Abstract
Though shoot apical meristems (SAMs) commonly exhibit low or no competence for transformation, the potent regeneration of this tissue merits further research. Especially, when shoot regeneration is recalcitrant using other tissues as explants, SAM probably is an excellent selection. In cockscomb plants, using SAMs from seedlings obtained from MS medium with 0.5 mg l−1 6-BA as explants, high frequency of transformation (approximate 20%) is obtained; whereas control SAMs performed poorly for transformation (approximate 3%). These SAMs are malformed in morphology compared to control SAMs. Further observation found that, in these SAMs, cell proliferation and/or TE formation are seen; which are not found in control SAMs. GUS assays indicated that GUS-positive blue spots at TE zones are obvious; whereas the case was contrary in control SAMs. All these data suggest that cell proliferation and/or TE formation might cause high effective transformation. This transformation system should facilitate the use of this species for studies on gene manipulation and expression. Therefore, we introduced 35S:ASL11–GFP to cockscomb via Agrobacterium tumefaciens. ASYMMETRIC LEAVES2-LIKE11 (ASL11) gene of Arabidopsis is a member of the ASYMMETRIC LEAVES2 (AS2)/LATERAL ORGAN BOUNDARIES (LOB) domain gene family, and its function is largely unclear. By confocal laser scanning microscopy, we found that in most over 35S:ASL11–GFP cockscomb plants, ASL11–GFP fusion protein was in discrete nuclear location. These results indicate that the T-DNA contains within the construct inserted into the host chromosomes in an integral form, and also suggest that ASL11 might be a nuclear protein and function as a potential transcription factor. Moreover, SAMs of the over 35S:ASL11–GFP plants show needle-like patterns that lack organ primordial; suggesting ASL11 might be involved in sustaining indeterminate cell fate of SAMs.
Similar content being viewed by others
References
Sinha NR, Williams RE, Hake S (1993) Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7:787–795
de Kathen A, Jacobsen HJ (1995) Cell competence for Agrobacterium-mediated DNA transfer in Pisum sativum L. Transgenic Res 4:184–191
Schrammeijer B, Sijmons PC, Elzen PJM, van den Hoekema A (1990) Meristem transformation of sunflower via Agrobacterium. Plant Cell Rep 9:55–60
Ulian EC, Smith RH, Gould JH, McKnight TD (1988) Transformation of plants via the shoot apex. In Vitro Cell Dev Biol 24:951–954
Gould J, Banister S, Haseganwa O, Fakima M, Smith RH (1991) Regeneration of Gossypium hirsutum and G. barbadense from shoot apex tissues for transformation. Plant Cell Rep 10:12–16
Schlappi M, Hohn B (1992) Competence of immature maize embryos for Agrobacterium-mediated gene transfer. Plant Cell 4:7–16
Escudero J, Neuhaus G, Schlappi M, Hohn B (1996) T-DNA transfer in meristematic cells of maize provided with intracellular Agrobacterium. Plant J 10:356–360
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282
Potrykus I (1990) Gene transfer to cereals: assessment and perspectives. Physiol Plant 79:125–134
Zambryski PC (1992) Chronicles from the Agrobacterium plant cell DNA transfer story. Annu Rev Plant Physiol Plant Mol Biol 43:465–490
Medford JI (1992) Vegetative apical meristems. Plant Cell 4:1029–1039
Sangwan RS, Bourgeois Y, Brown S, Vasseur G, Brigitte SN (1992) Characterization of competent cells and early events of Agrobacterium-mediated genetic transformation in Arabidopsis thaliana. Planta 188:439–456
Meng LS, Ding WQ, Hu X, Wang CY (2009) Transformation of PttKN1 gene to cockscomb. Acta Physiol Plant 31:683–691
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
Nakazawa M, Ichikawa T, Ishikawa A, Kobayashi H, Tsuhara Y, Kawashima M, Suzuki K, Muto S, Matsui M (2003) Activation tagging, a novel tool to dissect the functions of a gene family. Plant J 34:741–750
Chalfun-Junior A, Franken J, Mes JJ, Marsch-Martinez N, Pereira A, Angenent GC (2005) ASYMMETRIC LEAVES2-LIKE1 gene, a member of the AS2/LOB family, controls proximaldistal patterning in Arabidopsis petals. Plant Mol Biol 57:559–575
Ori N, Eshed Y, Chuck G, Bowman JL, Hake S (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127:5523–5532
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
Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965
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
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
Waites R, Selvadurai HRN, 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
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
Timmermans MCP, 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
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
Bortiri E, Chuck G, Vollbrecht E, Rocheford T, Martienssen R, Hake S (2006) ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18:574–585
Evans MM (2007) The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell 19:46–62
Borghi L, Bureau M, Simon R (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19:1795–1808
Ni RJ, Shen Z, Yang CP, Wu YD, Bi YD, Wang BC (2010) Identification of low abundance polyA-binding proteins in Arabidopsis chloroplast using polyA-affinity column. Mol Biol Rep 37:637–641
Zhu B, Xiong AS, Peng RH, Xu J, Jin XF, Meng XR, Yao QH (2010) Over-expression of ThpI from Choristoneura fumiferana enhances tolerance to cold in Arabidopsis. Mol Biol Rep 37:961–966
Liu C, Zhang L, Sun J, Luo Y, Wang MB, Fan YL, Wang L (2010) a simple artificial microRNA vector based on ath-miR169d precursor from Arabidopsis. Mol Biol Rep 37:903–909
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
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
Guo XH, Deng KQ, Wang J, Yu DS, Zhao Q, Liu XM (2010) Mutational analysis of Arabidopsis PP2CA2 involved in abscisic acid signal transduction. Mol Biol Rep 37:763–769
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: B-Glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMOB J 6:3901–3907
Abdollahi MR, Corral-Mart′ınez P, Mousavi A, Salmanian AH, Moieni A, Segui-Simarro JM (2009) An efficient method for transformation of pre-androgenic, isolated Brassica napus microspores involving microprojectil bombardment and Agrobacterium-mediated transformation. Acta Physiol Plant 31:1313–1317
Yasmeen A (2009) an improved protocol for the regeneration and transformation of tomato (cv Rio Grande). Acta Physiol Plant 31:1271–1277
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
Fiuk A, Rybczynski JJ (2008) Morphogenic capability of Gentiana kurroo Royle seedling and leaf explants. Acta Physiol Plant 30:157–166
Meng LS, Sun XD, Li F, Liu HL, Feng ZH, Zhu J (2010) Modification of flowers and leaves in Cockscomb (Celosia cristata) ectopically expressing Arabidopsis ASYMMERTIC LEAVES2-LIKE38 (ASL38/LBD41) gene. Acta Physiol Plant 32:315–324
An G (1985) High efficiency transformation of cultured tobacco cells. Plant Physiol 79:568–570
Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant Physiol 38:179–204
Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altmann T, Redei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171–182
Yamamoto R, Demura T, Fukuda H (1997) Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells. Plant Cell Physiol 38:980–983
Choe S, Dilkes BP, Gregory BD, Ross AS, Yuan H, Noguchi T, Fujioka S, Takatsuto S et al (1999) The Arabidopsis dwarf mutant is defective in the conversion of 2, 4-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiol 119:897–907
Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5:379–391
Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429:873–878
Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842–845
Cao Z, Jia Z, Liu Y, Wang M, Zhao J, Zheng J, Wang G (2010) Constitutive expression of ZmsHSP in Arabidopsis enhances their cytokinin sensitivity. Mol Biol Rep 37:1089–1097
Schmidt F, Marnef A, Cheung MK, Wilson I, Hancock J, Staiger D, Ladomery M (2010) A proteomic analysis of oligo(dT)-bound mRNP containing oxidative stress-induced Arabidopsis thaliana RNA-binding proteins ATGRP7 and ATGRP8. Mol Biol Rep 37:839–845
Turner S, Gallois P, Brown D (2007) Tracheary element differentiation. Annu Rev Plant Biol 58:407–433
Geier T, Sangwan RS (1996) Histology and chimeral segregation reveal cell-specific differences in the competence for shoot regeneration and Agrobacterium-mediated transformation in Kohleria internode explants. Plant Cell Rep 15:386–390
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 lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478
Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396
Naito T, Yamashino T, Kiba T, Koizumi N, Kojima M, Sakakibara H, Mizuno T (2007) A link between cytokinin and ASL9 (ASYMMETRIC LEAVES 2 LIKE 9) that belongs to the AS2/LOB (LATERAL ORGAN BOUNDARIES) family genes in Arabidopsis thaliana. Biosci Biotechnol Biochem 71:1269–1278
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
Guo M, Thomas J, Collins G, Timmermansa MCP (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20:48–58
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
Theodoris G, Inada N, Freeling M (2003) Conservation and molecular dissection of ROUGH SHEATH2 and ASYMMETRIC LEAVES1 function in leaf development. Proc Natl Acad Sci USA 100:6837–6842
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sun, SB., Meng, LS., Sun, XD. et al. 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 (2010). https://doi.org/10.1007/s11033-010-0056-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-010-0056-8