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The FEATHERED gene is required for polarity establishment in lateral organs especially flowers of the Japanese morning glory (I pomoea nil )

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Abstract

Most strains harboring the feathered (fe) mutation in the Japanese morning glory (Ipomoea nil or Pharbitis nil) show deformed phenotypes such as upcurled leaves and separated or tubular petals. These phenotypes seem to be caused by loss of abaxial identity in lateral organs. The FE gene was isolated using the inserted transposon as a tag. An En/Spm-related transposable element, Tpn102, inserted in the fourth intron of the FE gene, was responsible for the fe mutation. FE encodes a GARP transcription factor closely related to Arabidopsis KANADI1 (KAN1), which promotes an abaxial cell fate. Genetic analyses and molecular studies, which showed that all fe mutant strains have the same fe allele despite their phenotypic differences, revealed that fe strains with strong phenotypes have additional mutations enhancing the fe phenotype. These findings and historical records of fe phenotypes suggest that these enhancer mutations were accumulated in the fe background during selection for strong phenotypes. The mutant phenotypes and molecular analysis of fe strains suggest that FE regulates the abaxial identity of lateral organs redundantly with modifier genes, as KAN1 does in Arabidopsis. FE, however, affects flower phenotype even in the single mutant unlike KAN1, moreover, modifier mutations affect flower phenotype only in the fe mutant background, suggesting that FE may play a more crucial role in promotion of abaxial cell fate in flowers of the Japanese morning glory.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396

    PubMed  CAS  Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418

    PubMed  CAS  Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–2067

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209

    Article  PubMed  CAS  Google Scholar 

  • Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Fletcher JC (2001) The ULTRAPETALA gene controls shoot and floral meristem size in Arabidopsis. Development 128:1323–1333

    PubMed  CAS  Google Scholar 

  • Fukada-Tanaka S, Hoshino A, Hisatomi Y, Habu Y, Hasebe M, Iida S (1997) Identification of new chalcone synthase genes for flower pigmentation in the Japanese and common morning glories. Plant Cell Physiol 38:754–758

    PubMed  CAS  Google Scholar 

  • Fukada-Tanaka S, Inagaki Y, Yamaguchi T, Iida S (2001) Simplified transposon display (STD): a new procedure for isolation of a gene tagged by a transposable element belonging to the Tpn1 family in the Japanese morning glory. Plant Biotech 18:143–149

    Article  CAS  Google Scholar 

  • Fukada-Tanaka S, Inagaki Y, Yamaguchi T, Saito N, Iida S (2000) Colour-enhancing protein in blue petals. Nature 407:581

    Article  PubMed  CAS  Google Scholar 

  • Glover B, Martin C (1998) The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80:778–784

    Article  Google Scholar 

  • Golz JF, Roccaro M, Kuzoff R, Hudson A (2004) GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131:3661–3670

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara T (1956) Genes and chromosome maps in the Japanese morning glory. Bull Res Coll Agr Vet Sci Nihon Univ 5:34–56

    Google Scholar 

  • Hawker NP, Bowman JL (2004) Roles for Class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol 135:2261–2270

    Article  PubMed  CAS  Google Scholar 

  • Hoshino A, Abe Y, Saito N, Inagaki Y, Iida S (1997) The gene encoding flavanone 3-hydroxylase is expressed normally in the pale yellow flowers of the Japanese morning glory carrying the speckled mutation which produce neither flavonol nor anthocyanin but accumulate chalcone, aurone and flavanone. Plant Cell Physiol 38:970–974

    PubMed  CAS  Google Scholar 

  • Hudson A (2001) Plant development: two sides to organ asymmetry. Curr Biol 11:R756–R758

    Article  PubMed  CAS  Google Scholar 

  • Iida S, Hoshino A, Johzuka-Hisatomi Y, Habu Y, Inagaki Y (1999) Floricultural traits and transposable elements in the Japanese and common morning glories. Ann N Y Acad Sci 870:265–274

    Article  PubMed  CAS  Google Scholar 

  • Iida S, Morita Y, Choi JD, Park KI, Hoshino A (2004) Genetics and epigenetics in flower pigmentation associated with transposable elements in morning glories. Adv Biophys 38:141–159

    Article  CAS  Google Scholar 

  • Imai Y (1926) On the rolled leaves and their linked characters in the Japanese morning glory (Pharbitis Nil). Zeitschr f ind Abst -u Verebgsl 40:205–231

    Article  Google Scholar 

  • Imai Y (1929) Linkage groups of the Japanese morning glory. Genetics 14:223–255

    PubMed  CAS  Google Scholar 

  • Imai Y (1931a) Creased flowers of Parbitis Nil. Zeitschr f ind Abst -u Verebgsl 58:248–258

    Article  Google Scholar 

  • Imai Y (1931b) Description of the genes found in Pharbitis nil. Genetica 12:297–318

    Article  Google Scholar 

  • Imai Y (1933) Linkage studies in Pharbitis nil. Zeitschr f ind Abst -u Verebgsl 66:219–235

    Article  Google Scholar 

  • Imai Y (1938) Genetic literature of the Japanese morning glory. Jpn J Genet 14:91–96

    Google Scholar 

  • Inagaki Y, Hisatomi Y, Suzuki T, Kasahara K, Iida S (1994) Isolation of a Suppressor-mutator/Enhancer-like transposable element, Tpn1, from Japanese morning glory bearing variegated flowers. Plant Cell 6:375–383

    Article  PubMed  CAS  Google Scholar 

  • Inagaki Y, Johzuka-Hisatomi Y, Mori T, Takahashi S, Hayakawa Y, Peyachoknagul S, Ozeki Y, Iida S (1999) Genomic organization of the genes encoding dihydroflavonol 4-reductase for flower pigmentation in the Japanese and common morning glories. Gene 226:181–188

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Juarez MT, Twigg RW, Timmermans MC (2004b) Specification of adaxial cell fate during maize leaf development. Development 131:4533–4544

    Article  CAS  Google Scholar 

  • Kawasaki S, Nitasaka E (2004) Characterization of Tpn1 family in the Japanese morning glory: En/Spm-related transposable elements capturing host genes. Plant Cell Physiol 45:933–944

    Article  PubMed  CAS  Google Scholar 

  • Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–84

    CAS  Google Scholar 

  • Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851

    PubMed  CAS  Google Scholar 

  • Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709

    Article  PubMed  CAS  Google Scholar 

  • McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nitasaka E (2003) Insertion of an En/Spm-related transposable element into a floral homeotic gene DUPLICATED causes a double flower phenotype in the Japanese morning glory. Plant J 36:522–531

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Takahashi S, Inagaki Y, Satoh H, Hoshino A, Iida S (1999) Capture of a genomic HMG domain sequence by the En/Spm-related transposable element Tpn1 in the Japanese morning glory. Mol Gen Genet 261:447–451

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Waites R, Hudson A (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Williams MH, Vesk M, Mullins MG (1987) Tissue-preparation for scanning electron-microscopy of fruit surfaces—comparison of fresh and cryopreserved specimens and replicas of banana peel. Micron and Microscopica Acta 18:27–31

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank E. Kikuchi and K. Tsuji for providing fe revertant plants, Y. Toh for help with SEM analysis, and S. Iida, T. Tsurimoto, K. Iba and C. Machida for helpful discussions. We also thank National BioResource Project (NBRP; morning glory) for the mutant strains. This study was supported by PRESTO, Japan Science and Technology Corporation, and grants (Nos. 15570007 and Grant-in-Aid for Scientific Research on Priority Areas (C) Genome Science) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Correspondence to Eiji Nitasaka.

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Iwasaki, M., Nitasaka, E. The FEATHERED gene is required for polarity establishment in lateral organs especially flowers of the Japanese morning glory (I pomoea nil ). Plant Mol Biol 62, 913–925 (2006). https://doi.org/10.1007/s11103-006-9066-2

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