Abstract
The leaf primordium derives from the peripheral zone of shoot apical meristem. During the formation of leaf primordia, they need to establish the proximodistal, mediolateral, and ab/adaxial axes. Among these axes, the ab/adaxial axis might be the most important. ASYMMETRIC LEAVES2 (AS2) gene is a member of AS2/LATERAL ORGAN BOUNDARY (LOB) family of Arabidopsis thaliana. In this work, we transformed 35S:AS2 transgene constructs to cockscomb (Celosia cristata) via Agrobacterium tumefaciens. All primary transformants subsequently obtained were placed into phenotypic categories and self-pollinated. As a whole, a total of 44 T1 35S:AS2 cockscomb plants obtained were grouped into two major categories: (I) slightly wrinkled leaves (28/44), (II) extremely curved leaves (16/44), on the basis of their leaf phenotypes. Furthermore, we characterized the anatomical features of these malformed leaves; and found the transformation of adaxial cell types into abaxial cell ones. A series of data suggest that AS2 might be involved in the determination of abaxial polarity in cockscomb plants. However, a few research teams have reported that AS2 might be involved in the determination of adaxial polarity in leaf primodia of Arabidopsis thaliana. These data above indicate that the roles of the same ab/adaxial determinant might differ between distinct species. At last, the different function of AS2 in distinct species was discussed.
Similar content being viewed by others
References
Hudson A (2000) Development of symmetry in plants. Annu Rev Plant Physiol Plant Mol Biol 51:349–370
Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141
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
Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209
Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260
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
Sawa S, Watanabe K, Goto K, 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
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
Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709
Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910
McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942
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
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
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
Kim YS, Kim SG, Lee M, Lee I, Park HY, Seo PJ, Jung JH, Kwon EJ, Suh SW, Paek KH, Park CM (2008) HD-ZIP III activity is modulated by competitive inhibitors via a feedback loop in Arabidopsis shoot apical meristem development. Plant Cell 20:920–933
Waites R, Hudson A (1995) Phantastica: a gene required for dorsiventrality of leaves in Antirrhinum majus. Development 121:2143–2154
Waites R, Hudson A (2001) The Handlebars gene is required with Phantastica for dorsoventral asymmetry of organs and for stem cell activity in Antirrhinum. Development 128:1923–1931
Redei GP, Hirono Y (1964) Linkage studies. Arabidopsis Inf Serv 1:9
Serrano-Cartagena J, Robles P, Ponce MR, Micol JL (1999) Genetic analysis of leaf form mutants from the Arabidopsis Information Service collection. Mol Gen Genet 261:725–739
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
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
Xu L, Xu Y, Dong A, Sun Y, Pi L, Xu Y, 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 adaxial identity. Development 130:4097–4107
Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478
Shuai B, Reynaga-Peña CG, Springer PS (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761
Husbands A, Bell EM, Shuai B, Smith HMS, Springer PS (2007) LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins. Nucleic Acids Res 35:6663–6671
Lin WC, Shuai B, Springer PS (2003) The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell 15:2241–2252
Ueno Y, Ishikawa T, Watanabe K, Terakura S, Iwakaw H, Okada K, Machida C, Machidaa Y (2007) Histone deacetylases and ASYMMETRIC LEAVES2 are involved in the establishment of polarity in leaves of Arabidopsis. Plant Cell 19:445–457
Iwakawa H, Iwasaki M, Kojima S et al (2007) Expression of the ASYMMETRIC LEAVES2 gene in the adaxial domain of Arabidopsis leaves represses cell proliferation in this domain and is critical for the development of properly expanded leaves. Plant Journal 51:173–184
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 ASYMMETRC LEAVES1 and 2 to repress BREVIPEDICELLUS and microRNA165/166 in Arabidopsis leaf development. Plant Cell 17:2157–2171
Matsumura Y, Iwakawa H, Machida Y, Machida C (2009) Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members. Plant J 58:525–537
Meng LS, Ding WQ, Hu X, Wang CY (2009) Transformation of PttKN1 gene to cockscomb. Acta Physiol Plant 31:683–691
Meng LS, Liu HL, Cui XH, Sun XD, Zhu J (2009) ASYMMETRIC LEAVES2-LIKE38 gene, a member of AS2/LOB family of Arabidopsis, causes leaf dorsoventral alternation in transgenic cockscomb plants. Acta Physiol Plant 31:1301–1306
Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965
Meng LS, Song JP, Sun SB, Wang CY (2009) The ectopic expression of PttKN1 gene causes pleiotropic alternation of morphology in transgenic carnation (Dianthus caryophyllus L.). Acta Physiol Plant 31:1155–1164
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Fuchs C (1963) Fuchsin staining with NaOH clearing for lignified elements of whole plants or plant organs. Stain Technol 38:141–144
Sun SB, Meng LS, Sun XD, Feng ZH (2010) Using high competent shoot apical meristems of cockscomb as explants for studying function of ASYMMETRIC LEAVES2-LIKE11 (ASL11) gene of Arabidopsis. Mol Biol Rep 37:3973–3982
Wabiko H, Minemura M (1996) Exogenous phytohormone-independent growth and regeneration of tobacco plants transgenic for the 6b gene of Agrobacterium tumefaciens AKE10. Plant Physiol 112:939–951
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105
Pena L, Martin-Trillo M, Juarez J, Pina JA, Navarro L, Martinez-Zapater JM (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat Biotechnol 19:263–267
Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M (2005) Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 14:703–712
Chitwood DH, Guo M, Nogueira FTS, Timmermans MCP (2007) Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex. Development 134:813–823
Golz JF, Roccaro M, Kuzoff R, Hudson A (2004) GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131:3661–3670
Byrne ME (2005) Networks in leaf development. Curr Opin Plant Biol 8:59–66
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
Ha CM, Jun JH, Nam HG, Fletcher JC (2007) BLADE-ON-PETIOLE1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 19:1809–1825
Author information
Authors and Affiliations
Corresponding author
Additional information
S.-B. Sun and J.-P. Song contributed equally to this work.
Rights and permissions
About this article
Cite this article
Sun, SB., Song, JP. & Meng, LS. ASYMMETRIC LEAVES2 gene, a member of LOB/AS2 family of Arabidopsis thaliana, causes an abaxializing leaves in transgenic cockscomb. Mol Biol Rep 39, 4927–4935 (2012). https://doi.org/10.1007/s11033-011-1288-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-011-1288-y