Plant Molecular Biology

, Volume 62, Issue 6, pp 913–925 | Cite as

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

Article

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 ArabidopsisKANADI1 (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.

Keywords

FEATHERED KANADI Ipomoea nil Japanese morning glory En/Spm Tpn1 family 

Supplementary material

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedCrossRefGoogle Scholar
  2. Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141PubMedCrossRefGoogle Scholar
  3. 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 126:2387–2396PubMedGoogle Scholar
  4. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418PubMedGoogle Scholar
  5. 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 121:2057–2067Google Scholar
  6. 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 13:1768–1774PubMedCrossRefGoogle Scholar
  7. Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209PubMedCrossRefGoogle Scholar
  8. Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260PubMedCrossRefGoogle Scholar
  9. 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 131:2997–3006PubMedCrossRefGoogle Scholar
  10. Fletcher JC (2001) The ULTRAPETALA gene controls shoot and floral meristem size in Arabidopsis. Development 128:1323–1333PubMedGoogle Scholar
  11. 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 38:754–758PubMedGoogle Scholar
  12. 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 18:143–149CrossRefGoogle Scholar
  13. Fukada-Tanaka S, Inagaki Y, Yamaguchi T, Saito N, Iida S (2000) Colour-enhancing protein in blue petals. Nature 407:581PubMedCrossRefGoogle Scholar
  14. Glover B, Martin C (1998) The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80:778–784CrossRefGoogle Scholar
  15. Golz JF, Roccaro M, Kuzoff R, Hudson A (2004) GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131:3661–3670PubMedCrossRefGoogle Scholar
  16. Hagiwara T (1956) Genes and chromosome maps in the Japanese morning glory. Bull Res Coll Agr Vet Sci Nihon Univ 5:34–56Google Scholar
  17. Hawker NP, Bowman JL (2004) Roles for Class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol 135:2261–2270PubMedCrossRefGoogle Scholar
  18. 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 38:970–974PubMedGoogle Scholar
  19. Hudson A (2001) Plant development: two sides to organ asymmetry. Curr Biol 11:R756–R758PubMedCrossRefGoogle Scholar
  20. 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 870:265–274PubMedCrossRefGoogle Scholar
  21. 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 38:141–159CrossRefGoogle Scholar
  22. Imai Y (1926) On the rolled leaves and their linked characters in the Japanese morning glory (Pharbitis Nil). Zeitschr f ind Abst -u Verebgsl 40:205–231CrossRefGoogle Scholar
  23. Imai Y (1929) Linkage groups of the Japanese morning glory. Genetics 14:223–255PubMedGoogle Scholar
  24. Imai Y (1931a) Creased flowers of Parbitis Nil. Zeitschr f ind Abst -u Verebgsl 58:248–258CrossRefGoogle Scholar
  25. Imai Y (1931b) Description of the genes found in Pharbitis nil. Genetica 12:297–318CrossRefGoogle Scholar
  26. Imai Y (1933) Linkage studies in Pharbitis nil. Zeitschr f ind Abst -u Verebgsl 66:219–235CrossRefGoogle Scholar
  27. Imai Y (1938) Genetic literature of the Japanese morning glory. Jpn J Genet 14:91–96Google Scholar
  28. 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 6:375–383PubMedCrossRefGoogle Scholar
  29. 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 226:181–188PubMedCrossRefGoogle Scholar
  30. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC (2004a) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88CrossRefGoogle Scholar
  31. Juarez MT, Twigg RW, Timmermans MC (2004b) Specification of adaxial cell fate during maize leaf development. Development 131:4533–4544CrossRefGoogle Scholar
  32. 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 45:933–944PubMedCrossRefGoogle Scholar
  33. Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–84Google Scholar
  34. Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851PubMedGoogle Scholar
  35. Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709PubMedCrossRefGoogle Scholar
  36. McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942PubMedGoogle Scholar
  37. 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 411:709–713PubMedCrossRefGoogle Scholar
  38. 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 36:522–531PubMedCrossRefGoogle Scholar
  39. 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 17:61–76PubMedCrossRefGoogle Scholar
  40. 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 290:2105–2110PubMedCrossRefGoogle Scholar
  41. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  42. 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 13:1079–1088PubMedGoogle Scholar
  43. 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 126:4117–4128PubMedGoogle Scholar
  44. 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 261:447–451PubMedCrossRefGoogle Scholar
  45. 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 121:2723–2735PubMedGoogle Scholar
  46. Waites R, Hudson A (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154Google Scholar
  47. 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 93:779–789PubMedCrossRefGoogle Scholar
  48. 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 18:27–31CrossRefGoogle Scholar
  49. 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 16:500–509PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  1. 1.Department of Biological ScienceGraduate School of Science, Kyushu UniversityHigashi-ku, FukuokaJapan

Personalised recommendations