Abstract
The AGAMOUS (AG)-like gene has been reported to be involved in the formation of the stamens and carpels. The genus Asparagus contains hermaphrodite and dioecious species, and analysis of the AG-like genes in these species may reveal how these different reproductive systems have evolved in this genus. We isolated one AG-like gene, designated AVAG1, from the ornamental hermaphrodite species Asparagus virgatus. Phylogenetic analysis showed that the AVAG1 gene is closely related to HAG1 from Hyacinthus and PeMADS1 from Phalaenopsis. Northern blot analysis showed that AVAG1 transcripts were detected in flower buds, but not in roots, stems or phylloclades. In situ hybridization analyses revealed that the AVAG1 mRNA is expressed specifically in the floral meristem and the developing reproductive organs. Early in flower development, expression of AVAG1 was restricted mainly to the stamens and carpels, with AVAG1 expression in the stamen disappearing at later stages of flower development, although it remained strong in the ovule.
Similar content being viewed by others
References
Ainsworth C, Crossley S, Buchanan-Wollaston V, Thangavelu M, Parker J (1995) Male and female of the dioecious plant sorrel show different patterns of MADS box gene expression. Plant Cell 7:1583–1598
Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum majus. Cell 72:85–95
Caporali E, Spada A, Losa A, Marziani G (2000) The MADS box gene AOM1 is expressed in reproductive meristems and flowers of the dioecious species Asparagus officinalis. Sex Plant Reprod 13:151–156
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37
Demura T, Fukuda H (1996) In situ hybridization to cellular RNA using 35S-labeled cRNA probes. Plant Tissue Cult Lett 13:343–349
Franken AA (1970) Sex characteristic and inheritance of sex in Asparagus (Asparagus officinalis L.). Euphytica 19:277–287
Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002
Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560
Gustafson-Brown C, Savidge B, Yanofsky MF (1994) Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76:131–143
Hardenack S, Ye De, Saedler H, Grant S (1994) Comparison of MADS box gene expression in developing male and female of the dioecious plant white campion. Plant Cell 6:1775–1787
Honda H, Hirai A (1990) A simple and efficient method for identification of hybrids using nonradioactive rDNA as probe. Jpn J Breed 40:339–348
Huijser PW, Klein J, Lönnig W-E, Meijer H, Saedler H, Sommer H (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene SQUAMOSA in Antirrhinum majus. EMBO J:1239–1249
Jack T, Brochman LL, Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697
Kang H-G, Jeon J-S, Lee S, An G (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol 36:1021–1029
Kater MM, Colombo L, Franken J, Busscher M, Masiero S, Van Lookeren CMM, Angenent GC (1998) Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant Cell 10:171–182
Kempin SA, Mandel MA, Yanofsky MF (1993) Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol 103:1041–1046
Kim YS, Lee HS, Lee SH, Yoo OJ, Liu JR (1998) A MADS box gene homologous to AG is expressed in seedlings as well as in flowers of ginseng. Plant Cell Physiol 39:836–845
Kyozuka J, Shimamoto K (2002) Ectopic expression of OsMADS3, a rice ortholog of AGAMOUS, caused a homeotic transformation of lodicules to stamens in transgenic rice plants. Plant Cell Physiol 43:130–135
Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A,B and C genes. Plant Cell Physiol 41:710–718
Lee YO, Kanno A, Kameya T (1997) Phylogenetic relationships in the genus Asparagus based on the restriction enzyme analysis of the chloroplast DNA. Breed Sci 47:375–378
Li QZ, Li XG, Bai SN, Lu WL, Zang XS (2002) Isolation of HAG1 and its regulation by plant hormones during in vitro floral organogenesis in Hyacinthus orientalis L. Planta 215:533–540
Lopez-Dee ZP, Wittich P, Pe E, Rigola D, Del Buono I, Sari-Gorla M, Kater MM, Colombo L (1999) OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet 25:237–244
Losa A, Caporali E, Spada A, Martinelli S, Marziani G (2004) AOM3 and AOM4: two MADS box genes expressed in reproductive structures of Asparagus officinalis. Sex Plant Reprod 16:215-221
Ma H, Yanofsky MF, Meyerowitz EM (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484–495
Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277
Matsunaga S, Isono E, Kejnovsky E, Vyskot B, Dolezel J, Kawano S, Charlesworth D (2003) Duplicative transfer of a MADS box gene to a plant Y chromosome Mol Biol Evol 207:1062–1069
Meguro A, Takumi S, Ogihara Y, Murai K (2003) WAG, a wheat AGAMOUS homolog, is associated with development of pistil-like stamens in alloplasmic wheats. Sex Plant Reprod 15:221–230
Mena M, Ambrose BA, Meeley RB, Briggs SP, Yanofsky MF, Schmidt RJ (1996) Diversification of C-function activity in maize flower development. Science 274:1537–1540
Meyerowitz EM, Bowman JL, Brockman LL, Drews GN, Jack T, Sieburth LE, Weigel D (1991) A genetic and molecular model for flower development in Arabidopsis thaliana. Development 113:157–167
Mizukami Y, Ma H (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71:119–131
Münster T, Pahnke J, Di Rosa A, Kim JT, Martin W, Saedler H, Theissen G (1997) Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc Natl Acad Sci USA 94:2415–2420
Park J-H, Ishikawa Y, Yoshida R, Kanno A, Kameya T (2003) Expression of AODEF, a B-functional MADS-box gene, in stamens and inner tepals of the dioecious species Asparagus officinalis L. Plant Mol Biol 51:867–875
Park J-H, Ishikawa Y, Ochiai T, Kanno A, Kameya T (2004) Two GLOBOSA-like genes are expressed in second and third whorls of homochlamydeous flowers in Asparagus officinalis L. Plant Cell Physiol (in press)
Perrière G, Gouy M (1996) WWW-Query: an on-line retrieval system for biological sequence banks. Biochemie 78:364–369
Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky M (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88
Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky M (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356
Rigola D, Pe ME, Fabrizio C, Me G, Sari-Gorla M (1998) CaMADS1, a MADS box gene expressed in the carpel of hazelnut. Plant Mol Biol 38:1147–1160
Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF (1993) Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5:729–737
Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. Eur J Biochem 229:1–13
Sommer H, Beitran J-P, Huijser PW, Pape H, Lönnig W-E, Saedler H, Schwarz-Sommer Z (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus. EMBO J 9:605–613
Theissen G, Strater T, Fischer A, Saedler H (1995) Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize. Gene 156:155–166
Theissen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516
Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig W-E, Saedler H, Sommer H, Schwarz-Sommer Z (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11:4693–4704
Tzeng T-Y, Chen H-Y, Yang C-H (2002) Ectopic expression of carpel-specific MADS box genes from lily and lisianthus causes similar homeotic conversion of sepal and petal in Arabidopsis. Plant Physiol 130:1827–1836
Yanofsky MF, Ma H, Bowman JL, Drew G, Feldmann K, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346:35–39
Yu D, Kotilainen M, Pöllänen E, Mehto M, Elomaa P, Helariutta Y, Albert VA, Teeri TH (1999) Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant J 17:51–62
Acknowledgements
We wish to thank Professor H. Takahashi and Dr. M. Kamada (Tohoku University, Sendai, Japan) for their help and discussions regarding the in situ experiments. We also thank Dr. T. Ochiai (Tohoku University) for helpful discussions and Mr. H. Tokairin for his collaboration in culturing the plants. We are also grateful to Dr. T. Yamaguchi (Fukukaen Nursery & Bulb Co., Mie, Japan), Dr. K. Sudo (National Institute of Floricultural Science, Tsukuba, Japan) and Dr. T. Sonoda (Fukushima Agricultural Experiment Station, Koriyama, Japan) for providing seeds and/or plants of A. virgatus. This work was supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports Science and Technology, Japan.
Author information
Authors and Affiliations
Corresponding author
Additional information
The nucleotide sequence data of the cDNA reported in this paper has been deposited with the EMBL, GenBank and DDBJ nucleotide sequence databases under the accession number AB125347 (AVAG1)
Rights and permissions
About this article
Cite this article
Yun, PY., Ito, T., Kim, SY. et al. The AVAG1 gene is involved in development of reproductive organs in the ornamental asparagus, Asparagus virgatus . Sex Plant Reprod 17, 1–8 (2004). https://doi.org/10.1007/s00497-004-0212-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00497-004-0212-1