasaki M, Takahashi H, Iwakawa H, Nakagawa A, Ishikawa T, Tanaka H, Matsumura Y, Pekker I, Eshed Y, Vial-Pradel S, Ito T, Watanabe Y, Ueno Y, Fukazawa H, Kojima S, Machida Y, Machida C. 2013. Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis. Development 140:1958-1969.
50. James SA, Bell DT. 2000. Leaf orientation, light interception and stomatal conductance of Eucalyptus globulus ssp. globulus leaves. Tree Physiology 20:815-823.
51. Johnston R, Candela H, Hake S, Foster T. 2010. The maize milkweed pod1 mutant reveals a mechanism to modify organ morphology. genesis 48:416-423.
52. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC. 2004a. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84-88.
53. Juarez MT, Twigg RW, Timmermans MCP. 2004b. Specification of adaxial cell fate during maize leaf development. Development 131:4533-4544.
54. Juniper BE, Robins RJ, Joel DM. 1989. The carnivorous plants. London: Academic Press.
55. Kaplan D. 1975. Comparative developmental evaluation of the morphology of unifacial leaves in the monocotyledons. Bot Jahrb Syst 95:1-105.
56. Kaplan DR. 1970. Comparative foliar histogenesis in Acorus calamus and its bearing on the phyllode theory of monocotyledonous leaves. Am J Bot 57:331-361.
57. Kaplan DR. 1973. The problem of leaf morphology and evolution in the monocotyledons. Q Rev Biol 48:437-457.
58. Kaplan DR. 2001. Fundamental concepts of leaf morphology and morphogenesis: A contribution to the interpretation of molecular genetic mutants. Int J Plant Sci 162:465-474.
59. Kaul RB. 1977. The role of the multiple epidermis in foliar succulence of Peperomia (Piperaceae). Bot Gaz 138:213-218.
60. 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.
61. Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS. 2001. KANADI regulates organ polarity in Arabidopsis. Nature 411:706-709.
62. Kidner CA, Martienssen RA. 2004. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428:81-84.
63. Kidner CA, Wrigley S. 2010. Patches, pegs and piggies. New Phytol 187:13-17.
64. Kim M, McCormick S, Timmermans M, Sinha N. 2003a. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424:438-443.
65. Kim M, Pham T, Hamidi A, McCormick S, Kuzoff RK, Sinha N. 2003b. Reduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves. Development 130:4405-4415.
66. Kojima S, Iwasaki M, Takahashi H, Imai T, Matsumura Y, Fleury D, Van Lijsebettens M, Machida Y, Machida C. 2011. ASYMMETRIC LEAVES2 and Elongator, a histone acetyltransferase complex, mediate the establishment of polarity in leaves of Arabidopsis thaliana. Plant Cell Physiol 52:1259-1273.
67. Korn RW. 2010. Naturally occurring ectopic growths in certain Xanthosoma and Begonia cultivars and the problem of leaf dorsiventral polarity. New Phytol 187:9-13.
68. Kron K, Judd W, Stevens P, Crayn D, Anderberg A, Gadek P, Quinn C, Luteyn J. 2002. Phylogenetic classification of Ericaceae: Molecular and morphological evidence. Bot Rev 68:335-423.
69. La Rota C, Chopard J, Das P, Paindavoine S, Rozier F, Farcot E, Godin C, Traas J, Moneger F. 2011. A data-driven integrative model of sepal primordium polarity in Arabidopsis. Plant Cell 23:4318-4333.
70. Levine E, McHale P, Levine H. 2007. Small regulatory RNAs may sharpen spatial expression patterns. PLoS Comput Biol 3:e233.
71. Li H, Xu L, Wang H, Yuan Z, Cao X, Yang Z, Zhang D, Xu Y, Huang H. 2005. The Putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis leaf development. Plant Cell 17:2157-2171.
72. Liu Q, Yao X, Pi L, Wang H, Cui X, Huang H. 2009. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J 58:27-40.
73. Magnani E, Barton MK. 2011. A per-ARNT-sim-like sensor domain uniquely regulates the activity of the homeodomain leucine zipper transcription factor REVOLUTA in Arabidopsis. Plant Cell 23:567-582.
74. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP. 2004. MicroRNA control of PHABULOSA in leaf development: Importance of pairing to the microRNA 5′ region. EMBO J 23:3356-3364.
75. McConnell JR, Barton MK. 1998. Leaf polarity and meristem formation in Arabidopsis. Development 125:2935-2942.
76. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK. 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709-713.
77. McHale NA. 1993. LAM-1 and FAT genes control development of the leaf blade in Nicotiana sylvestris. Plant Cell 5:1029-1038.
78. McHale NA, Koning RE. 2004a. MicroRNA-directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems. Plant Cell 16:1730-1740.
79. McHale NA, Koning RE. 2004b. PHANTASTICA regulates development of the adaxial mesophyll in Nicotiana leaves. Plant Cell 16:1251-1262.
80. Mecchia MA, Debernardi JM, Rodriguez RE, Schommer C, Palatnik JF. 2013. MicroRNA miR396 and RDR6 synergistically regulate leaf development. Mech Dev 130:2-13.
81. Miyashima S, Honda M, Hashimoto K, Tatematsu K, Hashimoto T, Sato-Nara K, Okada K, Nakajima K. 2013. A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function. Plant Cell Physiol 54:375-384.
82. Miyashima S, Koi S, Hashimoto T, Nakajima K. 2011. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303-2313.
83. 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 328:872-875.
84. Nagasaki H, Itoh J, Hayashi K, Hibara K, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y. 2007. The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci USA 104:14867-14871.
85. Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K. 2012. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24:519-535.
86. Nardmann J, Ji J, Werr W, Scanlon MJ. 2004. The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827-2839.
87. Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W. 2007. WOX gene phylogeny in Poaceae: A comparative approach addressing leaf and embryo development. Mol Biol Evol 24:2474-2484.
88. Neale S, Goodall-Copestake W, Kidner C, Teixeira da Silva J. 2006. The evolution of diversity in Begonia. In: JA TdS, editor. Floriculture, ornamental and plant biotechnology: Advances and topical issues. London: Global Science Books. pp 606-611.
89. Nishimura T, Wada T, Okada K. 2004. A key factor of translation reinitiation, ribosomal protein L24, is involved in gynoecium development in Arabidopsis. Biochem Soc Trans 32:611-613.
90. Nishimura T, Wada T, Yamamoto KT, Okada K. 2005. The Arabidopsis STV1 protein, responsible for translation reinitiation, is required for auxin-mediated gynoecium patterning. Plant Cell 17:2940-2953.
91. Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC. 2007. Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21:750-755.
92. Ozerova LV, Timonin AC. 2009. On the evidence of subunifacial and unifacial leaves: Developmental studies in leaf-succulent Senecio L. species (Asteraceae). Wulfenia 16:61-77.
93. Pekker I, Alvarez JP, Eshed Y. 2005. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899-2910.
94. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE. 2005. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61-76.
95. Reinhardt D, Frenz M, Mandel T, Kuhlemeier C. 2005. Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato. Development 132:15-26.
96. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. 2002. Prediction of plant microRNA targets. Cell 110:513-520.
97. Rosado A, Li R, van de Ven W, Hsu E, Raikhel NV. 2012. Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors. Proc Natl Acad Sci USA 109:19537-19544.
98. Rudall PJ, Buzgo M. 2002. Evolutionary history of the monocot leaf. In: Cronk QCB, Bateman RM, Hawkins JA, editors. Developmental genetics and plant evolution. London: Taylor and Francis. pp 431-458.
99. Sarojam R, Sappl PG, Goldshmidt A, Efroni I, Floyd SK, Eshed Y, Bowman JL. 2010. Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell 22:2113-2130.
100. Sawa S, Watanabe K, Goto K, Liu YG, Shibata D, Kanaya E, Morita EH, Okada K. 1999. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev 13:1079-1088.
101. Scanlon MJ, Chen KD, McKnight CI. 2000. The narrow sheath duplicate genes: Sectors of dual aneuploidy reveal ancestrally conserved gene functions during maize leaf development. Genetics 155:1379-1389.
102. Scanlon MJ, Freeling M. 1997. Clonal sectors reveal that a specific meristematic domain is not utilized in the maize mutant narrow sheath. Dev Biol 182:52-66.
103. Scanlon MJ, Schneeberger RG, Freeling M. 1996. The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 122:1683-1691.
104. Schneeberger R, Tsiantis M, Freeling M, Langdale JA. 1998. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125:2857-2865.
105. Schwab R, Maizel A, Ruiz-Ferrer V, Garcia D, Bayer M, Crespi M, Voinnet O, Martienssen RA. 2009. Endogenous tasiRNAs mediate non-cell autonomous effects on gene regulation in Arabidopsis thaliana. PLoS One 4:e5980.
106. Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y. 2001. The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128:1771-1783.
107. Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC. 1997. ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124:4481-4491.
108. Sessions RA, Zambryski PC. 1995. Arabidopsis gynoecium structure in the wild and in ettin mutants. Development 121:1519-1532.
109. Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL. 1999. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117-4128.
110. Snow M, Snow R. 1959. The dorsiventrality of leaf primordia. New Phytol 58:188-207.
111. Snow R, Snow M. 1954. Experiments on the cause of dorsiventrality in leaves. Nature 174:352-353.
112. Soma S. 1965. Developmental studies on the orientation and the dorsiventrality of the leaf of Zelkova serrata Makino. J Fac Sci Univ Tokyo Sec III Bot 9:1-17.
113. Stahle MI, Kuehlich J, Staron L, von Arnim AG, Golz JF. 2009. YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21:3105-3118.
114. Steeves TA, Sussex IM. 1989. Patterns in Plant Development. New York: Cambridge University Press.
115. Sun Y, Zhou Q, Zhang W, Fu Y, Huang H. 2002. ASYMMETRIC LEAVES1, an Arabidopsis gene that is involved in the control of cell differentiation in leaves. Planta 214:694-702.
116. Sussex IM. 1951. Experiments on the cause of dorsiventrality in leaves. Nature 167:651-652.
117. Sussex IM. 1954. Experiments on the cause of dorsiventrality in leaves. Nature 174:351-352.
118. Sussex IM. 1955. Morphogenesis in Solanum tuberosum L.: Experimental investigation of leaf dorsiventrality and orientation in the juvenile shoot. Phytomorphology 5:286-300.
119. Tadege M, Lin H, Bedair M, Berbel A, Wen J, Rojas CM, Niu L, Tang Y, Sumner L, Ratet P, McHale NA, Madueno F, Mysore KS. 2011. STENOFOLIA regulates blade outgrowth and leaf vascular patterning in Medicago truncatula and Nicotiana sylvestris. Plant Cell 23:2125-2142.
120. Talbert PB, Adler HT, Parks DW, Comai L. 1995. The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121:2723-2735.
121. Tameshige T, Fujita H, Watanabe K, Toyokura K, Kondo M, Tatematsu K, Matsumoto N, Tsugeki R, Kawaguchi M, Nishimura M, Okada K. 2013. Pattern dynamics in adaxial-abaxial specific gene expression are modulated by a plastid retrograde signal during Arabidopsis thaliana leaf development. PLoS Genet 9:e1003655.
122. Tang G, Reinhart BJ, Bartel DP, Zamore PD. 2003. A biochemical framework for RNA silencing in plants. Genes Dev 17:49-63.
123. Tattersall AD, Turner L, Knox MR, Ambrose MJ, Ellis TH, Hofer JM. 2005. The mutant crispa reveals multiple roles for PHANTASTICA in pea compound leaf development. Plant Cell 17:1046-1060.
124. Tepfer SS. 1960. The shoot apex and early leaf development in Clematis. Am J Bot 47:655-664.
125. Timmermans MC, Hudson A, Becraft PW, Nelson T. 1999. ROUGH SHEATH2: A Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284:151-153.
126. Toriba T, Ohmori Y, Hirano H-Y. 2011. Common and distinct mechanisms underlying the establishment of adaxial and abaxial polarity in stamen and leaf development. Plant Signal Behav 6:430-433.
127. Toriba T, Suzaki T, Yamaguchi T, Ohmori Y, Tsukaya H, Hirano HY. 2010. Distinct regulation of adaxial-abaxial polarity in anther patterning in rice. Plant Cell 22:1452-1462.
128. Toyokura K, Watanabe K, Oiwaka A, Kusano M, Tameshige T, Tatematsu K, Matsumoto N, Tsugeki R, Saito K, Okada K. 2011. Succinic semialdehyde dehydrogenase is involved in the robust patterning of Arabidopsis leaves along the adaxial-abaxial axis. Plant Cell Physiol 52:1340-1353.
129. Troll W. 1932. Morphologie der schildförmigen Blätter. Planta 17:231-314.
130. Tsiantis M, Schneeberger R, Golz JF, Freeling M, Langdale JA. 1999. The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284:154-156.
131. Tsukaya H. 2013. Leaf development. In: The Arabidopsis book. Rockville: The American Society of Plant Biologists. p e0163.
132. Turchi L, Carabelli M, Ruzza V, Possenti M, Sassi M, Penalosa A, Sessa G, Salvi S, Forte V, Morelli G, Ruberti I 2013. Arabidopsis HD-Zip II transcription factors control apical embryo development and meristem function. Development 140:2118-2129.
133. Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS, Gerats T. 2009. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell 21:2269-2283.
134. Vatén A, Dettmer J, Wu S, Stierhof YD, Miyashima S, Yadav SR, Roberts CJ, Campilho A, Bulone V, Lichtenberger R, Lehesranta S, Mähönen AP, Kim JY, Jokitalo E, Sauer N, Scheres B, Nakajima K, Carlsbecker A, Gallagher KL, Helariutta Y. 2011. Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21:1144-1155.
135. Waites R, Hudson A. 1995. phantastica: A gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143-2154.
136. Waites R, Selvadurai HR, Oliver IR, Hudson A. 1998. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93:779-789.
137. Wang W, Xu B, Wang H, Li J, Huang H, Xu L. 2011. YUCCA genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiol 157:1805-1819.
138. Weber JN, Peterson BK, Hoekstra HE. 2013. Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice. Nature 493:402-405.
139. Wenkel S, Emery J, Hou BH, Evans MM, Barton MK. 2007. A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell 19:3379-3390.
140. 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. Proc Natl Acad Sci USA 102:9703-9708.
141. Wu G, Lin WC, Huang T, Poethig RS, Springer PS, Kerstetter RA. 2008. KANADI1 regulates adaxial-abaxial polarity in Arabidopsis by directly repressing the transcription of ASYMMETRIC LEAVES2. Proc Natl Acad Sci USA 105:16392-16397.
142. Xu D, Huang W, Li Y, Wang H, Huang H, Cui X. 2012. Elongator complex is critical for cell cycle progression and leaf patterning in Arabidopsis. Plant J 69:792-808.
143. Xu L, Xu Y, Dong A, Sun Y, Pi L, Huang H. 2003. Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130:4097-4107.
144. Xu L, Yang L, Pi L, Liu Q, Ling Q, Wang H, Poethig RS, Huang H. 2006. Genetic interaction between the AS1-AS2 and RDR6-SGS3-AGO7 pathways for leaf morphogenesis. Plant Cell Physiol 47:853-863.
145. Xu Y, Sun Y, Liang WQ, Huang H. 2002. The Arabidopsis AS2 gene encoding a predicted leucine-zipper protein is required for the leaf polarity formation. Acta Bot Sin 44:1194-1202.
146. Yamada T, Yokota S, Hirayama Y, Imaichi R, Kato M, Gasser CS. 2011. Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms. Plant J 67:26-36.
147. Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY. 2004. The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500-509.
148. Yamaguchi T, Tsukaya H. 2010. Evolutionary and developmental studies of unifacial leaves in monocots: Juncus as a model system. J Plant Res 123:35-41.
149. Yamaguchi T, Yano S, Tsukaya H. 2010. Genetic framework for flattened leaf blade formation in unifacial leaves of Juncus prismatocarpus. Plant Cell 22:2141-2155.
150. Yan S, Yan CJ, Zeng XH, Yang YC, Fang YW, Tian CY, Sun YW, Cheng ZK, Gu MH. 2008. ROLLED LEAF 9, encoding a GARP protein, regulates the leaf abaxial cell fate in rice. Plant Mol Biol 68:239-250.
151. Yang L, Huang W, Wang H, Cai R, Xu Y, Huang H. 2006. Characterizations of a hypomorphic argonaute1 mutant reveal novel AGO1 functions in Arabidopsis lateral organ development. Plant Mol Biol 61:63-78.
152. Yao X, Wang H, Li H, Yuan Z, Li F, Yang L, Huang H. 2009. Two types of cis-acting elements control the abaxial epidermis-specific transcription of the MIR165a and MIR166a genes. FEBS Lett 583:3711-3717.
153. Yifhar T, Pekker I, Peled D, Friedlander G, Pistunov A, Sabban M, Wachsman G, Alvarez JP, Amsellem Z, Eshed Y. 2012. Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24:3575-3589.
154. Yuan Z, Luo D, Li G, Yao X, Wang H, Zeng M, Huang H, Cui X. 2010. Characterization of the AE7 gene in Arabidopsis suggests that normal cell proliferation is essential for leaf polarity establishment. Plant J 64:331-342.
155. Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW. 2009. SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719-735.
156. Zhang X, Zong J, Liu J, Yin J, Zhang D. 2010. Genome-wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. J Integr Plant Biol 52:1016-1026.
157. Zhong R, Ye ZH. 2004. amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol 45:369-385.
158. Zhu H, Hu F, Wang R, Zhou X, Sze SH, Liou LW, Barefoot A, Dickman M, Zhang X. 2011. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145:242-256.
159. Zhuang LL, Ambrose M, Rameau C, Weng L, Yang J, Hu XH, Luo D, Li X. 2012. LATHYROIDES, encoding a WUSCHEL-related Homeobox1 transcription factor, controls organ lateral growth, and regulates tendril and dorsal petal identities in garden pea (Pisum sativum L.). Mol Plant 5:1333-1345.
160. Zoulias N, Koenig D, Hamidi A, McCormick S, Kim M. 2012. A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves. Ann Bot 109:407-418.